Abstract
The present study assessed the presence of ESBL-producing Escherichia coli in livestock farm wastewater (LFWW), hospital wastewater (HWW), and natural water sources (NWS) from five districts (Prayagraj, Mirzapur, Varanasi, Sonbhadra, and Jaunpur) of eastern parts of Uttar Pradesh, India (n = 134). Phenotypic ESBL production among cefotaxime-resistant E. coli isolates (91.29%, 283/310) was significantly different (p < 0.05) in the samples from Jaunpur and Sonbhadra, but not from Prayagraj, Mirzapur and Varanasi (p > 0.05). The MIC of cefotaxime and ceftazidime against these isolates were in the ranges of 64–512 µg/mL and 16–512 µg/mL, respectively. Genotypically, 38.51% (109/283) of the isolates harbored at least one or more plasmid-mediated ESBL-genes, of which, blaCTX-M-gr-1 was the predominant (90.82%, 99/109), followed by blaTEM (73.39%, 80/109). A non-significant difference (p > 0.05) was observed in the occurrence of ESBL genes among the phenotypically positive isolates of different sampling places. Multidrug-resistant (MDR) traits were observed in 105 (96.33%) of 109 tested isolates with a MAR index ranging from 0.31 to 1.0. Absolute resistance (100%) was evident against azithromycin for all isolates recovered from Varanasi, Prayagraj, and Sonbhadra irrespective of their sources. The majority of the isolates belonged to commensal phylogroup A (40.37%, 44/109) and B1 (27.44%, 31/109), while only two isolates recovered from HWW sources of Varanasi belonged to the extra-intestinal pathogenic phylogroup B2. These findings suggested that the wastewater and natural water sources of eastern parts of Uttar Pradesh, India, harbored a high magnitude of MDR-ESBL E. coli with the potential to be transmitted to humans and animals.
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Data Availability
All data supporting the findings of this study are available within the paper and its supplementary files. The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Adekanmbi, A. O., Akinpelu, M. O., Olaposi, A. V., & Oyelade, A. A. (2020). Diversity of Extended Spectrum Beta-lactamase (ESBL) genes in Escherichia coli isolated from wastewater generated by a Sick Bay located in a University Health Care Facility. Gene Reports, 20. https://doi.org/10.1016/j.genrep.2020.100738
Adelowo, O. O., Caucci, S., Banjo, O. A., Nnanna, O. C., Awotipe, E. O., Peters, F. B., et al. (2018). Extended spectrum beta-lactamase (ESBL)-producing bacteria isolated from hospital wastewaters, rivers and aquaculture sources in Nigeria. Environmental Science and Pollution Research, 25(3), 2744–2755. https://doi.org/10.1007/s11356-017-0686-7
Afunwa, R. A., Ezeanyinka, J., Afunwa, E. C., Udeh, A. S., Oli, A. N., & Unachukwu, M. (2020). Multiple antibiotic resistant index of gram-negative bacteria from bird droppings in two commercial poultries in Enugu. Nigeria. Open Journal of Medical Microbiology, 10(04), 171–181. https://doi.org/10.4236/ojmm.2020.104015
Akiba, M., Sekizuka, T., Yamashita, A., Kuroda, M., Fujii, Y., Murata, M., et al. (2016). Distribution and relationships of antimicrobial resistance determinants among extended-spectrum-cephalosporin-resistant or carbapenem-resistant Escherichia coli isolates from rivers and sewage treatment plants in India. Antimicrobial Agents and Chemotherapy, 60(5), 2972–2980. https://doi.org/10.1128/AAC.01950-15
Alouache, S., Estepa, V., Messai, Y., Ruiz, E., Torres, C., & Bakour, R. (2014). Characterization of ESBLs and associated quinolone resistance in escherichia coli and klebsiella pneumoniae isolates from an urban wastewater treatment plant in Algeria. Microbial Drug Resistance, 20(1), 30–38. https://doi.org/10.1089/mdr.2012.0264
Alsanjary, L. H., & Sheet, O. H. (2022). Molecular detection of uidA gene in Escherichia coli isolated from the dairy farms in Nineveh governorate, Iraq. Iraqi Journal of Veterinary Sciences, 36(3), 599–603. https://doi.org/10.33899/ijvs.2021.131046.1913
Amos, G. C. A., Hawkey, P. M., Gaze, W. H., & Wellington, E. M. (2014). Waste water effluent contributes to the dissemination of CTX-M-15 in the natural environment. Journal of Antimicrobial Chemotherapy, 69(7), 1785–1791. https://doi.org/10.1093/jac/dku079
Ayerbe, L., Risco-Risco, C., Forgnone, I., Pérez-Piñar, M., & Ayis, S. (2022). Azithromycin in patients with COVID-19: A systematic review and meta-analysis. Journal of Antimicrobial Chemotherapy, 77(2), 303–309. https://doi.org/10.1093/jac/dkab404
Baird, R. B., Eaton, A. D., & Rice, E. W. E. (2017). Part 9000 Microbiological Examination. Standard Methods for the Examination of Water and Wastewater (23rd ed., pp. 36–39). Washington D.C.: American Public Health Association, American Water Works Association, Water Environment Federation. https://doi.org/10.2105/SMWW.2882.184
Bajaj, P., Singh, N. S., Kanaujia, P. K., & Virdi, J. S. (2015). Distribution and molecular characterization of genes encoding CTX-M and AmpC β-lactamases in Escherichia coli isolated from an Indian urban aquatic environment. Science of the Total Environment, 505, 350–356. https://doi.org/10.1016/j.scitotenv.2014.09.084
Bardhan, T., Chakraborty, M., & Bhattacharjee, B. (2020). Prevalence of colistin-resistant carbapenem-hydrolyzing proteobacteria in hospital water bodies and out-falls of West Bengal, India. International Journal of Environmental Research and Public Health, 17(3), 1007. https://doi.org/10.3390/ijerph17031007
Barrasa, H., Rello, J., Tejada, S., Martín, A., Balziskueta, G., Vinuesa, C., et al. (2020). SARS-CoV-2 in Spanish intensive care units: Early experience with 15-day survival in Vitoria. Anaesthesia Critical Care and Pain Medicine, 39(5), 553–561. https://doi.org/10.1016/j.accpm.2020.04.001
Bell, J. M., Chitsaz, M., Turnidge, J. D., Barton, M., Walters, L. J., & Jones, R. N. (2007). Prevalence and significance of a negative extended-spectrum β-lactamase (ESBL) confirmation test result after a positive ESBL screening test result for isolates of Escherichia coli and Klebsiella pneumoniae: Results from the SENTRY asia-pacific surveillan. Journal of Clinical Microbiology, 45(5), 1478–1482. https://doi.org/10.1128/JCM.02470-06
Bengtsson-Palme, J., Kristiansson, E., & Larsson, D. G. J. (2018). Environmental factors influencing the development and spread of antibiotic resistance. FEMS Microbiology Reviews, 42(1), 68–80. https://doi.org/10.1093/femsre/fux053
Blaak, H., Lynch, G., Italiaander, R., Hamidjaja, R. A., Schets, F. M., & De Husman, A. M. R. (2015). Multidrug-resistant and extended spectrum beta-lactamase-producing escherichia coli in dutch surface water and wastewater. PLoS ONE, 10(6). https://doi.org/10.1371/journal.pone.0127752
Brisse, S., Diancourt, L., Laouénan, C., Vigan, M., Caro, V., Arlet, G., et al. (2012). Phylogenetic distribution of CTX-M- and non-extended-spectrum-β- lactamase-producing Escherichia coli isolates: Group B2 isolates, except clone ST131, rarely produce CTX-M enzymes. Journal of Clinical Microbiology, 50(9), 2974–2981. https://doi.org/10.1128/JCM.00919-12
Caltagirone, M., Nucleo, E., Spalla, M., Zara, F., Novazzi, F., Marchetti, V. M., et al. (2017). Occurrence of extended spectrum β-lactamases, KPC-Type, and MCR-1.2-producing enterobacteriaceae from wells, river water, and wastewater treatment plants in Oltrepò Pavese area, Northern Italy. Frontiers in Microbiology, 8(NOV). https://doi.org/10.3389/fmicb.2017.02232
Cantón, R., González-Alba, J. M., & Galán, J. C. (2012). CTX-M enzymes: Origin and diffusion. Frontiers in Microbiology, 3(APR). https://doi.org/10.3389/fmicb.2012.00110
Chaturvedi, P., Chaurasia, D., Pandey, A., & Gupta, P. (2020). Co-occurrence of multidrug resistance, β-lactamase and plasmid mediated AmpC genes in bacteria isolated from river Ganga, northern India. Environmental Pollution, 267. https://doi.org/10.1016/j.envpol.2020.115502
Chen, H., Shu, W., Chang, X., Chen, J. A., Guo, Y., & Tan, Y. (2010). The profile of antibiotics resistance and integrons of extended-spectrum beta-lactamase producing thermotolerant coliforms isolated from the Yangtze River basin in Chongqing. Environmental Pollution, 158(7), 2459–2464. https://doi.org/10.1016/j.envpol.2010.03.023
Chukwu, K. B., Abafe, O. A., Amoako, D. G., Essack, S. Y., & Abia, A. L. K. (2023). Antibiotic, heavy metal, and biocide concentrations in a wastewater treatment plant and its receiving water body exceed PNEC limits: Potential for antimicrobial resistance selective pressure. Antibiotics, 12(7). https://doi.org/10.3390/antibiotics12071166
Clermont, O., Christenson, J. K., Denamur, E., & Gordon, D. M. (2013). The Clermont Escherichia coli phylo-typing method revisited: Improvement of specificity and detection of new phylo-groups. Environmental Microbiology Reports, 5(1), 58–65. https://doi.org/10.1111/1758-2229.12019
CLSI. (2018). Performance Standards for Antimicrobial Susceptibility Testing. CLSI supplement M100 (28th ed.). Wayne, PA: Clinical and Laboratory Standards Institute, Wayne, PA. Accessed 20 May 2023.
Conte, D., Palmeiro, J. K., da Silva Nogueira, K., de Lima, T. M. R., Cardoso, M. A., Pontarolo, R., et al. (2017). Characterization of CTX-M enzymes, quinolone resistance determinants, and antimicrobial residues from hospital sewage, wastewater treatment plant, and river water. Ecotoxicology and Environmental Safety, 136, 62–69. https://doi.org/10.1016/j.ecoenv.2016.10.031
D’Andrea, M. M., Arena, F., Pallecchi, L., & Rossolini, G. M. (2013). CTX-M-type β-lactamases: A successful story of antibiotic resistance. International Journal of Medical Microbiology, 303(6–7), 305–317. https://doi.org/10.1016/j.ijmm.2013.02.008
Dallenne, C., da Costa, A., Decré, D., Favier, C., & Arlet, G. (2010). Development of a set of multiplex PCR assays for the detection of genes encoding important β-lactamases in Enterobacteriaceae. Journal of Antimicrobial Chemotherapy, 65(3), 490–495. https://doi.org/10.1093/jac/dkp498
Dhanji, H., Doumith, M., Rooney, P. J., O’Leary, M. C., Loughrey, A. C., Hope, R., Woodford, N., & Livermore, D. M. (2011). Molecular epidemiology of fluoroquinolone-resistant ST131 Escherichia coli producing CTX-M extended-spectrum β-lactamases in nursing homes in Belfast, UK. Journal of Antimicrobial Chemotherapy, 66(2), 297–303. https://doi.org/10.1093/jac/dkq463
Diwan, V., Chandran, S. P., Tamhankar, A. J., Stålsby Lundborg, C., & Macaden, R. (2012). Identification of extended-spectrum β-lactamase and quinolone resistance genes in Escherichia coli isolated from hospital wastewater from central India. Journal of Antimicrobial Chemotherapy, 67(4), 857–859. https://doi.org/10.1093/jac/dkr564
Diwan, V., Tamhankar, A. J., Khandal, R. K., Sen, S., Aggarwal, M., Marothi, Y., et al. (2010). Antibiotics and antibiotic-resistant bacteria in waters associated with a hospital in Ujjain, India. BMC Public Health, 10. https://doi.org/10.1186/1471-2458-10-414
Drieux, L., Brossier, F., Sougakoff, W., & Jarlier, V. (2008). Phenotypic detection of extended-spectrum β-lactamase production in Enterobacteriaceae: Review and bench guide. Clinical Microbiology and Infection, 14(SUPPL. 1), 90–103. https://doi.org/10.1111/j.1469-0691.2007.01846.x
Escobar-Páramo, P., Le Menac’h, A., Le Gall, T., Amorin, C., Gouriou, S., Picard, B., et al. (2006). Identification of forces shaping the commensal Escherichia coli genetic structure by comparing animal and human isolates. Environmental Microbiology, 8(11), 1975–1984. https://doi.org/10.1111/j.1462-2920.2006.01077.x
Galvin, S., Boyle, F., Hickey, P., Vellinga, A., Morris, D., & Cormican, M. (2010). Enumeration and characterization of antimicrobial-resistant escherichia coli bacteria in effluent from municipal, hospital, and secondary treatment facility sources. Applied and Environmental Microbiology, 76(14), 4772–4779. http://aem.asm.org/cgi/reprint/76/14/4772%5Cnhttp://ovidsp.ovid.com/ovidweb.cgi?T=JS&PAGE=reference&D=emed9&NEWS=N&AN=20525867.
Garcia-Aljaro, C., Moreno, E., Andreu, A., Prats, G., & Blanch, A. R. (2009). Phylogroups, virulence determinants and antimicrobial resistance in stx2 gene-carrying Escherichia coli isolated from aquatic environments. Research in Microbiology, 160(8), 585–591. https://doi.org/10.1016/j.resmic.2009.08.004
Ghatak, S., Singha, A., Sen, A., Guha, C., Ahuja, A., Bhattacharjee, U., et al. (2013). Detection of new delhi metallo-beta-lactamase and extended-spectrum beta-lactamase genes in escherichia coli isolated from mastitic milk samples. Transboundary and Emerging Diseases, 60(5), 385–389. https://doi.org/10.1111/tbed.12119
Girijan, S. K., & Pillai, D. (2023). Genetic diversity and prevalence of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in aquatic environments receiving untreated hospital effluents. Journal of Water and Health, 21(1), 66–80. https://doi.org/10.2166/wh.2022.194
Gregova, G., Kmet, V., & Szaboova, T. (2021). New insight on antibiotic resistance and virulence of escherichia coli from municipal and animal wastewater. Antibiotics, 10(9). https://doi.org/10.3390/antibiotics10091111
Gyselinck, I., Janssens, W., Verhamme, P., & Vos, R. (2021). Rationale for azithromycin in COVID-19: An overview of existing evidence. BMJ Open Respiratory Research, 8(1). https://doi.org/10.1136/bmjresp-2020-000806
Hanna, N., Purohit, M., Diwan, V., Chandran, S. P., Riggi, E., Parashar, V., et al. (2020). Monitoring of water quality, antibiotic residues, and antibiotic-resistant Escherichia coli in the Kshipra River in India over a 3-year period. International Journal of Environmental Research and Public Health, 17(21), 1–22. https://doi.org/10.3390/ijerph17217706
Hartmann, A., Locatelli, A., Amoureux, L., Depret, G., Jolivet, C., Gueneau, E., & Neuwirth, C. (2012). Occurrence of CTX-M producing Escherichia coli in soils, cattle, and farm environment in France (Burgundy region). Frontiers in Microbiology, 3(MAR). https://doi.org/10.3389/fmicb.2012.00083
Higgins, J., Hohn, C., Hornor, S., Frana, M., Denver, M., & Joerger, R. (2007). Genotyping of Escherichia coli from environmental and animal samples. Journal of Microbiological Methods, 70(2), 227–235. https://doi.org/10.1016/j.mimet.2007.04.009
Hooban, B., Joyce, A., Fitzhenry, K., Chique, C., & Morris, D. (2020). The role of the natural aquatic environment in the dissemination of extended spectrum beta-lactamase and carbapenemase encoding genes: A scoping review. Water Research, 180. https://doi.org/10.1016/j.watres.2020.115880
Hsu, L. Y., Tan, T. Y., Tam, V. H., Kwa, A., Fisher, D. A., Koh, T. H., et al. (2010). Surveillance and correlation of antibiotic prescription and resistance of gram-negative bacteria in Singaporean hospitals. Antimicrobial Agents and Chemotherapy, 54(3), 1173–1178. https://doi.org/10.1128/AAC.01076-09
Hussain, H. I., Aqib, A. I., Seleem, M. N., Shabbir, M. A., Hao, H., Iqbal, Z., et al. (2021). Genetic basis of molecular mechanisms in β-lactam resistant gram-negative bacteria. Microbial Pathogenesis, 158. https://doi.org/10.1016/j.micpath.2021.105040
Ibrahim, D. R., Dodd, C. E. R., Stekel, D. J., Ramsden, S. J., & Hobman, J. L. (2016). Multidrug resistant extended spectrum β-lactamase (ESBL)-producing Escherichia coli isolated from a dairy farm. FEMS Microbiology Ecology, 92(4), fiw013. https://doi.org/10.1093/femsec/fiw013
Ibrahimagić, A., Bedenić, B., Kamberović, F., & Uzunović, S. (2015). High prevalence of CTX-M-15 and first report of CTX-M-3, CTX-M-22, CTX-M-28 and plasmid-mediated AmpC beta-lactamase producing Enterobacteriaceae causing urinary tract infections in Bosnia and Herzegovina in hospital and community settings. Journal of Infection and Chemotherapy, 21(5), 363–369. https://doi.org/10.1016/j.jiac.2015.01.003
Jørgensen, S. B., Søraas, A. V., Arnesen, L. S., Leegaard, T. M., Sundsfjord, A., & Jenum, P. A. (2017). A comparison of extended spectrum β-lactamase producing Escherichia coli from clinical, recreational water and wastewater samples associated in time and location. PLoS ONE, 12(10). https://doi.org/10.1371/journal.pone.0186576
Kalasseril, S. G., Krishnan, R., Vattiringal, R. K., Paul, R., Mathew, P., & Pillai, D. (2020). Detection of New Delhi Metallo-β-lactamase 1 and cephalosporin resistance genes among carbapenem-resistant Enterobacteriaceae in water bodies adjacent to hospitals in India. Current Microbiology, 77(10), 2886–2895. https://doi.org/10.1007/s00284-020-02107-y
Kamruzzaman, M., Shoma, S., Naymul Bari, S. M. N., Ginn, A. N., Wiklendt, A. M., Partridge, S. R., et al. (2013). Genetic diversity and antibiotic resistance in Escherichia coli from environmental surface water in Dhaka City, Bangladesh. Diagnostic Microbiology and Infectious Disease, 76(2), 222–226. https://doi.org/10.1016/j.diagmicrobio.2013.02.016
Kasanga, M., Kwenda, G., Wu, J., Kasanga, M., Mwikisa, M. J., Chanda, R., et al. (2023). Antimicrobial resistance patterns and risk factors associated with ESBL-producing and MDR Escherichia coli in hospital and environmental settings in Lusaka, Zambia: Implications for One Health, Antimicrobial Stewardship and Surveillance Systems. Microorganisms, 11(8). https://doi.org/10.3390/microorganisms11081951
Kemper, N. (2008). Veterinary antibiotics in the aquatic and terrestrial environment. Ecological Indicators, 8(1), 1–13. https://doi.org/10.1016/j.ecolind.2007.06.002
Kim, J., Kang, H. Y., & Lee, Y. (2008). The identification of CTX-M-14, TEM-52, and CMY-1 enzymes in Escherichia coli isolated from the Han River in Korea. Journal of Microbiology, 46(5), 478–481. https://doi.org/10.1007/s12275-008-0150-y
Korzeniewska, E., Korzeniewska, A., & Harnisz, M. (2013). Antibiotic resistant Escherichia coli in hospital and municipal sewage and their emission to the environment. Ecotoxicology and Environmental Safety, 91, 96–102. https://doi.org/10.1016/j.ecoenv.2013.01.014
Krumperman, P. H. (1983). Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods | Applied and Environmental Microbiology. Applied and Environmental Microbiology, 46, 165–170. https://journals.asm.org/doi/abs/10.1128/aem.46.1.165-170.1983.
Kutilova, I., Medvecky, M., Leekitcharoenphon, P., Munk, P., Masarikova, M., Davidova-Gerzova, L., et al. (2021). Extended-spectrum beta-lactamase-producing Escherichia coli and antimicrobial resistance in municipal and hospital wastewaters in Czech Republic: Culture-based and metagenomic approaches. Environmental Research, 193. https://doi.org/10.1016/j.envres.2020.110487
Lamba, M., Graham, D. W., & Ahammad, S. Z. (2017). Hospital wastewater releases of carbapenem-resistance pathogens and genes in urban India. Environmental Science and Technology, 51(23), 13906–13912. https://doi.org/10.1021/acs.est.7b03380
Lavilla, S., González-López, J. J., Sabaté, M., García-Fernández, A., Larrosa, M. N., Bartolomé, R. M., et al. (2008). Prevalence of qnr genes among extended-spectrum β-lactamase-producing enterobacterial isolates in Barcelona, Spain. Journal of Antimicrobial Chemotherapy, 61(2), 291–295. https://doi.org/10.1093/jac/dkm448
Liakopoulos, A., Mevius, D., & Ceccarelli, D. (2016). A review of SHV extended-spectrum β-lactamases: Neglected yet ubiquitous. Frontiers in Microbiology, 7(SEP). https://doi.org/10.3389/fmicb.2016.01374
Liedhegner, E., Bojar, B., Beattie, R. E., Cahak, C., Hristova, K. R., & Skwor, T. (2022). Similarities in virulence and extended spectrum beta-lactamase gene profiles among cefotaxime-resistant Escherichia coli wastewater and clinical isolates. Antibiotics, 11(2). https://doi.org/10.3390/antibiotics11020260
López-Jácome, L. E., Fernández-Rodríguez, D., Franco-Cendejas, R., Camacho-Ortiz, A., Morfin-Otero, M. D. R., Rodríguez-Noriega, E., et al. (2022). Increment antimicrobial resistance during the COVID-19 pandemic: Results from the Invifar Network. Microbial Drug Resistance, 28(3), 338–345. https://doi.org/10.1089/mdr.2021.0231
Magiorakos, A. P., Srinivasan, A., Carey, R. B., Carmeli, Y., Falagas, M. E., Giske, C. G., et al. (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection, 18(3), 268–281. https://doi.org/10.1111/j.1469-0691.2011.03570.x
Mahmud, Z. H., Kabir, M. H., Ali, S., Moniruzzaman, M., Imran, K. M., Nafiz, T. N., et al. (2020). Extended-spectrum beta-lactamase-producing Escherichia coli in drinking water samples from a forcibly displaced, densely populated community setting in Bangladesh. Frontiers in Public Health, 8. https://doi.org/10.3389/fpubh.2020.00228
Manyi-Loh, C., Mamphweli, S., Meyer, E., & Okoh, A. (2018). Antibiotic use in agriculture and its consequential resistance in environmental sources: Potential public health implications. Molecules, 23(4). https://doi.org/10.3390/molecules23040795
Marathe, N. P., Berglund, F., Razavi, M., Pal, C., Dröge, J., Samant, S., et al. (2019). Sewage effluent from an Indian hospital harbors novel carbapenemases and integron-borne antibiotic resistance genes. Microbiome, 7(1). https://doi.org/10.1186/s40168-019-0710-x
McDaniels, A. E., Rice, E. W., Reyes, A. L., Johnson, C. H., Haugland, R. A., & Stelma, G. N. (1996). Confirmational identification of Escherichia coli, a comparison of genotypic and phenotypic assays for glutamate decarboxylase and β-D- glucuronidase. Applied and Environmental Microbiology, 62(9), 3350–3354. https://doi.org/10.1128/aem.62.9.3350-3354.1996
Murugan, M. S., Sinha, D. K., Vinodh Kumar, O. R., Yadav, A. K., Pruthvishree, B. S., Vadhana, P., et al. (2019). Epidemiology of carbapenem-resistant Escherichia coli and first report of blaVIM carbapenemases gene in calves from India. Epidemiology and Infection, 147. https://doi.org/10.1017/S0950268819000463
Nyirabahizi, E., Tyson, G. H., Dessai, U., Zhao, S., Kabera, C., Crarey, E., et al. (2020). Evaluation of Escherichia coli as an indicator for antimicrobial resistance in Salmonella recovered from the same food or animal ceca samples. Food Control, 115. https://doi.org/10.1016/j.foodcont.2020.107280
Nzima, B., Adegoke, A. A., Ofon, U. A., Al-Dahmoshi, H. O. M., Saki, M., Ndubuisi-Nnaji, U. U., & Inyang, C. U. (2020). Resistotyping and extended-spectrum beta-lactamase genes among Escherichia coli from wastewater treatment plants and recipient surface water for reuse in South Africa. New Microbes and New Infections, 38. https://doi.org/10.1016/j.nmni.2020.100803
Paterson, D. L., & Bonomo, R. A. (2005). Extended-spectrum beta-lactamases: A clinical update. Clinical Microbiology Reviews, 18, 657–686.
Pruthvishree, B. S., Vinodh Kumar, O. R., Sinha, D. K., Malik, Y. P. S., Dubal, Z. B., Desingu, P. A., et al. (2017). Spatial molecular epidemiology of carbapenem-resistant and New Delhi metallo beta-lactamase (blaNDM)-producing Escherichia coli in the piglets of organized farms in India. Journal of Applied Microbiology, 122(6), 1537–1546. https://doi.org/10.1111/jam.13455
Raimondi, S., Righini, L., Candeliere, F., Musmeci, E., Bonvicini, F., Gentilomi, G., et al. (2019). Antibiotic resistance, virulence factors, phenotyping, and genotyping of E. Coli isolated from the feces of healthy subjects. Microorganisms, 7(8). https://doi.org/10.3390/microorganisms7080251
Ramos, S., Silva, V., de Lurdes Enes Dapkevicius, M., Caniça, M., Tejedor-Junco, M. T., Igrejas, G., & Poeta, P. (2020). Escherichia coli as commensal and pathogenic bacteria among food-producing animals: Health implications of extended spectrum β-lactamase (ESBL) production. Animals, 10(12), 1–15. https://doi.org/10.3390/ani10122239
Rawat, N., Singh, F., Hirpurkar, S. D., Sannat, C., & Gade, N. E. (2018). Detection and characterization of extended-spectrum beta-lactamase genes (bla TEM and bla SHV ) among beta-lactam-resistant fecal coliforms of dairy cattle from Chhattisgarh, India. Turkish Journal of Veterinary and Animal Sciences, 42(6), 503–511. https://doi.org/10.3906/vet-1706-77
Runcharoen, C., Raven, K. E., Reuter, S., Kallonen, T., Paksanont, S., Thammachote, J., et al. (2017). Whole genome sequencing of ESBL-producing Escherichia coli isolated from patients, farm waste and canals in Thailand. Genome Medicine, 9(1). https://doi.org/10.1186/s13073-017-0471-8
Sabaté, M., Prats, G., Moreno, E., Ballesté, E., Blanch, A. R., & Andreu, A. (2008). Virulence and antimicrobial resistance profiles among Escherichia coli strains isolated from human and animal wastewater. Research in Microbiology, 159(4), 288–293. https://doi.org/10.1016/j.resmic.2008.02.001
Saekhow, P., & Sriphannam, C. (2021). Prevalence of extended-spectrum beta-lactamase-producing escherichia coli strains in dairy farm wastewater in chiang mai. Veterinary Integrative Sciences, 19(3), 349–362. https://doi.org/10.12982/vis.2021.030
Sageerabanoo, S., Malini, A., Mangaiyarkarasi, T., & Hemalatha, G. (2015). Phenotypic detection of extended spectrum β-lactamase and Amp-C β-lactamase producing clinical isolates in a Tertiary Care Hospital: A preliminary study. Journal of Natural Science, Biology and Medicine, 6(2), 383–387. https://doi.org/10.4103/0976-9668.160014
Samanta, A., Mahanti, A., Chatterjee, S., Joardar, S. N., Bandyopadhyay, S., Sar, T. K., et al. (2018). Pig farm environment as a source of beta-lactamase or AmpC-producing Klebsiella pneumoniae and Escherichia coli. Annals of Microbiology, 68(11), 781–791. https://doi.org/10.1007/s13213-018-1387-2
Sambrook, J., & Russell, D. (Eds.). (2001). Molecular Cloning: A Laboratory Manual (3rd ed.). Cold Spring Harbor Laboratory Press.
Sandhu, R. (2016). Evaluation of multiple antibiotic resistance (MAR) index and Doxycycline susceptibility of Acinetobacter species among inpatients. International Journal of Infectious Diseases, 45, 327. https://doi.org/10.1016/j.ijid.2016.02.710
Schmid, A., Hörmansdorfer, S., Messelhäusser, U., Käsbohrer, A., Sauter-Louis, C., & Mansfeld, R. (2013). Prevalence of extended-spectrum β-lactamase-producing Escherichia coli on Bavarian dairy and beef cattle farms. Applied and Environmental Microbiology, 79(9), 3027–3032. https://doi.org/10.1128/AEM.00204-13
Seabra, G., Ventura Mendes, R. F., dos Santos Amorim, L. F. V., Peregrino, I. V., Branquinha, M. H., dos Santos, A. L. S., & Nunes, A. P. F. (2021). Azithromycin use in COVID-19 patients: Implications on the antimicrobial resistance. Current Topics in Medicinal Chemistry, 21(8), 677–683. https://doi.org/10.2174/156802662108210319145317
Shaikh, S., Fatima, J., Shakil, S., Rizvi, S. M. D., & Kamal, M. A. (2015). Antibiotic resistance and extended spectrum beta-lactamases: Types epidemiology and treatment. Saudi Journal of Biological Sciences, 22(1), 90–101. https://doi.org/10.1016/j.sjbs.2014.08.002
Silva Segundo, R. J. E., Rufino, J. P., Sousa, L. G. V., Rodrigues, A. E. L., Falcão, A. L. S., de Melo Lima, I. C., et al. (2022). Bacterial resistance to azithromycin: Causes, effects, and the fight against COVID-19. Research, Society and Development, 11(6), e27711629198. https://doi.org/10.33448/rsd-v11i6.29198
Singer, R. S., Johnson, W. O., Jeffrey, J. S., Chin, R. P., Carpenter, T. E., Atwill, E. R., & Hirsh, D. C. (2000). A statistical model for assessing sample size for bacterial colony selection: A case study of Escherichia coli and avian cellulitis. Journal of Veterinary Diagnostic Investigation, 12(2), 118–125. https://doi.org/10.1177/104063870001200203
Snow, L. C., Warner, R. G., Cheney, T., Wearing, H., Stokes, M., Harris, K., et al. (2012). Risk factors associated with extended spectrum beta-lactamase Escherichia coli (CTX-M) on dairy farms in North West England and North Wales. Preventive Veterinary Medicine, 106(3–4), 225–234. https://doi.org/10.1016/j.prevetmed.2012.03.009
Sta Ana, K. M., Madriaga, J., & Espino, M. P. (2021). β-Lactam antibiotics and antibiotic resistance in Asian lakes and rivers: An overview of contamination, sources and detection methods. Environmental Pollution, 275. https://doi.org/10.1016/j.envpol.2021.116624
Stoppe, N. de C., Silva, J. S., Carlos, C., Sato, M. I. Z., Saraiva, A. M., Ottoboni, L. M. M., & Torres, T. T. (2017). Worldwide phylogenetic group patterns of Escherichia coli from commensal human and wastewater treatment plant isolates. Frontiers in Microbiology, 8(DEC). https://doi.org/10.3389/fmicb.2017.02512
Sultana, J., Cutroneo, P. M., Crisafulli, S., Puglisi, G., Caramori, G., & Trifirò, G. (2020). Azithromycin in COVID-19 patients: Pharmacological mechanism, clinical evidence and prescribing guidelines. Drug Safety, 43(8), 691–698. https://doi.org/10.1007/s40264-020-00976-7
Van Boeckel, T. P., Gandra, S., Ashok, A., Caudron, Q., Grenfell, B. T., Levin, S. A., & Laxminarayan, R. (2014). Global antibiotic consumption 2000 to 2010: An analysis of national pharmaceutical sales data. The Lancet Infectious Diseases, 14(8), 742–750. https://doi.org/10.1016/S1473-3099(14)70780-7
Vinueza-Burgos, C., Ortega-Paredes, D., Narvaéz, C., De Zutter, L., & Zurita, J. (2019). Characterization of cefotaxime resistant Escherichia coli isolated from broiler farms in Ecuador. PLoS ONE, 14(4). https://doi.org/10.1371/journal.pone.0207567
Wambugu, P., Kiiru, J., & Matiru, V. (2018). Escherichia coli harbouring resistance genes, virulence genes and integron 1 isolated from Athi River in Kenya. Advances in Microbiology, 08(11), 846–858. https://doi.org/10.4236/aim.2018.811056
Watkinson, A. J., Murby, E. J., Kolpin, D. W., & Costanzo, S. D. (2009). The occurrence of antibiotics in an urban watershed: From wastewater to drinking water. Science of the Total Environment, 407(8), 2711–2723. https://doi.org/10.1016/j.scitotenv.2008.11.059
WHO. (2017). Global Antimicrobial Resistance Surveillance System (GLASS) Report Early Implementation 2017–2018. Available online: https://www.who.int/glass/resources/publications/earlyimplementation-report-2017-2018/en/. Accessed 08.05.2023.
WHO. (2019). Ten threats to global health in 2019. Available Online. https://www.who.int/news-room/feature-stories/ten-threats-to-global-health-in-2019. Accessed 08.05.2023.
Wu, Z., McGoogan, J. M., Wang, D., Hu, B., Hu, C., Zhu, F., et al. (2020). Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA - Journal of the American Medical Association, 323(13), 1239–1242.
Xi, C., Zhang, Y., Marrs, C. F., Ye, W., Simon, C., Foxman, B., & Nriagu, J. (2009). Prevalence of antibiotic resistance in drinking water treatment and distribution systems. Applied and Environmental Microbiology, 75(17), 5714–5718. https://doi.org/10.1128/AEM.00382-09
Zarfel, G., Lipp, M., Gürtl, E., Folli, B., Baumert, R., & Kittinger, C. (2017). Troubled water under the bridge: Screening of River Mur water reveals dominance of CTX-M harboring Escherichia coli and for the first time an environmental VIM-1 producer in Austria. Science of the Total Environment, 593–594, 399–405. https://doi.org/10.1016/j.scitotenv.2017.03.138
Acknowledgements
The authors would like to acknowledge Prof. Dr. Balaji Veeraraghavan, Professor and Head, Department of Clinical Microbiology, Christian Medical College, Vellore, Tamil Nadu, India, for providing the positive control strains encoding blaCTX-M gr-1, blaCTX-M gr-2, blaCTX-M gr-8, blaCTX-M gr-9, blaCTX-M gr-25, blaTEM, blaOXA-1 like, and blaSHV genes. The authors would like to thank the Director, ICAR-Indian Veterinary Research Institute, Izatnagar, and the Vice-Chancellor, Banaras Hindu University, Varanasi, for providing support to conduct the research work.
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Conceptualization and design: DBR, SVSM, and SBB; sample collection: KS and AD; experimental work: KS; original draft preparation: KS and DBR; review and editing: DBR, SVSM, and SBB; supervision: DBR and PPK; statistical analysis: VMR and AD. All authors have read and agreed to the published version of the manuscript.
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Satyaprakash, K., Pesingi, P.K., Das, A. et al. Occurrence of Multidrug-Resistant (MDR) Extended-Spectrum Beta-lactamase (ESBL)-Producing Escherichia coli in Wastewater and Natural Water Sources from the Eastern Part of Uttar Pradesh, India. Water Air Soil Pollut 235, 125 (2024). https://doi.org/10.1007/s11270-024-06914-y
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DOI: https://doi.org/10.1007/s11270-024-06914-y