Phenotypic and genotypic study of antibiotic-resistant Escherichia coli isolates from a wastewater treatment plant in Zulia state, Venezuela.
Estudio fenotípico y genotípico de aislados de Escherichia coli resistentes a antibióticos de una planta de tratamiento de aguas residuales del estado Zulia, Venezuela.
Palabras clave:
genes de resistencia, E. coli, aguas residuales, filogrupos
Resumen
La resistencia bacteriana a antibióticos es un problema de salud global y las plantas de tratamiento pueden jugar un papel en su diseminación. En este trabajo caracterizamos, mediante PCR y transformación de plásmidos, la resistencia a antibióticos y los grupos filogenéticos de Escherichia coli aislada de una planta de tratamiento en el estado Zulia, Venezuela. Se analizaron 36 aislados bacterianos, de los cuales 27 resultaron resistentes por difusión en disco principalmente a tetraciclina y sulfisoxazol, pero también a trimetoprim, cloranfenicol y ampicilina. Los genes tetA, sul2, floR y blaTEM se encontraron comúnmente en los aislados resistentes y fueron en la mayoría de los casos transferibles; adicionalmente se detectaron los genes dfrA12, tetB, sul3, sul1 y aadA2. El gen de integrasa intI1 se detectó en la mayoría de los aislados multiresistentes. Estos resultados sugieren que E. coli en la planta de tratamiento es un reservorio de genes de resistencia a antibióticos, lo que significa una amenaza potencial para la salud. Adicionalmente predominó el filogrupo C, lo que es inusual y podría deberse a una adaptación de este a las condiciones ambientales o podría ser el mayoritario en el influente.
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Citas
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Grehs BWN, Linton MAO, Clasen B, de Oliveira Silveira A, Carissimi E. Antibiotic resistance in wastewater treatment plants: understanding the problem and future perspectives. Arch Microbiol 2021; 203(3): 1009-1020.
American Public Health Association. Standard Methods For the Examination of Water and Wastewater. 20 th Ed. Washington DC: APHA; 2005, p 2215-2218.
Clinical and Laboratory Standards Institute. Performance Standards for Animicrobial Susceptibility testing. Twenty-Fifth Informational Supplement M100-S25. Wayne PA, USA: CLSI; 2015, p 44-50.
Jones CH, Tuckman M, Murphy E, Bradford PA. Identification and sequence of a tet(M) tetracycline resistance determinant homologue in clinical isolates of Escherichia coli. J Bacteriol 2006; 188(20):7151-7164.
Van TT, Chin J, Chapman T, Tran LT, Coloe PJ. Safety of raw meat and shellfish in Vietnam: an analysis of Escherichia coli isolations for antibiotic resistance and virulence genes. Int J Food Microbiol 2008; 124(3):217-223.
Lanz R, Kuhnert P, Boerlin P. Antimicrobial resistance and resistance gene determinants in clinical Escherichia coli from different animal species in Switzerland. Vet Microbiol 2003; 91(1):73-84.
Perreten V, Boerlin P. A new sulfonamide resistance gene (sul3) in Escherichia coli is widespread in the pig population of Switzerland. Antimicrob Agents Chemother 2003; 47(3):1169-1172.
Fang H, Ataker F, Hedin G, Dornbusch K. Molecular epidemiology of extended-spectrum beta-lactamases among Escherichia coli isolates collected in a Swedish hospital and its associated health care facilities from 2001 to 2006. J Clin Microbiol 2008;46(2):707-712.
Guerra B, Soto SM, Arguelles JM, Mendoza MC. Multidrug resistance is mediated by large plasmids carrying a class 1 integron in the emergent Salmonella enterica serotype [4,5,12:i:-]. Antimicrob Agents Chemother 2001; 45(4):1305-1308.
Grape M, Motakefi A, Pavuluri S, Kahlmeter G. Standard and real-time multiplex PCR methods for detection of trimethoprim resistance dfr genes in large collections of bacteria. Clin Microbiol Infect 2007; 13(11):1112-1118.
Moura A, Henriques I, Ribeiro R, Correia A. Prevalence and characterization of integrons from bacteria isolated from a slaughterhouse wastewater treatment plant. J Antimicrob Chemother 2007; 60(6):1243-1250.
Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 2013; 5(1):58-65.
Versalovic J, Koeuth T, and Lupski JR. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 1991; 19(24): 6823–6831.
Sabat G, Rose P, Hickey W.J and Harkin M. Selective and sensitive methods for PCR amplification of Escherichia coli 16S rRNA genes in Soil. Appl Environ Microbiol 2000; 66 (2): 844-849.
McDaniels AE, Rice EW, Reyes AL, Johnson CH, Haugland RA, Stelma GN Jr. Confirmational identification of Escherichia coli, a comparison of genotypic and phenotypic assays for glutamate decarboxylase and beta-D-glucuronidase. Appl Environ Microbiol 1996; 62(9):3350-3354.
Ogura Y, Ueda T, Nukazawa K, Hiroki H, Xie H, Arimizu Y. The level of antimicrobial resistance of sewage isolates is higher than that of river isolates in different Escherichia coli lineages. Sci Rep 2020;10(1):17880.
Paulshus E, Kuhn I, Mollby R, Colque P, O’Sullivan K, Midtvedt T, Lingaas E, Holmstad R, Sørum H. Diversity and antibiotic resistance among Escherichia coli populations in hospital and community wastewater compared to wastewater at the receiving urban treatment plant. Water Res 2019; 161:232-241.
Blaak H, Lynch G, Italiaander R, Hamid- jaja RA, Schets FM, de Roda Husman AM. Multidrug-resistant and extended spectrum beta-lactamase-producing Escherichia coli in Dutch surface water and wastewater. PLoS One 2015; 10(6):e0127752.
Figueira V, Serra E, Manaia CM. Differential patterns of antimicrobial resistance in population subsets of Escherichia coli isolated from waste and surface waters. Sci Total Environ 2011; 409(6):1017-1023.
Zambrano J L, Botero L, Cavazza M E, Avila M. Resistencia a antimicrobianos y presencia de plásmidos en cepas de Escherichia coli aisladas de aguas residuales crudas y tratadas por lagunas de estabilización con fines de reuso en agricultura. Rev Soc Ven Microbiol 2002; 22( 1 ): 44-50
Martínez, RE, Villalobos LB. Susceptbilidad antimicrobiana de cepas de Escherichia coli aisladas de alimentos y aguas residuales en Cumaná, Venezuela. SABER 2008; 20(2), 172-176.
World Health Organization. Critically important antimicrobials for human medicine. 6th revision. Geneva: WHO; 2019, p 14-15.
Nji E, Kazibwe J, Hambridge T, Joko CA, Larbi AA, Damptey LAO, Nkansa Gyamfi NA, Stålsby Lundborg C, Lien TQ. High prevalence of antibiotic resistance in commensal Escherichia coli from healthy human sources in community settings. Sci Rep 2021; 11(1):3372.
Raven KE, Ludden C, Gouliouris T, Blane B, Naydenova P, Brown NM, Parkhill J, Peacock SJ. Genomic surveillance of Escherichia coli in municipal wastewater treatment plants as an indicator of clinically relevant pathogens and their resistance genes. Microb Genom 2019; 5(5): e000267.
Turolla A, Cattaneo M, Marazzi F, Mezzanotte V, Antonelli M. Antibiotic resistant bacteria in urban sewage: Role of full-scale wastewater treatment plants on environmental spreading. Chemosphere 2018;191:761-769.
Osinska A, Korzeniewska E, Harnisz M, Niestepski S. The prevalence and characterization of antibiotic-resistant and virulent Escherichia coli strains in the municipal wastewater system and their environmental fate. Sci Total Environ 2017; 577:367-375.
Souque C, Escudero JA, MacLean RC. Integron activity accelerates the evolution of antibiotic resistance. Elife 2021; 10: e62474.
Smyth C, O’Flaherty A, Walsh F, Do TT. Antibiotic resistant and extended- spectrum β-lactamase producing faecal coliforms in wastewater treatment plant effluent. Environ Pollut 2020; 262:114244.
Wang Y, Batra A, Schulenburg H, Dagan T. Gene sharing among plasmids and chromosomes reveals barriers for antibiotic resistance gene transfer. Philos Trans R Soc Lond B Biol Sci 2022; 377(1842):20200467.
Hansen KH, Andreasen MR, Pedersen MS, Westh H, Jelsbak L, Schonning K. Resistance to piperacillin/tazobactam in Escherichia coli resulting from extensive IS26-associated gene amplification of bla- TEM-1. J Antimicrob Chemother 2019; 74(11):3179-3183.
Sunde M, Sorum H. Self-transmissible multidrug resistance plasmids in Escherichia coli of the normal intestinal flora of healthy swine. Microb Drug Resist 2001; 7(2):191-196.
Jiang H, Cheng H, Liang Y, Yu S, Yu T, Fang J, Zhu C. Diverse mobile genetic elements and conjugal transferability of sulfonamide resistance genes (sul1, sul2, and sul3) in Escherichia coli isolates from penaeus vannamei and pork from large markets in Zhejiang, China. Front Microbiol 2019;10:1787.
Meunier D, Jouy E, Lazizzera C, Doublet B, Kobisch M, Cloeckaert A, Madec JY. Plasmid-borne florfenicol and ceftiofur resistance encoded by the floR and blaCMY-2 genes in Escherichia coli isolates from diseased cattle in France. J Med Microbiol 2010; 59(Pt 4):467-471.
Yu HS, Lee JC, Kang HY, Jeong YS, Lee EY, Choi CH, Tae SH, Lee YC, Seol SY, Cho DT. Prevalence of dfr genes associated with integrons and dissemination of dfrA17 among urinary isolates of Escherichia coli in Korea. J Antimicrob Chemother 2004; 53(3):445-450.
Clermont O, Olier M, Hoede C, Diancourt L, Brisse S, Keroudean M, Glodt J, Picard B, Oswald E, Denamur E. Animal and human pathogenic Escherichia coli strains share common genetic backgrounds. Infect Genet Evol 2011; 11(3):654-662.
Biggel M, Xavier BB, Johnson JR, Nielsen KL, Frimodt-Møller N, Matheeussen V, Goossens H, Moons P, Van Puyvelde S. Horizontally acquired papGII-containing pathogenicity islands underlie the emergence of invasive uropathogenic Escherichia coli lineages. Nat Commun 2020; 11(1):5968.
Jafari E, Oloomi M, Bouzari S. Characterization of antimicrobial susceptibility, extended-spectrum β-lactamase genes and phylogenetic groups of Shigatoxin producing Escherichia coli isolated from patients with diarrhea in Iran. Ann Clin Microbiol Antimicrob 2021; 20(1), 24.
Citterio B, Andreoni F, Simoni S, Carloni E, Magnani M, Mangiaterra G, Cedraro N, Biavasco F, Vignaroli C. Plasmid replicon typing of antibiotic resistant Escherichia coli from clams and marine sediments. Front Microbiol 2020; 11:1101.
Sabaté M, Prats G, Moreno E, Ballesté E, Blanch AR, Andreu A. Virulence and anti- microbial resistance profiles among Escherichia coli strains isolated from human and animal wastewater. Res Microbiol 2008; 159(4):288-93.
Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000; 66(10):4555-4558.
Tenaillon O, Skurnik D, Picard B, Denamur E. The population genetics of commensal Escherichia coli. Nat Rev Microbiol 2010; 8(3):207-217.
Lescat M, Clermont O, Woerther PL, Glodt J, Dion S, Skurnik D, Djossou F, Dupont C, Perroz G, Picard B, Catzeflis F, Andremont A, Denamur E. Commensal Escherichia coli strains in Guiana reveal a high genetic diversity with host-dependant population structure. Environ Microbiol Rep 2013; 5(1):49-57.
Petit F, Clermont O, Delannoy S, Servais P, Gourmelon M, Fach P, Oberlé K, Fournier M, Denamur E, Berthe T. Change in the structure of Escherichia coli population and the pattern of virulence genes along a rural aquatic continuum. Front Microbiol 2017; 8:609.
Touchon M, Perrin A, de Sousa JAM, Vangchhia B, Burn S, O’Brien CL, Denamur E, Gordon D, Rocha EP. Phylogenetic background and habitat drive the genetic diversification of Escherichia coli. PLoS Genet 2020 ;16(6):e1008866.
Zhi S, Banting G, Li Q, Edge TA, Topp E, Sokurenko M, Scott C, Braithwaite S, Ruecker NJ, Yasui Y, McAllister T, Chui L, Neumann NF. Evidence of naturalized stress-tolerant strains of Escherichia coli in Municipal wastewater treatment plants. Appl Environ Microbiol 2016; 82(18):5505-
5518.
Grehs BWN, Linton MAO, Clasen B, de Oliveira Silveira A, Carissimi E. Antibiotic resistance in wastewater treatment plants: understanding the problem and future perspectives. Arch Microbiol 2021; 203(3): 1009-1020.
American Public Health Association. Standard Methods For the Examination of Water and Wastewater. 20 th Ed. Washington DC: APHA; 2005, p 2215-2218.
Clinical and Laboratory Standards Institute. Performance Standards for Animicrobial Susceptibility testing. Twenty-Fifth Informational Supplement M100-S25. Wayne PA, USA: CLSI; 2015, p 44-50.
Jones CH, Tuckman M, Murphy E, Bradford PA. Identification and sequence of a tet(M) tetracycline resistance determinant homologue in clinical isolates of Escherichia coli. J Bacteriol 2006; 188(20):7151-7164.
Van TT, Chin J, Chapman T, Tran LT, Coloe PJ. Safety of raw meat and shellfish in Vietnam: an analysis of Escherichia coli isolations for antibiotic resistance and virulence genes. Int J Food Microbiol 2008; 124(3):217-223.
Lanz R, Kuhnert P, Boerlin P. Antimicrobial resistance and resistance gene determinants in clinical Escherichia coli from different animal species in Switzerland. Vet Microbiol 2003; 91(1):73-84.
Perreten V, Boerlin P. A new sulfonamide resistance gene (sul3) in Escherichia coli is widespread in the pig population of Switzerland. Antimicrob Agents Chemother 2003; 47(3):1169-1172.
Fang H, Ataker F, Hedin G, Dornbusch K. Molecular epidemiology of extended-spectrum beta-lactamases among Escherichia coli isolates collected in a Swedish hospital and its associated health care facilities from 2001 to 2006. J Clin Microbiol 2008;46(2):707-712.
Guerra B, Soto SM, Arguelles JM, Mendoza MC. Multidrug resistance is mediated by large plasmids carrying a class 1 integron in the emergent Salmonella enterica serotype [4,5,12:i:-]. Antimicrob Agents Chemother 2001; 45(4):1305-1308.
Grape M, Motakefi A, Pavuluri S, Kahlmeter G. Standard and real-time multiplex PCR methods for detection of trimethoprim resistance dfr genes in large collections of bacteria. Clin Microbiol Infect 2007; 13(11):1112-1118.
Moura A, Henriques I, Ribeiro R, Correia A. Prevalence and characterization of integrons from bacteria isolated from a slaughterhouse wastewater treatment plant. J Antimicrob Chemother 2007; 60(6):1243-1250.
Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 2013; 5(1):58-65.
Versalovic J, Koeuth T, and Lupski JR. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 1991; 19(24): 6823–6831.
Sabat G, Rose P, Hickey W.J and Harkin M. Selective and sensitive methods for PCR amplification of Escherichia coli 16S rRNA genes in Soil. Appl Environ Microbiol 2000; 66 (2): 844-849.
McDaniels AE, Rice EW, Reyes AL, Johnson CH, Haugland RA, Stelma GN Jr. Confirmational identification of Escherichia coli, a comparison of genotypic and phenotypic assays for glutamate decarboxylase and beta-D-glucuronidase. Appl Environ Microbiol 1996; 62(9):3350-3354.
Ogura Y, Ueda T, Nukazawa K, Hiroki H, Xie H, Arimizu Y. The level of antimicrobial resistance of sewage isolates is higher than that of river isolates in different Escherichia coli lineages. Sci Rep 2020;10(1):17880.
Paulshus E, Kuhn I, Mollby R, Colque P, O’Sullivan K, Midtvedt T, Lingaas E, Holmstad R, Sørum H. Diversity and antibiotic resistance among Escherichia coli populations in hospital and community wastewater compared to wastewater at the receiving urban treatment plant. Water Res 2019; 161:232-241.
Blaak H, Lynch G, Italiaander R, Hamid- jaja RA, Schets FM, de Roda Husman AM. Multidrug-resistant and extended spectrum beta-lactamase-producing Escherichia coli in Dutch surface water and wastewater. PLoS One 2015; 10(6):e0127752.
Figueira V, Serra E, Manaia CM. Differential patterns of antimicrobial resistance in population subsets of Escherichia coli isolated from waste and surface waters. Sci Total Environ 2011; 409(6):1017-1023.
Zambrano J L, Botero L, Cavazza M E, Avila M. Resistencia a antimicrobianos y presencia de plásmidos en cepas de Escherichia coli aisladas de aguas residuales crudas y tratadas por lagunas de estabilización con fines de reuso en agricultura. Rev Soc Ven Microbiol 2002; 22( 1 ): 44-50
Martínez, RE, Villalobos LB. Susceptbilidad antimicrobiana de cepas de Escherichia coli aisladas de alimentos y aguas residuales en Cumaná, Venezuela. SABER 2008; 20(2), 172-176.
World Health Organization. Critically important antimicrobials for human medicine. 6th revision. Geneva: WHO; 2019, p 14-15.
Nji E, Kazibwe J, Hambridge T, Joko CA, Larbi AA, Damptey LAO, Nkansa Gyamfi NA, Stålsby Lundborg C, Lien TQ. High prevalence of antibiotic resistance in commensal Escherichia coli from healthy human sources in community settings. Sci Rep 2021; 11(1):3372.
Raven KE, Ludden C, Gouliouris T, Blane B, Naydenova P, Brown NM, Parkhill J, Peacock SJ. Genomic surveillance of Escherichia coli in municipal wastewater treatment plants as an indicator of clinically relevant pathogens and their resistance genes. Microb Genom 2019; 5(5): e000267.
Turolla A, Cattaneo M, Marazzi F, Mezzanotte V, Antonelli M. Antibiotic resistant bacteria in urban sewage: Role of full-scale wastewater treatment plants on environmental spreading. Chemosphere 2018;191:761-769.
Osinska A, Korzeniewska E, Harnisz M, Niestepski S. The prevalence and characterization of antibiotic-resistant and virulent Escherichia coli strains in the municipal wastewater system and their environmental fate. Sci Total Environ 2017; 577:367-375.
Souque C, Escudero JA, MacLean RC. Integron activity accelerates the evolution of antibiotic resistance. Elife 2021; 10: e62474.
Smyth C, O’Flaherty A, Walsh F, Do TT. Antibiotic resistant and extended- spectrum β-lactamase producing faecal coliforms in wastewater treatment plant effluent. Environ Pollut 2020; 262:114244.
Wang Y, Batra A, Schulenburg H, Dagan T. Gene sharing among plasmids and chromosomes reveals barriers for antibiotic resistance gene transfer. Philos Trans R Soc Lond B Biol Sci 2022; 377(1842):20200467.
Hansen KH, Andreasen MR, Pedersen MS, Westh H, Jelsbak L, Schonning K. Resistance to piperacillin/tazobactam in Escherichia coli resulting from extensive IS26-associated gene amplification of bla- TEM-1. J Antimicrob Chemother 2019; 74(11):3179-3183.
Sunde M, Sorum H. Self-transmissible multidrug resistance plasmids in Escherichia coli of the normal intestinal flora of healthy swine. Microb Drug Resist 2001; 7(2):191-196.
Jiang H, Cheng H, Liang Y, Yu S, Yu T, Fang J, Zhu C. Diverse mobile genetic elements and conjugal transferability of sulfonamide resistance genes (sul1, sul2, and sul3) in Escherichia coli isolates from penaeus vannamei and pork from large markets in Zhejiang, China. Front Microbiol 2019;10:1787.
Meunier D, Jouy E, Lazizzera C, Doublet B, Kobisch M, Cloeckaert A, Madec JY. Plasmid-borne florfenicol and ceftiofur resistance encoded by the floR and blaCMY-2 genes in Escherichia coli isolates from diseased cattle in France. J Med Microbiol 2010; 59(Pt 4):467-471.
Yu HS, Lee JC, Kang HY, Jeong YS, Lee EY, Choi CH, Tae SH, Lee YC, Seol SY, Cho DT. Prevalence of dfr genes associated with integrons and dissemination of dfrA17 among urinary isolates of Escherichia coli in Korea. J Antimicrob Chemother 2004; 53(3):445-450.
Clermont O, Olier M, Hoede C, Diancourt L, Brisse S, Keroudean M, Glodt J, Picard B, Oswald E, Denamur E. Animal and human pathogenic Escherichia coli strains share common genetic backgrounds. Infect Genet Evol 2011; 11(3):654-662.
Biggel M, Xavier BB, Johnson JR, Nielsen KL, Frimodt-Møller N, Matheeussen V, Goossens H, Moons P, Van Puyvelde S. Horizontally acquired papGII-containing pathogenicity islands underlie the emergence of invasive uropathogenic Escherichia coli lineages. Nat Commun 2020; 11(1):5968.
Jafari E, Oloomi M, Bouzari S. Characterization of antimicrobial susceptibility, extended-spectrum β-lactamase genes and phylogenetic groups of Shigatoxin producing Escherichia coli isolated from patients with diarrhea in Iran. Ann Clin Microbiol Antimicrob 2021; 20(1), 24.
Citterio B, Andreoni F, Simoni S, Carloni E, Magnani M, Mangiaterra G, Cedraro N, Biavasco F, Vignaroli C. Plasmid replicon typing of antibiotic resistant Escherichia coli from clams and marine sediments. Front Microbiol 2020; 11:1101.
Sabaté M, Prats G, Moreno E, Ballesté E, Blanch AR, Andreu A. Virulence and anti- microbial resistance profiles among Escherichia coli strains isolated from human and animal wastewater. Res Microbiol 2008; 159(4):288-93.
Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000; 66(10):4555-4558.
Tenaillon O, Skurnik D, Picard B, Denamur E. The population genetics of commensal Escherichia coli. Nat Rev Microbiol 2010; 8(3):207-217.
Lescat M, Clermont O, Woerther PL, Glodt J, Dion S, Skurnik D, Djossou F, Dupont C, Perroz G, Picard B, Catzeflis F, Andremont A, Denamur E. Commensal Escherichia coli strains in Guiana reveal a high genetic diversity with host-dependant population structure. Environ Microbiol Rep 2013; 5(1):49-57.
Petit F, Clermont O, Delannoy S, Servais P, Gourmelon M, Fach P, Oberlé K, Fournier M, Denamur E, Berthe T. Change in the structure of Escherichia coli population and the pattern of virulence genes along a rural aquatic continuum. Front Microbiol 2017; 8:609.
Touchon M, Perrin A, de Sousa JAM, Vangchhia B, Burn S, O’Brien CL, Denamur E, Gordon D, Rocha EP. Phylogenetic background and habitat drive the genetic diversification of Escherichia coli. PLoS Genet 2020 ;16(6):e1008866.
Zhi S, Banting G, Li Q, Edge TA, Topp E, Sokurenko M, Scott C, Braithwaite S, Ruecker NJ, Yasui Y, McAllister T, Chui L, Neumann NF. Evidence of naturalized stress-tolerant strains of Escherichia coli in Municipal wastewater treatment plants. Appl Environ Microbiol 2016; 82(18):5505-
5518.
Publicado
2023-08-25
Cómo citar
Guerrero, E., Caraballo, L., Takiff, H., García, D., & Montiel, M. (2023). Phenotypic and genotypic study of antibiotic-resistant Escherichia coli isolates from a wastewater treatment plant in Zulia state, Venezuela.: Estudio fenotípico y genotípico de aislados de Escherichia coli resistentes a antibióticos de una planta de tratamiento de aguas residuales del estado Zulia, Venezuela. Investigación Clínica, 64(3), 296-307. https://doi.org/10.54817/IC.v64n3a3
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