Elucidating the resistance repertoire, biofilm production, and phylogenetic characteristics of multidrug-resistant Escherichia coli isolated from community ponds: A study from West Bengal, India.
AcrAB
ESBL
MDR E. coli
blaCTXM-1
carbapenem
community ponds
Journal
Water environment research : a research publication of the Water Environment Federation
ISSN: 1554-7531
Titre abrégé: Water Environ Res
Pays: United States
ID NLM: 9886167
Informations de publication
Date de publication:
14 Dec 2021
14 Dec 2021
Historique:
revised:
29
11
2021
received:
09
08
2021
accepted:
08
12
2021
pubmed:
16
12
2021
medline:
16
12
2021
entrez:
15
12
2021
Statut:
aheadofprint
Résumé
This study details about the phenotypic and molecular characteristics of multidrug-resistant (MDR) Escherichia coli in the fresh community pond water (n = 257) collected from three districts of West Bengal, India. In total, 57 isolates were MDR of which 38 emerged as extended spectrum and 7 as AmpC-type β-lactamase producers in phenotypic assay. Among β-lactamase genes, blaCTXM-1was predominant (87.71%) followed by blaAmpC (77.2%) and blaTEM-1 (22.8%). Six MDR strains carried metallo-β-lactamase (MBL, blaNDM-1) gene. Tissue culture plate assay confirmed strong biofilm (SP) production in four MDR and one non-MDR isolates. In PCR-based replicon typing (PBRT), multiple plasmids of diverse replicon types (Frep, FIB, I1, FIA, K/B, HI1, and Y) were identified. The enterobacterial repetitive intergenic consensus-polymerase chain reaction (ERIC-PCR)-based phylogenetic analysis revealed a high degree of genetic divergence among the MDR isolates. Multiplex PCR-based phylogrouping categorized 11 isolates as virulent (B2/D/F), which carried blaCTXM-1 gene and three had blaNDM-1 gene. Relative transcriptional activity of AcrAB efflux pump was significantly elevated among the SP and MBL producers. The presence of MDR E. coli isolates, particularly those resistant to carbapenem, in pond water used for daily domestic and household work, is a cause of concern as these pathogens may sneak into human food chain causing life-threatening infections. PRACTITIONER POINTS: Multidrug-resistant biofilm producing E. coli isolated from community pond water. A few of them were carbapenem-resistant and belonged to virulent (B2/D) types. Expression of AcrAB efflux pumps was found significantly elevated among biofilm producers and carbapenem-resistant population.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1678Subventions
Organisme : CAAST-Advanced Centre for Livestock Health (ACLH)
Organisme : ICAR-World Bank
Organisme : National Agricultural Higher Education Project (NAHEP)
Informations de copyright
© 2021 Water Environment Federation.
Références
Adelowo, O. O., Caucci, S., Banjo, O. A., Nnanna, O. C., Awotipe, E. O., Peters, F. B., Fagade, O. E., & Berendonk, T. U. (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
Ahmed, W., Hodgers, L., Masters, N., Sidhu, J. P. S., Katouli, M., & Toze, S. (2011). Occurrence of intestinal and extraintestinal virulence genes in Escherichia coli isolates from rainwater tanks in Southeast Queensland, Australia. Applied and Environmental Microbiology, 77(20), 7394-7400. https://doi.org/10.1128/AEM.06047-11
Alav, I., Sutton, J. M., & Rahman, K. M. (2018). Role of bacterial efflux pumps in biofilm formation. The Journal of Antimicrobial Chemotherapy, 73(8), 2003-2020. https://doi.org/10.1093/jac/dky042
Bandyopadhyay, S., Banerjee, J., Bhattacharyya, D., Samanta, I., Mahanti, A., Dutta, T. K., Ghosh, S., Nanda, P. K., Dandapat, P., & Bandyopadhyay, S. (2018). Genomic identity of fluoroquinolone-resistant blaCTX-M-15-type ESBL and pMAmpC β-lactamase producing Klebsiella pneumoniae from buffalo milk, India. Microbial Drug Resistance, 24(9), 1345-1353. https://doi.org/10.1089/mdr.2017.0368
Bandyopadhyay, S., Banerjee, J., Bhattacharyya, D., Tudu, R., Samanta, I., Dandapat, P., Nanda, P. K., Das, A. K., Mondal, B., Batabyal, S., & Dutta, T. K. (2021). Companion animals emerged as an important reservoir of Carbapenem-resistant Enterobacteriaceae: A report from India. Current Microbiology, 78, 1006-1016. https://doi.org/10.1007/s00284-021-02355-6
Bandyopadhyay, S., Bhattacharyya, D., Samanta, I., Banerjee, J., Habib, M., Dutta, T. K., & Dutt, T. (2021). Characterization of multidrug-resistant biofilm-producing Escherichia coli and Klebsiella pneumoniae in healthy cattle and cattle with diarrhea. Microbial Drug Resistance, 27, 1457-1469. https://doi.org/10.1089/mdr.2020.0298
Bandyopadhyay, S., & Samanta, I. (2019a). Emergence of antimicrobial resistant bacteria in aquaculture. In Antimicrobial resistance in agriculture, perspective, policy and mitigation (First ed.) (pp. 29-37). Academic Press Inc. Elsevier.
Bandyopadhyay, S., & Samanta, I. (2019b). Emergence of antimicrobial-resistant bacteria in environment. In Antimicrobial resistance in agriculture, perspective, policy and mitigation (First ed.) (pp. 39-45). Academic Press Inc. Elsevier.
Bandyopadhyay, S., & Samanta, I. (2019c). Carbapenem resistance. In Antimicrobial resistance in agriculture, perspective, policy and mitigation (First ed.) (pp. 59-69). Academic Press Inc. Elsevier.
Bandyopadhyay, S., & Samanta, I. (2020). Antimicrobial resistance in agri-food chain and companion animals as a re-emerging menace in post-COVID epoch: Low-and middle-income countries perspective and mitigation strategies. Frontiers in Veterinary Science, 7, 620. https://doi.org/10.3389/fvets.2020.00620
Banerjee, A., Bardhan, R., Chowdhury, M., Joardar, S. N., Isore, D. P., Batabyal, K., Dey, S., & Sar, T. K. (2019). Characterization of beta-lactamase and biofilm producing Enterobacteriaceae isolated from organized and backyard farm ducks. Letters in Applied Microbiology, 69(2), 110-115. https://doi.org/10.1111/lam.13170
Banerjee, A., Batabyal, K., Singh, A. D., Joardar, S. N., Dey, S., Isore, D. P., Sar, T. K., Dutta, T. K., Bandyopadhyay, S., & Samanta, I. (2020). Multi-drug resistant, biofilm-producing high-risk clonal lineage of Klebsiella in companion and household animals. Letters in Applied Microbiology, 71(6), 580-587. https://doi.org/10.1111/lam.13381
Berthe, T., Ratajczak, M., Clermont, O., Denamur, E., & Petit, F. (2013). Evidence for coexistence of distinct Escherichia coli populations in various aquatic environments and their survival in estuary water. Applied and Environmental Microbiology, 79(15), 4684-4693. https://doi.org/10.1128/AEM.00698-13
Biswas, K., Paul, D., & Sinha, N. (2015). Prevalence of multiple antibiotic-resistant coliform bacteria in the water of River Ganga. Frontiers in Microbiology, 1(3), 44-46. https://doi.org/10.11648/j.fem.20150103.12
Cepas, V., López, Y., Muñoz, E., Rolo, D., Ardanuy, C., Martí, S., Xercavins, M., Horcajada, J. P., Bosch, J., & Soto, S. M. (2019). Relationship between biofilm formation and antimicrobial resistance in gram-negative bacteria. Microbial Drug Resistance, 25(1), 72-79. https://doi.org/10.1089/mdr.2018.0027
Chandran, S. P., Diwan, V., Tamhankar, A. J., Joseph, B. V., Rosales-Klintz, S., Mundayoor, S., Lundborg, C. S., & Macaden, R. (2014). Detection of carbapenem resistance genes and cephalosporin, and quinolone resistance genes along with oqxAB gene in Escherichia coli in hospital wastewater: A matter of concern. Journal of Applied Microbiology, 117(4), 984-995. https://doi.org/10.1111/jam.12591
Chetri, S., Bhowmik, D., Paul, D., Pandey, P., Chanda, D. D., Chakravarty, A., Bora, D., & Bhattacharjee, A. (2019). AcrAB-TolC efflux pump system plays a role in carbapenem non-susceptibility in Escherichia coli. BMC Microbiology, 19, 210. https://doi.org/10.1186/s12866-019-1589-1
Citterio, B., Andreoni, F., Simoni, S., Carloni, E., Magnani, M., Mangiaterra, G., Cedraro, N., Biavasco, F., & Vignaroli, C. (2020). Plasmid Replicon Typing of Antibiotic-Resistant Escherichia coli from Clams and Marine Sediments. Frontiers in Microbiology, 11(May), 1-8. https://doi.org/10.3389/fmicb.2020.01101
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
Clinton, A., & Carter, T. (2015). Chronic wound biofilms: Pathogenesis and potential therapies. Laboratoriums Medizin, 46(4), 277-284. https://doi.org/10.1309/LMBNSWKUI4JPN7SO
CLSI. (2018). Performance standards for antimicrobial disk susceptibility tests; approved standard (M02-A13 ed., Vol. 12th). Clinical and Laboratory Standards Institute.
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. The Journal of Antimicrobial Chemotherapy, 65(3), 490-495. https://doi.org/10.1093/jac/dkp498
Duriez, P., Clermont, O., Bonacorsi, S., Bingen, E., Chaventré, A., Elion, J., Picard, B., & Denamur, E. (2001). Commensal Escherichia coli isolates are phylogenetically distributed among geographically distinct human populations. Microbiology, 147(6), 1671-1676. https://doi.org/10.1099/00221287-147-6-1671
Edelstein, M., Pimkin, M., Palagin, I., Edelstein, I., & Stratchounski, L. (2003). Prevalence and molecular epidemiology of CTX-M in Russian hospitals. Antimicrobial Agents and Chemotherapy, 47(12), 3724-3732. https://doi.org/10.1128/AAC.47.12.3724-3732.2003
Godambe, L. P., Bandekar, J., & Shashidhar, R. (2017). Species specific PCR based detection of Escherichia coli from Indian foods. 3 Biotech, 7(2), 130. https://doi.org/10.1007/s13205-017-0784-8
Gomi, R., Matsuda, T., Matsumura, Y., Yamamoto, M., Tanaka, M., Ichiyama, S., & Yoneda, M. (2017). Whole-genome analysis of antimicrobial-resistant and extraintestinal pathogenic Escherichia coli in river water. Applied and Environmental Microbiology, 83(5), e02703-16. https://doi.org/10.1128/AEM.02703-16
Halder, M., Mookerjee, S., Batabyal, P., & Palit, A. (2018). Waterborne outbreaks in diarrhoea endemic foci of India: A longitudinal exploration and its implications. Environmental Monitoring and Assessment, 190(3), 172. https://doi.org/10.1007/s10661-017-6424-2
Harwood, V. J., Staley, C., Badgley, B. D., Borges, K., & Korajkic, A. (2014). Microbial source tracking markers for detection of fecal contamination in environmental waters: Relationships between pathogens and human health outcomes. FEMS Microbiology Reviews, 38(1), 1-40. https://doi.org/10.1111/1574-6976.12031
Helaly, G. F., Shawky, S., Amer, R., El-sawaf, G., & El Kholy, M. A. (2016). Expression of AcrAB efflux pump and role of mefloquine as efflux pump inhibitor in MDR E. coli. American Journal of Infectious Diseases, 4(1), 6-13.
Henriques, I. S., Fonseca, F., Alves, A., Saavedra, M. J., & Correia, A. (2006). Occurrence and diversity of integrons and β-lactamase genes among ampicillin-resistant isolates from estuarine waters. Research in Microbiology, 157(10), 938-947. https://doi.org/10.1016/j.resmic.2006.09.003
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
Johnson, T. J., Wannemuehler, Y. M., Johnson, S. J., Logue, C. M., White, D. G., Doetkott, C., & Nolan, L. K. (2007). Plasmid replicon typing of commensal and pathogenic Escherichia coli isolates. Applied and Environmental Microbiology, 73(6), 1976-1983. https://doi.org/10.1128/AEM.02171-06
Kamruzzaman, M., Shoma, S., Bari, S. M., Ginn, A. N., Wiklendt, A. M., Partridge, S. R., Faruque, S. M., & Iredell, J. R. (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
Kar, D., Bandyopadhyay, S., Bhattacharyya, D., Samanta, I., Mahanti, A., Nanda, P. K., Mondal, B., Dandapat, P., Das, A. K., Dutta, T. K., Bandyopadhyay, S., & Singh, R. K. (2015). Molecular and phylogenetic characterization of multidrug resistant extended spectrum beta-lactamase producing Escherichia coli isolated from poultry and cattle in Odisha, India. Infection, Genetics and Evolution, 29, 82-90. https://doi.org/10.1016/j.meegid.2014.11.003
Karczmarczyk, M., Abbott, Y., Walsh, C., Leonard, N., & Fanning, S. (2011). Characterization of multidrug-resistant Escherichia coli isolates from animals presenting at a University Veterinary Hospital. Applied and Environmental Microbiology, 77(20), 7104-7112. https://doi.org/10.1128/AEM.00599-11
Kern, Z. T., Jacob, M. E., Gilbertie, J. M., Vaden, S. L., & Lyle, S. K. (2018). Characteristics of dogs with biofilm-forming Escherichia coli urinary tract infections. Journal of Veterinary Internal Medicine, 32(5), 1645-1651. https://doi.org/10.1111/jvim.15231
Kittinger, C., Lipp, M., Folli, B., Kirschner, A., Baumert, R., Galler, H., Grisold, A. J., Luxner, J., Weissenbacher, M., Farnleitner, A. H., & Zarfel, G. (2016). Enterobacteriaceae isolated from the River Danube: Antibiotic resistances, with a focus on the presence of ESBL and carbapenemases. PLoS ONE, 11(11), 1-17. https://doi.org/10.1371/journal.pone.0165820
Kojima, A., Ishii, Y., Ishihara, K., Esaki, H., Asai, T., Oda, C., Tamura, Y., Takahashi, T., & Yamaguchi, K. (2005). Extended-spectrum--lactamase-producing. Society, 49(8), 3533-3537.
Koovapra, S., Bandyopadhyay, S., Das, G., Bhattacharyya, D., Banerjee, J., Mahanti, A., Samanta, I., Nanda, P. K., Kumar, A., Mukherjee, R., Dimri, U., & Singh, R. K. (2016). Molecular signature of extended spectrum β-lactamase producing Klebsiella pneumoniae isolated from bovine milk in eastern and north-eastern India. Infection, Genetics and Evolution, 44, 395-402. https://doi.org/10.1016/j.meegid.2016.07.032
Lin, Z., Yuan, T., Zhou, L., Cheng, S., Qu, X., Lu, P., & Feng, Q. (2020). Impact factors of the accumulation, migration and spread of antibiotic resistance in the environment. Environmental Geochemistry and Health, 43(5), 1741-1758.
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 25(4), 402-408. https://doi.org/10.1006/meth.2001.1262
Magiorakos, A. P., Srinivasan, A., Carey, R. B., Carmeli, Y., Falagas, M. E., Giske, C. G., Harbarth, S., Hindler, J. F., Kahlmeter, G., Olsson-Liljequist, B., Paterson, D. L., Rice, L. B., Stelling, J., Struelens, M. J., Vatopoulos, A., Weber, J. T., & Monnet, D. L. (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
Manchanda, V., Rai, S., Gupta, S., Rautela, R. S., Chopra, R., Rawat, D. S., Verma, N., Singh, N. P., Kaur, I. R., & Bhalla, P. (2011). Development of TaqMan real-time polymerase chain reaction for the detection of the newly emerging form of carbapenem resistance gene in clinical isolates of Escherichia coli, Klebsiella pneumoniae, and Acinetobacter baumannii. Indian Journal of Medical Microbiology, 29(3), 249-253. https://doi.org/10.4103/0255-0857.83907
Manna, S. K., Das, R., & Manna, C. (2008). Microbiological quality of finfish and shellfish with special reference to shiga toxin-producing Escherichia coli O157. Journal of Food Science, 73(6), 283-286. https://doi.org/10.1111/j.1750-3841.2008.00815.x
Monteiro, J., Widen, R. H., Pignatari, A. C. C., Kubasek, C., & Silbert, S. (2012). Rapid detection of carbapenemase genes by multiplex real-time PCR. The Journal of Antimicrobial Chemotherapy, 67(4), 906-909. https://doi.org/10.1093/jac/dkr563
Mukherjee, R., Halder, D., Saha, S., Shyamali, R., Subhranshu, C., Ramakrishnan, R., Murhekar, M. V., & Hutin, Y. J. (2011). Five pond-centred outbreaks of cholera in villages of West Bengal, India: Evidence for focused interventions. Journal of Health, Population and Nutrition, 29(5), 421-428. https://doi.org/10.3329/jhpn.v29i5.8895
Ng, L. K., Martin, I., Alfa, M., & Mulvey, M. (2001). Multiplex PCR for the detection of tetracycline resistant genes. Molecular and Cellular Probes, 15(4), 209-215. https://doi.org/10.1006/mcpr.2001.0363
Nowrouzian, F. L., Adlerberth, I., & Wold, A. E. (2006). Enhanced persistence in the colonic microbiota of Escherichia coli strains belonging to phylogenetic group B2: Role of virulence factors and adherence to colonic cells. Microbes and Infection, 8(3), 834-840. https://doi.org/10.1016/j.micinf.2005.10.011
Olajide Ajayi, A., & Ifeanyin Okoh, A. (2014). Bacteriological study of pond water for aquaculture purposes. Journal of Food, Agriculture and Environment, 12(2), 1260-1265.
Pal, A., Dhara, L., & Tripathi, A. (2019). Contribution of acrB upregulation & OmpC/Ompk36 loss over the presence of bla (NDM) towards carbapenem resistance development among pathogenic Escherichia coli & Klebsiella spp. The Indian Journal of Medical Research, 149(4), 528-538. https://doi.org/10.4103/ijmr.IJMR_716_17
Ponnusamy, P., Natarajan, V., & Sevanan, M. (2012). In vitro biofilm formation by uropathogenic Escherichia coli and their antimicrobial susceptibility pattern. Asian Pacific Journal of Tropical Medicine, 5(3), 210-213. https://doi.org/10.1016/S1995-7645(12)60026-1
Preena, P. G., Swaminathan, T. R., Rejish Kumar, V. J., & Bright Singh, I. S. (2020). Unravelling the menace: Detection of antimicrobial resistance in aquaculture. Letters in Applied Microbiology, 71(1), 26-38. https://doi.org/10.1111/lam.13292
Rashid, M., Rakib, M. M., & Hasan, B. (2015). Antimicrobial-resistant and ESBL-producing Escherichia coli in different ecological niches in Bangladesh. Infection Ecology & Epidemiology, 5(1), 26712. https://doi.org/10.3402/iee.v5.26712
Ratajczak, M., Laroche, E., Berthe, T., Clermont, O., Pawlak, B., Denamur, E., & Petit, F. (2010). Influence of hydrological conditions on the Escherichia coli population structure in the water of a creek on a rural watershed. BMC Microbiology, 10(1), 222. https://doi.org/10.1186/1471-2180-10-222
Rayasam, S. D. G., Ray, I., Smith, K. R., & Riley, L. W. (2019). Extraintestinal pathogenic Escherichia coli and antimicrobial drug resistance in a Maharashtrian drinking water system. The American Journal of Tropical Medicine and Hygiene, 100(5), 1101-1104. https://doi.org/10.4269/ajtmh.18-0542
Silva, V. O., Soares, L. O., Chang, Y., & Moreira, M. A. S. (2014). Biofilm formation on biotic and abiotic surfaces in the presence of antimicrobials by Escherichia coli isolates from cases of bovine mastitis. Applied and Environmental Microbiology, 80(19), 6136-6145. https://doi.org/10.1128/AEM.01953-14
Singh, F., Hirpurkar, S. D., Rawat, N., Shakya, S., Kumar, R., Kumar, S., Meena, R. K., Rajput, P. K., & Kumar, J. (2020). Carbapenemase and ESBL genes with class 1 integron among fermenting and nonfermenting bacteria isolated from water sources from India. Letters in Applied Microbiology, 71(1), 70-77. https://doi.org/10.1111/lam.13228
Tacão, M., Moura, A., Correia, A., & Henriques, I. (2014). Co-resistance to different classes of antibiotics among ESBL-producers from aquatic systems. Water Research, 48(1), 100-107. https://doi.org/10.1016/j.watres.2013.09.021
Talukdar, P. K., Rahman, M., Rahman, M., Nabi, A., Islam, Z., Hoque, M. M., Endtz, H. P., & Islam, M. A. (2013). Antimicrobial resistance, virulence factors and genetic diversity of Escherichia coli isolates from household water supply in Dhaka, Bangladesh. PLoS ONE, 8(4), 1-8. https://doi.org/10.1371/journal.pone.0061090
Tang, M., Wei, X., Wan, X., Ding, Z., Ding, Y., & Liu, J. (2020). The role and relationship with efflux pump of biofilm formation in Klebsiella pneumoniae. Microbial Pathogenesis, 147, 104244. https://doi.org/10.1016/j.micpath.2020.104244
Varga, C., Guerin, M. T., Brash, M. L., Slavic, D., Boerlin, P., & Susta, L. (2019). Antimicrobial resistance in fecal Escherichia coli and Salmonella enterica isolates: A two-year prospective study of small poultry flocks in Ontario, Canada. BMC Veterinary Research, 15, 464. https://doi.org/10.1186/s12917-019-2187-z
Walk, S. T., Alm, E. W., Calhoun, L. M., Mladonicky, J. M., & Whittam, T. S. (2007). Genetic diversity and population structure of Escherichia coli isolated from freshwater beaches. Environmental Microbiology, 9(9), 2274-2288. https://doi.org/10.1111/j.1462-2920.2007.01341.x