DOI QR코드

DOI QR Code

Characterization of Extended Spectrum Beta-Lactamases (ESBL) Producing Escherichia coli Isolates from Surface Water Adjacent to Pharmaceutical Industries in Bangladesh: Antimicrobial Resistance and Virulence Pattern

  • Taslin Jahan Mou (Department of Microbiology, Jahangirnagar University) ;
  • Nasrin Akter Nupur (Department of Microbiology, Jahangirnagar University) ;
  • Farhana Haque (Department of Microbiology, Jahangirnagar University) ;
  • Md Fokhrul Islam (Institute of Quantitative Biology, Biochemistry and Biotechnology, School of Biological Sciences, The University of Edinburgh) ;
  • Md. Shahedur Rahman (Department of Genetic Engineering and Biotechnology, Jashore University of Science and Technology) ;
  • Md. Amdadul Huq (Department of Food and Nutrition, College of Biotechnology and Natural Resource, Chung-Ang University) ;
  • Anowar Khasru Parvez (Department of Microbiology, Jahangirnagar University)
  • 투고 : 2023.05.21
  • 심사 : 2023.07.19
  • 발행 : 2023.09.28

초록

The pharmaceutical industry in Bangladesh produces a diverse range of antibiotics for human and animal use, however, waste disposal management is inadequate. This results in substantial quantities of antibiotics being discharged into water bodies, which provide suitable environment for the growth of antibiotic-resistant bacteria, capable of spreading resistance genes. This study intended for exploring the bacterial antibiotic resistance profile in adjoining aquatic environmental sources of pharmaceutical manufacturing facilities in Bangladesh. Seven surface water samples were collected from the vicinity of two pharmaceutical industries located in the Savar area and 51 Escherichia coli isolates were identified using both phenotypic and genotypic methods. Antibiotic susceptibility tests revealed the highest percentage of resistance against ampicillin, azithromycin, and nalidixic acid (100%) and the lowest resistance against meropenem (1.96%) out of sixteen different antibiotics tested. 100% of the study E. coli isolates were observed with Multidrug resistance phenotypes, with the Multiple Antibiotic Resistance (MAR) value ranging from 0.6-1.0. Furthermore, 69% of the isolates were Extended Spectrum Beta-Lactamases (ESBL) positive as per the Double Disk Diffusion Synergy Test (DDST). ESBL resistance genes blaTEM, blaCTX-M-13, blaCTX-M-15, and blaSHV were detected in 70.6% (n = 36), 60.8% (n = 32), 54.9% (n = 28), and 1.96% (n = 1) of the isolates, respectively, by Polymerase Chain Reaction (PCR). Additionally, 15.68% (n = 8) of the isolates were positive for E. coli specific virulence genes in PCR. These findings suggest that pharmaceutical wastewater, if not properly treated, could be a formidable source of antibiotic resistance spread in the surrounding aquatic environment. Therefore, continued surveillance for drug resistance among bacterial populations around drug manufacturing facilities in Bangladesh is necessary, along with proper waste disposal management.

키워드

과제정보

The investigation has been supported by grants from the University Grant Commission (UGC), Ministry of Science and Technology, Bangladesh and Jahangirnagar University.

참고문헌

  1. Larsson DG J, Flach CF. 2022. Antibiotic resistance in the environment. Nat. Rev. Microbiol. 20: 257-269.
  2. Miao J, Yin Z, Yang Y, Liang Y, Shi H, Xu X. 2022. Investigation of the microbial community structure and diversity in the environment surrounding a veterinary antibiotic production factory. RSC Adv. 12: 1021-1027.
  3. Zhu Y, Huang WE, Yang Q. 2022. Clinical perspective of antimicrobial resistance in bacteria. Infect. Drug Res. 15: 735-746.
  4. Tan L, Li L, Ashbolt N, Wang X, Cui Y, Zhu X, et al. 2018. Arctic antibiotic resistance gene contamination, a result of anthropogenic activities and natural origin. Sci. Total Environ. 621: 1176-1184.
  5. Koch N, Islam NF, Sonowal S, Prasad R, Sarma H. 2021. Environmental antibiotics and resistance genes as emerging contaminants: Methods of detection and bioremediation. Curr. Res. Microb. Sci. 2: 100027.
  6. Karkman A, Do TT, Walsh F, Virta MPJ. 2018. Antibiotic-resistance genes in waste water. Trends Microbiol. 26: 220-228.
  7. Hanna N, Tamhankar AJ, Stalsby Lundborg C. 2023. Antibiotic concentrations and antibiotic resistance in aquatic environments of the WHO Western Pacific and South-East Asia regions: a systematic review and probabilistic environmental hazard assessment. Lancet Planet. Health 7: e45-e54.
  8. Anh HQ, Le TPQ, Da Le N, Lu XX, Duong TT, Garnier J, et al. 2021. Antibiotics in surface water of East and Southeast Asian countries: A focused review on contamination status, pollution sources, potential risks, and future perspectives. Sci. Total Environ. 764: 142865.
  9. Ramos S, Silva V, Dapkevicius MLE, Canica M, Tejedor-Junco MT, Igrejas G, et al. 2020. Escherichia coli as commensal and pathogenic bacteria among food-producing animals: Health implications of extended spectrum β-lactamase (ESBL) Production. Animals 10: 2239.
  10. Jang J, Hur HG, Sadowsky MJ, Byappanahalli MN, Yan T, Ishii S. 2017. Environmental Escherichia coli: ecology and public health implications-a review. J. Appl. Microbiol. 123: 570-581.
  11. Kawamura K, Nagano N, Suzuki M, Wachino JI, Kimura K, Arakawa Y. 2017. ESBL-producing Escherichia coli and its rapid rise among healthy people. Food Saf. 5: 122-150.
  12. Parvez AK, Taslin TJM, Feroz, A. 2017. Extended Spectrum Beta-Lactamase (ESBL) producing enterobacteria in aquatic environmental sources of Bangladesh. Int. Biol. Biomed. J. 3: 21-24.
  13. Subramanya SH, Bairy I, Metok Y, Baral BP, Gautam D, Nayak N. 2021. Detection and characterization of ESBL-producing Enterobacteriaceae from the gut of subsistence farmers, their livestock, and the surrounding environment in rural Nepal. Sci. Rep. 11: 2091.
  14. Sultan I, Siddiqui MT, Gogry FA, Haq QMR. 2022. Molecular characterization of resistance determinants and mobile genetic elements of ESBL producing multidrug-resistant bacteria from freshwater lakes in Kashmir, India. Sci. Total Environ. 827: 154221.
  15. Franz E, Veenman C, van Hoek AH, de Roda Husman A, Blaak H. 2015. Pathogenic Escherichia coli producing extended-spectrum β-lactamases isolated from surface water and wastewater. Sci. Rep. 5: 14372.
  16. Dihan MR, Abu Nayeem SM, Roy H, Islam MS, Islam A, Alsukaibi AKD, et al. 2023. Healthcare waste in Bangladesh: Current status, the impact of Covid-19 and sustainable management with life cycle and circular economy framework. Sci. Total Environ. 871: 162083.
  17. Talukdar PK, Rahman M, Rahman M, Nabi A, Islam Z, Hoque MM, et al. 2013. Antimicrobial resistance, virulence factors and genetic diversity of Escherichia coli isolates from household water supply in Dhaka, Bangladesh. PLoS One 8: e61090.
  18. Cleuziat P, Robert-Baudouy J. 1990. Specific detection of Escherichia coli and Shigella species using fragments of genes coding for beta-glucuronidase. FEMS Microbiol. Lett. 60: 315-322.
  19. Sultana M, Mou TJ, Sanyal SK, Diba F, Mahmud ZH, Parvez AK, et al. 2017. Investigation of arsenotrophic microbiome in arsenic-affected Bangladesh groundwater. Ground Water 55: 736-746.
  20. Titilawo Y, Obi L, Okoh A. 2015. Occurrence of virulence gene signatures associated with diarrhoeagenic and non-diarrhoeagenic pathovars of Escherichia coli isolates from some selected rivers in South-Western Nigeria. BMC Microbiol. 15: 204.
  21. Bauer AW, Kirby WM, Sherris JC, Turck M. 1966. Antibiotic susceptibility testing by a standardized single disk method. Am. J. Clin. Pathol. 45: 493-496.
  22. Ahmed I, Haque F, Rahman MT, Parvez MAK, Mou TJ. 2020. Screening of methyl red degrading bacteria isolated from textile effluents of Savar area, Dhaka, Bangladesh. Adv. Biosci. Biotechnol. 11: 301-318.
  23. Zainab SM, Junaid M, Xu N, Malik RN. 2020. Antibiotics and antibiotic resistant genes (ARGs) in groundwater: A global review on dissemination, sources, interactions, environmental and human health risks. Water Res. 187: 116455.
  24. Bengtsson-Palme J, Milakovic M, Svecova H, Ganjto M, Jonsson V, Grabic R, et al. 2019. Industrial wastewater treatment plant enriches antibiotic resistance genes and alters the structure of microbial communities. Water Res. 162: 437-445.
  25. Nguyen AQ, Vu HP, Nguyen LN, Wang Q, Djordjevic SP, Donner E, et al. 2021. Monitoring antibiotic resistance genes in wastewater treatment: Current strategies and future challenges. Sci. Total Environ. 783: 146964.
  26. Manoharan RK, Ishaque F, Ahn YH. 2022. Fate of antibiotic resistant genes in wastewater environments and treatment strategies - A review. Chemosphere 298: 134671.
  27. Hassoun-Kheir N, Stabholz Y, Kreft JU, de la Cruz R, Romalde JL, Nesme J, et al. 2020. Comparison of antibiotic-resistant bacteria and antibiotic resistance genes abundance in hospital and community wastewater: A systematic review. Sci. Total Environ. 743: 140804.
  28. Guenther S, Ewers C, Wieler LH. 2011. Extended-spectrum Beta-lactamases producing E. coli in wWildlife, yet another form of environmental pollution?. Front. Microbiol. 2: 246.
  29. Rahman A, Jahanara I, Jolly YN. 2021. Assessment of physicochemical properties of water and their seasonal variation in an urban river in Bangladesh. Water Sci. Eng. 14: 139e148.
  30. Mira P, Lozano-Huntelman N, Johnson A, Savage VM, Yeh P. 2022. Evolution of antibiotic resistance impacts optimal temperature and growth rate in Escherichia coli and Staphylococcus epidermidis. J. Appl. Microbiol. 133: 2655-2667.
  31. Martinez JL, Baquero F. 2014. Emergence and spread of antibiotic resistance: setting a parameter space. Upsala J. Med. Sci. 119: 68-77.
  32. Poire L, Madec JY, Lupo A, Schink AK, Kieffer N, Nordmann P, et al. 2018. Antimicrobial Resistance in Escherichia coli. Microbiol. Spectrum 6: 10.1128/microbiolspec. ARBA-0026-2017.
  33. Ouyang Y, Nkedi-Kizza P, Wu QT, Shinde D, Huang CH. 2006. Assessment of seasonal variations in surface water quality. Water Res. 40: 3800-3810.
  34. Vaz-Moreira I, Nunes OC, Manaia CM. 2014. Bacterial diversity and antibiotic resistance in water habitats: searching the links with the human microbiome. FEMS Microbiol. Rev. 38: 761-778.
  35. Leong SS, Ismail J, Denil NA, Sarbini SR, Wasli W, Debbie A. 2018. Microbiological and physicochemical water quality assessments of river water in an industrial region of the Northwest coast of Borneo. Water 10: 1648.
  36. Fagerstrom A, Molling P, Khan FA, Sundqvist M, Jass J, Soderquist B. 2019. Comparative distribution of extended-spectrum beta-lactamase-producing Escherichia coli from urine infections and environmental waters. PLoS One 14: e0224861.
  37. Ibrahim IA, Al-Shwaikh RM, Ismaeil MI. 2014. Virulence and antimicrobial resistance of Escherichia coli isolated from Tigris River and children diarrhea. Infect. Drug Res. 7: 317-322.
  38. Odonkor ST, Addo KK. 2018. Prevalence of mltidrug-rsistant Escherichia coli iolated from dinking wter surces. Int. J. Microbiol. 2018: 7204013.
  39. Williams-Nguyen J, Sallach JB, Bartelt-Hunt S, Boxall AB, Durso LM, McLain JE, et al. 2016. Antibiotics and antibiotic resistance in agroecosystems: State of the science. J. Environ. Qual. 45: 394-406.
  40. Coleman BL, Salvadori MI, McGeer AJ, Sibley KA, Neumann NF, Bondy SJ, et al. 2012. The role of drinking water in the transmission of antimicrobial-resistant E. coli. Epidemiol. Infect. 140: 633-642.
  41. Teshome A, Alemayehu T, Deriba W, Ayele Y. 2020. Antibiotic resistance profile of bacteria isolated from wastewater systems in Eastern Ethiopia. J. Environ. Public Health 2020: 2796365.
  42. Rahman MM, Haq JA, Hossain MA, Sultana R, Islam F, Islam AH. 2004. Prevalence of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in an urban hospital in Dhaka, Bangladesh. Int. J. Antimicrob. Agents 24: 508-510.
  43. Mahmud ZH, Kabir MH, Ali S, Moniruzzaman M, Imran KM, Nafiz TN, et al. 2020. Extended-spectrum beta-Lactamase-producing Escherichia coli in drinking water samples from a forcibly displaced, densely populated community setting in Bangladesh. Front. Public Health 8: 228.
  44. Islam MS, Rahman AMM T, Hassan J, Rahman MT. 2020. Extended-spectrum beta-lactamase in Escherichia coli isolated from humans, animals, and environments in Bangladesh: A One Health perspective systematic review and meta-analysis. One Health 16: 100526.
  45. Castanheira M, Simner PJ, Bradford PA. 2021. Extended-spectrum β-lactamases: an update on their characteristics, epidemiology and detection. JAC-Antimicrob. Res. 3: dlab092. 10.1093/jacamr/dlab092.
  46. Pitout JD. 2010. Infections with extended-spectrum beta-lactamase-producing enterobacteriaceae: changing epidemiology and drug treatment choices. Drugs 70: 313-333.
  47. Moglad E, Adam OJ, Alnosh M, Altayb H. 2020. Detection of virulence genes of diarrheagenic Escherichia coli strains from drinking water in Khartoum State. J. Water Health jwh2020097, doi: 10.2166/wh.2020.097.
  48. Crofts AA, Giovanetti SM, Rubin EJ, Poly FM, Gutierrez RL, Talaat KR, et al. 2018. Enterotoxigenic E. coli virulence gene regulation in human infections. Proc. Natl. Acad. Sci. USA 115: E8968-E8976.
  49. Lauber CL, Glatzer L, Sinsabaugh RL. 2003. Prevalence of pathogenic Escherichia coli in recreational waters. J. Great Lakes Res. 29: 301-306.
  50. Hamilton MJ, Hadi AZ, Griffith JF, Ishii S, Sadowsky MJ. 2010. Large scale analysis of virulence genes in Escherichia coli strains isolated from Avalon Bay, CA. Water Res. 44: 5463-5473.
  51. Pishtiwan AH, Khadija KM. 2019. Prevalence of blaTEM, blaSHV, and blaCTX-M Genes among ESBL-producing Klebsiella pneumoniae and Escherichia coli isolated from Thalassemia patients in Erbil, Iraq. Mediterr. J. Hematol. Infect. Dis. 11: e2019041.
  52. Muzaheed, Sattar Shaikh N, Sattar Shaikh S, Acharya S, Sarwar Moosa S, Habeeb Shaikh M, et al. 2021. Molecular epidemiological surveillance of CTX-M-15-producing Klebsiella pneumoniae from the patients of a teaching hospital in Sindh, Pakistan. F1000Res. 10: 444.
  53. Eckert C, Gautier V, Saladin-Allard M, Hidri N, Verdet C, Ould-Hocine Z, et al. 2004. Dissemination of CTX-M-type beta-lactamases among clinical isolates of Enterobacteriaceae in Paris, France. Antimicrob. Agents Chemother. 48: 1249-1255.
  54. Ibrahim RA, Cryer TL, Lafi SQ, Basha EA, Good L, Tarazi YH. 2019. Identification of Escherichia coli from broiler chickens in Jordan, their antimicrobial resistance, gene characterization and the associated risk factors. BMC Vet. Res. 15: 159.
  55. Stacy-Phipps S, Mecca JJ, Weiss JB. 1995. Multiplex PCR assay and simple preparation method for stool specimens detect enterotoxigenic Escherichia coli DNA during course of infection. J. Clin. Microbiol. 33: 1054-1059.