Characterization of beta-lactamase producing Enterobacterales isolated from an urban community wastewater treatment plant in Iran
-
Kamal Hasani
,
Hadi Sadeghi
,
Mehdi Vosoughi
,
Mehran Sardari
,
Meysam Manouchehrifar
,
Mohsen Arzanlou
Abstract
Background and Objectives: he occurrence and characteristics of Extended Spectrum- and AmpC-β-lactamase producing Enterobacterales (ESBL-PE and AmpC-PE) in an urban wastewater treatment plant (WWTP) were investigated.
Materials and Methods: A total of 30 wastewater samples were collected from all sections of WWTP. Enterobacterales were isolated and identified using standard microbiological tests. The antibiotic resistance profile was determined by the Kirby–Bauer disk diffusion method. Phenotypic screening for ESBL-PE and AmpC-PE isolates was performed by double-disk synergy and boronic acid disk potentiation tests, respectively. The isolates were examined for AmpC- and ESBL-encoding genes by PCR and sequencing methods.
Results: Among 146 Enterobacterales isolates, 8.9% (n=13) [ESBL-only; 5.48% (n=8) and ESBL + AmpC; 3.42% (n=5)] were ESBL-producers and 15.75% (n=23) [AmpC-only; 12.33% (n=18) and ESBL + AmpC; 3.42% (n=5)] AmpC-producers. Hafnia spp. with 33.33% (n=1/3) and E. coli with 20.58% (n=7/34) [ESBL-only; 17.64% (n=6/34) and ESBL + AmpC; 2.94% (n=1/34)] were the most common ESBL-producing bacteria. Enterobacter spp. with 37.50% (n=6/16) of isolates were the most common AmpC-producing organisms. ESBL- and/or AmpC-producing isolates were identified in all parts of the WWTP including 80% (n=8/10) of samples taken from effluent. Among ESBL-producing isolates, blaCTX-M, blaTEM, and blaSHV ESBL-encoding genes were found in 61.5% (n=8), 15.3% (n=2), and 7.7% (n=1) of isolates, respectively. All CTX-M-type enzymes belonged to the CTX-M-1 group and CTX-M-15 subgroup. blaTEM and blaSHV type genes belonged to blaTEM-20 and blaHSV-12 subtypes, respectively. blaDHA with 73.9% (n=17/23), and blaCIT and blaFOX with 30.4% (n=7/23) each, were the most common AmpC-encoding genes among AmpC-producing isolates. Overall, 75% of ESBL-producing and 55.5% of AmpC-producing isolates exhibited multi-drug resistance phenotypes. The organisms were most resistant against ampicillin (82.2%) nalidixic acid (43.8%) and cephalexin (41.1%).
Conclusion: ESBL- and AmpC-producing Enterobacterales spp. with diverse genetic resistance backgrounds in WWTP effluent poses a significant risk to public health.
1. Kümmerer K. Antibiotics in the aquatic environment–a review–part I. Chemosphere 2009; 75: 417-434.
2. Zhang X-X, Zhang T, Zhang M, Fang HH, Cheng S-P. Characterization and quantification of class 1 integrons and associated gene cassettes in sewage treatment plants. Appl Microbiol Biotechnol 2009; 82: 1169-1177.
3. Pei R, Cha J, Carlson KH, Pruden A. Response of antibiotic resistance genes (ARG) to biological treatment in dairy lagoon water. Environ Sci Technol 2007; 41: 5108-5113.
4. Capita R, Alonso-Calleja C. Antibiotic-resistant bacteria: a challenge for the food industry. Crit Rev Food Sci Nutr 2013; 53: 11-48.
5. Ojer-Usoz E, González D, García-Jalón I, Vitas AI. High dissemination of extended-spectrum β-lactamase-producing Enterobacteriaceae in effluents from wastewater treatment plants. Water Res 2014; 56: 37-47.
6. Gao P, Munir M, Xagoraraki I. Correlation of tetracycline and sulfonmide antibiotics with corresponding resistance genes and resistant bacteria in a conventional municipal wastewater treatment plant. Sci Total Environ 2012; 421-422: 173-183.
7. Korzeniewska E, Harnisz M. Extended-spectrum beta-lactamase (ESBL)-positive Enterobacteriaceae in municipal sewage and their emission to the environment. J Environ Manage 2013; 128: 904-911.
8. Adeolu M, Alnajar S, Naushad S, S Gupta R. Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’1: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol 2016; 66: 5575-5599.
9. Patrick R M, Rosenthal KS, Pfaller MA. Medical Microbiology (Elsevier Health Sciences) 2015.
10. Chandel DS, Johnson JA, Chaudhry R, Sharma N, Shinkre N, Parida S, et al. Extended-spectrum β-lactamase-producing Gram-negative bacteria causing neonatal sepsis in India in rural and urban settings. J Med Microbiol 2011; 60: 500-507.
11. Arzanlou M, Chai WC, Henrietta V. Intrinsic, adaptive and acquired antimicrobial resistance in Gram-negative bacteria. Essays Biochem 2017; 61: 49-59.
12. Harris PNA, Ferguson JK. Antibiotic therapy for inducible AmpC β-lactamase-producing gram-negative bacilli: what are the alternatives to carbapenems, quinolones and aminoglycosides?. Int J Antimicrob Agents 2012; 40: 297-305.
13. Lukac PJ, Bonomo RA, Logan LK. Extended-spectrum β-lactamase–producing Enterobacteriaceae in children: old foe, emerging threat. Clin Infect Dis 2015; 60: 1389-1397.
14. Castanheira M, Mendes RE, Rhomberg PR, Jones RN. Rapid emergence of blaCTX-M among Enterobacteriaceae in US medical centers: molecular evaluation from the MYSTIC Program (2007). Microb Drug Resist 2008; 14: 211-216.
15. Pitout JD, Laupland KB. Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 2008; 8: 159-166.
16. Lee JH, Bae IK, Hee Lee S. New definitions of extended‐spectrum β‐lactamase conferring worldwide emerging antibiotic resistance. Med Res Rev 2012; 32: 216-232.
17. Cantón R, Novais A, Valverde A, Machado E, Peixe L, Baquero F, et al. Prevalence and spread of ‐spectrum β‐lactamase‐producing Enterobcteriaceae in Europe. Clin Microbiol Infect 2008; 14 Suppl 1: 144-153.
18. Marti E, Huerta B, Rodríguez-Mozaz S, Barceló D, Jofre J, Balcázar JL. Characterization of ciprofloxacin-resistant isolates from a wastewater treatment plant and its receiving river. Water Res 2014; 61: 67-76.
19. Handa D, Pandey A, Asthana AK, Rawat A, Handa S, Thakuria B. Evaluation of phenotypic tests for the detection of AmpC beta-lactamase in clinical isolates of Escherichia coli. Indian J Pathol Microbiol 2013; 56: 135-138.
20. Grover N, Sahni AK, Bhattacharya S. Therapeutic challenges of ESBLS and AmpC beta-lactamase producers in a tertiary care center. Med J Armed Forces India 2013; 69: 4-10.
21. Verdet C, BenzeraraY, Gautier V, Adam O, Ould-Hocine Z, Arlet G. Emergence of DHA-1-producing Klebsiella spp. in the Parisian region: genetic organization of the ampC and ampR genes originating from Morganella morganii. Antimicrob Agents Chemother 2006; 50: 607-17.
22. Pérez-Pérez FJ, Hanson ND. Detection of plthe asmid-mediated AmpC β-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 2002; 40: 2153-2162.
23. Gude MJ, Seral C, Sáenz Y, Cebollada R, Torres C, Castillo FJ. Molecular epidemiology, resistance profiles and clinical features in clinical plasmid-mediated AmpC-producing Enterobacteriaceae. Int J Med Microbiol 2013; 303: 553-557.
24. Tan TY, Ng LS, He J, Koh TH, Hsu LY. Evaluation of screening methods to detect plasmid-mediated AmpC in Escherichia coli, Klebsiella pneumoniae, and Proteus mirabilis. Antimicrob Agents Chemother 2009; 53: 146-149.
25. Mata C, Miró E, Rivera A, Mirelis B, Coll P, Navarro F. Prevalence of acquired AmpC β-lactamases in Enterobacteriaceae lacking inducible chromosomal ampC genes at a Spanish hospital from 1999 to 2007. Clin Microbiol Infect 2010; 16: 472-476.
26. Sóki J, Gonzalez SM, Urbán E, Nagy E, Ayala JA. Molecular analysis of the effector mechanisms of cefoxitin resistance among Bacteroides strains. J Antimicrob Chemother 2011; 66: 2492-2500.
27. Mohammadi M, Fataei E. Comparative life cycle assessment of municipal wastewater treatment systems: lagoon and activated sludge. Caspian J Environ Sci 2019; 17: 327-336.
28. Miyagi K, Hirai I. A survey of extended-spectrum β-lactamase-producing Enterobacteriaceae in environmental water in Okinawa prefecture of Japan and relationship with indicator organisms. Environ Sci Pollut Res Int 2019; 26: 7697-7710.
29. Connie R M, Lehman DC, Manuselis Jr G. Textbook of diagnostic microbiology-e-book (Elsevier Health Sciences). 2018.
30. Clinical, and Laboratory Standards Institute."Performance standards for antimicrobial susceptibility testing." In.: Clinical and Laboratory Standards Institute Wayne, PA. 2023.
31. EUCAST, T. "European Committee on Antimicrobial Susceptibility Testing, Breakpoint tables for interpretation of MICs and zone diameters." In.: European Society of Clinical Microbiology and Infectious Diseases Basel. 2023.
32. Gupta G, Tak V, Mathur P. Detection of AmpC β lactamases in gram-negative bacteria. J Lab Physicians 2014; 6: 1-6.
33. Coudron PE. Inhibitor-based methods for detection of plasmid-mediated AmpC β-lactamases in Klebsiella spp., Escherichia coli, and Proteus mirabilis. J Clin Microbiol 2005; 43: 4163-4167.
34. Ruppé E, Hem S, Lath S, Gautier V, Ariey F, Sarthou JL. CTX-M β-lactamases in Escherichia coli from community-acquired urinary tract infections, Cambodia. Emerg Infect Dis 2009; 15: 741-748.
35. Afzali H, Firoozeh F, Amiri A, Moniri R, Zibaei M. Characterization of CTX-M-type extend-spectrum β-lactamase producing Klebsiella spp. in Kashan, Iran. Jundishapur J Microbiol 2015; 8(10): e27967.
36. Al-Riyami IM, Ahmed M, Al-Busaidi A, Choudri BS. Antibiotics in wastewaters: a review with focus on Oman. Appl Water Sci 2018; 8: 199.
37. Zaatout N, Bouras S, Slimani N. Prevalence of extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae in wastewater: a systematic review and meta-analysis. J Water Health 2021; 19: 705-723.
38. Raven KE, Ludden C, Gouliouris T, Blane B, Naydenova P, Brown NM. 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.
39. Habibzadeh N, Peeri Doghaheh H, Manouchehri Far M, Alimohammadi Asl H, Iranpour S, Arzanlou M. Fecal carriage of Extended-Spectrum β-Lactamases and pAmpC producing Enterobacterales in an Iranian community: prevalence, risk factors, molecular epidemiology, and antibiotic resistance. Microb Drug Resist 2022; 28: 921-934.
40. Röderová M, Sedláková MH, Pudová V, Hricová K, Silová R, Imwensi PEO. Occurrence of bacteria producing broad-spectrum beta-lactamases and qnr genes in hospital and urban wastewater samples. New Microbiol 2016; 39: 124-133.
41. Fadare FT, Okoh AI. The Abundance of genes encoding ESBL, pAmpC and Non-β-Lactam resistance in multidrug-resistant Enterobacteriaceae recovered from wastewater effluents. Front Environ Sci 2021; 9: 711950.
42. Korzeniewska E, Harnisz M. Beta-lactamase-producing Enterobacteriaceae in hospital effluents. J Environ Manage 2013; 123: 1-7.
43. Lenart-Boroń AM, Kulik K, Jelonkiewicz E. Antimicrobial resistance and ESBL genes in E. coli isolated in proximity to a sewage treatment plant. J Environ Sci Health A Tox Hazard Subst Environ Eng 2020; 55: 1571-15800.
44. Stoppe NdC, Silva JS, Carlos C, Sato MIZ, Saraiva AM, Ottoboni LMM, et al. Worldwide phylogenetic group patterns of Escherichia coli from commensal human and wastewater treatment plant isolates. Front Microbiol 2017; 8: 2512.
45. Amador PP, Fernandes RM, Prudêncio MC, Barreto MP, Duarte IM. Antibiotic resistance in wastewater: Occurrence and fate of Enterobacteriaceae producers of Class A and Class C β-lactamases. J Environ Sci Health A Tox Hazard Subst Environ Eng 2015; 50: 26-39.
46. Haller L, Chen H, Ng C, Le TH, Koh, TH, Barkham T. Occurrence and characteristics of extended-spectrum β-lactamase-and carbapenemase-producing bacteria from hospital effluents in Singapore. Sci Total Environ 2018; 615: 1119-1125.
47. Tokajian S, Moghnieh R, Salloum T, Arabaghian H, Alousi S, Moussa J. Extended-spectrum β-lactamase-producing Escherichia coli in wastewaters and refugee camp in Lebanon. Future Microbiol 2018; 13: 81-95.
48. Blaak H, Lynch G, Italiaander R, Hamidjaja RA, Schets FM, De Husman AMR. Multidrug-resistant and extended spectrum beta-lactamase-producing Escherichia coli in Dutch surface water and wastewater. PLoS One 2015; 10(6): e0127752.
49. Diallo AA, Brugère H, Kérourédan M, Dupouy V, Toutain PL, Bousquet-Mélou A, et al. Persistence and prevalence of pathogenic and extended-spectrum beta-lactamase-producing Escherichia coli in municipal wastewater treatment plant receiving slaughterhouse wastewater. Water Res 2013; 47: 4719-4729.
2. Zhang X-X, Zhang T, Zhang M, Fang HH, Cheng S-P. Characterization and quantification of class 1 integrons and associated gene cassettes in sewage treatment plants. Appl Microbiol Biotechnol 2009; 82: 1169-1177.
3. Pei R, Cha J, Carlson KH, Pruden A. Response of antibiotic resistance genes (ARG) to biological treatment in dairy lagoon water. Environ Sci Technol 2007; 41: 5108-5113.
4. Capita R, Alonso-Calleja C. Antibiotic-resistant bacteria: a challenge for the food industry. Crit Rev Food Sci Nutr 2013; 53: 11-48.
5. Ojer-Usoz E, González D, García-Jalón I, Vitas AI. High dissemination of extended-spectrum β-lactamase-producing Enterobacteriaceae in effluents from wastewater treatment plants. Water Res 2014; 56: 37-47.
6. Gao P, Munir M, Xagoraraki I. Correlation of tetracycline and sulfonmide antibiotics with corresponding resistance genes and resistant bacteria in a conventional municipal wastewater treatment plant. Sci Total Environ 2012; 421-422: 173-183.
7. Korzeniewska E, Harnisz M. Extended-spectrum beta-lactamase (ESBL)-positive Enterobacteriaceae in municipal sewage and their emission to the environment. J Environ Manage 2013; 128: 904-911.
8. Adeolu M, Alnajar S, Naushad S, S Gupta R. Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’1: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol 2016; 66: 5575-5599.
9. Patrick R M, Rosenthal KS, Pfaller MA. Medical Microbiology (Elsevier Health Sciences) 2015.
10. Chandel DS, Johnson JA, Chaudhry R, Sharma N, Shinkre N, Parida S, et al. Extended-spectrum β-lactamase-producing Gram-negative bacteria causing neonatal sepsis in India in rural and urban settings. J Med Microbiol 2011; 60: 500-507.
11. Arzanlou M, Chai WC, Henrietta V. Intrinsic, adaptive and acquired antimicrobial resistance in Gram-negative bacteria. Essays Biochem 2017; 61: 49-59.
12. Harris PNA, Ferguson JK. Antibiotic therapy for inducible AmpC β-lactamase-producing gram-negative bacilli: what are the alternatives to carbapenems, quinolones and aminoglycosides?. Int J Antimicrob Agents 2012; 40: 297-305.
13. Lukac PJ, Bonomo RA, Logan LK. Extended-spectrum β-lactamase–producing Enterobacteriaceae in children: old foe, emerging threat. Clin Infect Dis 2015; 60: 1389-1397.
14. Castanheira M, Mendes RE, Rhomberg PR, Jones RN. Rapid emergence of blaCTX-M among Enterobacteriaceae in US medical centers: molecular evaluation from the MYSTIC Program (2007). Microb Drug Resist 2008; 14: 211-216.
15. Pitout JD, Laupland KB. Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 2008; 8: 159-166.
16. Lee JH, Bae IK, Hee Lee S. New definitions of extended‐spectrum β‐lactamase conferring worldwide emerging antibiotic resistance. Med Res Rev 2012; 32: 216-232.
17. Cantón R, Novais A, Valverde A, Machado E, Peixe L, Baquero F, et al. Prevalence and spread of ‐spectrum β‐lactamase‐producing Enterobcteriaceae in Europe. Clin Microbiol Infect 2008; 14 Suppl 1: 144-153.
18. Marti E, Huerta B, Rodríguez-Mozaz S, Barceló D, Jofre J, Balcázar JL. Characterization of ciprofloxacin-resistant isolates from a wastewater treatment plant and its receiving river. Water Res 2014; 61: 67-76.
19. Handa D, Pandey A, Asthana AK, Rawat A, Handa S, Thakuria B. Evaluation of phenotypic tests for the detection of AmpC beta-lactamase in clinical isolates of Escherichia coli. Indian J Pathol Microbiol 2013; 56: 135-138.
20. Grover N, Sahni AK, Bhattacharya S. Therapeutic challenges of ESBLS and AmpC beta-lactamase producers in a tertiary care center. Med J Armed Forces India 2013; 69: 4-10.
21. Verdet C, BenzeraraY, Gautier V, Adam O, Ould-Hocine Z, Arlet G. Emergence of DHA-1-producing Klebsiella spp. in the Parisian region: genetic organization of the ampC and ampR genes originating from Morganella morganii. Antimicrob Agents Chemother 2006; 50: 607-17.
22. Pérez-Pérez FJ, Hanson ND. Detection of plthe asmid-mediated AmpC β-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 2002; 40: 2153-2162.
23. Gude MJ, Seral C, Sáenz Y, Cebollada R, Torres C, Castillo FJ. Molecular epidemiology, resistance profiles and clinical features in clinical plasmid-mediated AmpC-producing Enterobacteriaceae. Int J Med Microbiol 2013; 303: 553-557.
24. Tan TY, Ng LS, He J, Koh TH, Hsu LY. Evaluation of screening methods to detect plasmid-mediated AmpC in Escherichia coli, Klebsiella pneumoniae, and Proteus mirabilis. Antimicrob Agents Chemother 2009; 53: 146-149.
25. Mata C, Miró E, Rivera A, Mirelis B, Coll P, Navarro F. Prevalence of acquired AmpC β-lactamases in Enterobacteriaceae lacking inducible chromosomal ampC genes at a Spanish hospital from 1999 to 2007. Clin Microbiol Infect 2010; 16: 472-476.
26. Sóki J, Gonzalez SM, Urbán E, Nagy E, Ayala JA. Molecular analysis of the effector mechanisms of cefoxitin resistance among Bacteroides strains. J Antimicrob Chemother 2011; 66: 2492-2500.
27. Mohammadi M, Fataei E. Comparative life cycle assessment of municipal wastewater treatment systems: lagoon and activated sludge. Caspian J Environ Sci 2019; 17: 327-336.
28. Miyagi K, Hirai I. A survey of extended-spectrum β-lactamase-producing Enterobacteriaceae in environmental water in Okinawa prefecture of Japan and relationship with indicator organisms. Environ Sci Pollut Res Int 2019; 26: 7697-7710.
29. Connie R M, Lehman DC, Manuselis Jr G. Textbook of diagnostic microbiology-e-book (Elsevier Health Sciences). 2018.
30. Clinical, and Laboratory Standards Institute."Performance standards for antimicrobial susceptibility testing." In.: Clinical and Laboratory Standards Institute Wayne, PA. 2023.
31. EUCAST, T. "European Committee on Antimicrobial Susceptibility Testing, Breakpoint tables for interpretation of MICs and zone diameters." In.: European Society of Clinical Microbiology and Infectious Diseases Basel. 2023.
32. Gupta G, Tak V, Mathur P. Detection of AmpC β lactamases in gram-negative bacteria. J Lab Physicians 2014; 6: 1-6.
33. Coudron PE. Inhibitor-based methods for detection of plasmid-mediated AmpC β-lactamases in Klebsiella spp., Escherichia coli, and Proteus mirabilis. J Clin Microbiol 2005; 43: 4163-4167.
34. Ruppé E, Hem S, Lath S, Gautier V, Ariey F, Sarthou JL. CTX-M β-lactamases in Escherichia coli from community-acquired urinary tract infections, Cambodia. Emerg Infect Dis 2009; 15: 741-748.
35. Afzali H, Firoozeh F, Amiri A, Moniri R, Zibaei M. Characterization of CTX-M-type extend-spectrum β-lactamase producing Klebsiella spp. in Kashan, Iran. Jundishapur J Microbiol 2015; 8(10): e27967.
36. Al-Riyami IM, Ahmed M, Al-Busaidi A, Choudri BS. Antibiotics in wastewaters: a review with focus on Oman. Appl Water Sci 2018; 8: 199.
37. Zaatout N, Bouras S, Slimani N. Prevalence of extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae in wastewater: a systematic review and meta-analysis. J Water Health 2021; 19: 705-723.
38. Raven KE, Ludden C, Gouliouris T, Blane B, Naydenova P, Brown NM. 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.
39. Habibzadeh N, Peeri Doghaheh H, Manouchehri Far M, Alimohammadi Asl H, Iranpour S, Arzanlou M. Fecal carriage of Extended-Spectrum β-Lactamases and pAmpC producing Enterobacterales in an Iranian community: prevalence, risk factors, molecular epidemiology, and antibiotic resistance. Microb Drug Resist 2022; 28: 921-934.
40. Röderová M, Sedláková MH, Pudová V, Hricová K, Silová R, Imwensi PEO. Occurrence of bacteria producing broad-spectrum beta-lactamases and qnr genes in hospital and urban wastewater samples. New Microbiol 2016; 39: 124-133.
41. Fadare FT, Okoh AI. The Abundance of genes encoding ESBL, pAmpC and Non-β-Lactam resistance in multidrug-resistant Enterobacteriaceae recovered from wastewater effluents. Front Environ Sci 2021; 9: 711950.
42. Korzeniewska E, Harnisz M. Beta-lactamase-producing Enterobacteriaceae in hospital effluents. J Environ Manage 2013; 123: 1-7.
43. Lenart-Boroń AM, Kulik K, Jelonkiewicz E. Antimicrobial resistance and ESBL genes in E. coli isolated in proximity to a sewage treatment plant. J Environ Sci Health A Tox Hazard Subst Environ Eng 2020; 55: 1571-15800.
44. Stoppe NdC, Silva JS, Carlos C, Sato MIZ, Saraiva AM, Ottoboni LMM, et al. Worldwide phylogenetic group patterns of Escherichia coli from commensal human and wastewater treatment plant isolates. Front Microbiol 2017; 8: 2512.
45. Amador PP, Fernandes RM, Prudêncio MC, Barreto MP, Duarte IM. Antibiotic resistance in wastewater: Occurrence and fate of Enterobacteriaceae producers of Class A and Class C β-lactamases. J Environ Sci Health A Tox Hazard Subst Environ Eng 2015; 50: 26-39.
46. Haller L, Chen H, Ng C, Le TH, Koh, TH, Barkham T. Occurrence and characteristics of extended-spectrum β-lactamase-and carbapenemase-producing bacteria from hospital effluents in Singapore. Sci Total Environ 2018; 615: 1119-1125.
47. Tokajian S, Moghnieh R, Salloum T, Arabaghian H, Alousi S, Moussa J. Extended-spectrum β-lactamase-producing Escherichia coli in wastewaters and refugee camp in Lebanon. Future Microbiol 2018; 13: 81-95.
48. Blaak H, Lynch G, Italiaander R, Hamidjaja RA, Schets FM, De Husman AMR. Multidrug-resistant and extended spectrum beta-lactamase-producing Escherichia coli in Dutch surface water and wastewater. PLoS One 2015; 10(6): e0127752.
49. Diallo AA, Brugère H, Kérourédan M, Dupouy V, Toutain PL, Bousquet-Mélou A, et al. Persistence and prevalence of pathogenic and extended-spectrum beta-lactamase-producing Escherichia coli in municipal wastewater treatment plant receiving slaughterhouse wastewater. Water Res 2013; 47: 4719-4729.
| Files | ||
| Issue | Vol 15 No 4 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i4.13506 | |
| Keywords | ||
| Extended spectrum beta-lactamase; AmpC beta-lactamase; Enterobacterales; Municipal sewage; Antibiotic resistance | ||
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How to Cite
1.
Hasani K, Sadeghi H, Vosoughi M, Sardari M, Manouchehrifar M, Arzanlou M. Characterization of beta-lactamase producing Enterobacterales isolated from an urban community wastewater treatment plant in Iran. Iran J Microbiol. 2023;15(4):521-532.
