Antibiotic-Resistant Escherichia coli Isolated from Duck Cloacal and Tap Water Samples at Live Bird Markets in Bangladesh

Document Type : Original Paper

Authors

1 Antimicrobial Resistance Action Center (ARAC), Bangladesh Livestock Research Institute (BLRI), Savar, Dhaka-1341, Bangladesh

2 Department of Public Health and Informatics, Jahangirnagar University, Savar, Dhaka-1342, Bangladesh

3 Microbiology and Antibiotic Resistance Team (MicroART), Department of Veterinary Sciences, University of Trás-os-Montes and Alto Douro (UTAD), 5000-801 Vila Real, Portugal

4 Department of Microbiology and Veterinary Public Health, Faculty of Veterinary Medicine, Chattogram Veterinary and Animal Sciences University, Chattogram-4225, Bangladesh

Abstract

Antibiotic resistance is a growing concern all over the world. The current study sought to identify antimicrobial resistance (AMR) patterns and antibiotic-resistant genes in Escherichia coli (E. coli) isolated from seemingly healthy ducks and neighboring tap water sources at three separate live bird markets (LBMs) in Chattogram, Bangladesh. A total of ninety cloacal swab samples of Khaki Campbell ducks and fifteen water samples from nearby tap water sources were collected from three LBMs. Several cultural and molecular tests were conducted to determine  E. coli contamination. The disk diffusion technique was used to evaluate the antibiotic sensitivity of E. coli isolates to 12 different antibiotics. For each isolate, a Multiple Antibiotic Resistance (MAR) index was calculated. The resistance genes were detected using a polymerase chain reaction (PCR) assay. The overall prevalence of E. coli in feces and tap water samples was 64.4% (58/90, 95% CI 54.1-73.6) and 100% (15/15, 95% CI 76.1-100), respectively. Both fecal and water isolates showed 100% resistance to ampicillin, tetracycline, and nalidixic acid. Resistance to other antibiotics was also found to be high. Multidrug- resistance (MDR) was unveiled in all fecal (58/58) and water (15/15) isolates. MAR index ranged from 0.33 to 0.67 in all recovered isolates. Both fecal and water E. coli isolates harbored blaTEM, tetA, sul1, and sul2 genes. The resistance genes in MDR E. coli in live bird markets might transmit from ducks to humans and they, therefore local authorities should consider this issue a major public health risk.

Keywords


Abd El Tawab A, Ammar A, Nasef S & Reda R. 2015. Prevalence of E. coli in diseased chickens with its antibiogram pattern. Benha Veterinary Medical Journal, 28(2): 224–230. DOI: 10.21608/bvmj.2015.32507
Adelowo OO, Fagade OE & Agersø Y. 2014. Antibiotic resistance and resistance genes in Escherichia coli from poultry farms, southwest Nigeria. Journal of Infection in Developing Countries, 8(9): 1103–1112. DOI: 10.3855/jidc.4222
Adzitey F, Ali GRR, Huda N & Ting SL. 2013. Antibiotic resistance and plasmid profile of Escherichia coli isolated from ducks in Penang, Malaysia. International Food Research Journal, 20(3): 1473–1478.
Azad M, Rahman MM, Amin R, Begum M, Fries R, Husna A, Khairalla AS, Badruzzaman AT, El Zowalaty ME, Lampang KN & Ashour HM.  2019. Susceptibility and Multidrug Resistance Patterns of Escherichia coli Isolated from Cloacal Swabs of Live Broiler Chickens in Bangladesh. Pathogens (Basel, Switzerland), 8(3): 118. DOI: 10.3390/pathogens8030118
Batchelor M, Hopkins K, Threlfall E J, Clifton-Hadley FA, Stallwood AD, Davies RH & Liebana E. 2005. blaCTX-M genes in clinical Salmonella isolates recovered from humans in England and Wales from 1992 to 2003. Antimicrobial Agents and Chemotherapy, 49(4): 1319–1322. DOI: 10.1128/AAC.49.4.1319-1322.2005
Belaaouaj A, Lapoumeroulie C, Caniça MM, Vedel G, Névot P, Krishnamoorthy R & Paul G. 1994. Nucleotide sequences of the genes coding for the TEM-like β-lactamases IRT-1 and IRT-2 (formerly called TRI-1 and TRI-2).           FEMS Microbiology Letters, 120(1–2): 75–80. DOI: 10.1111/j.1574-6968.1994.tb07010.x
Beninati C, Reich F, Muscolino D, Giarratana F, Panebianco A, Klein G & Atanassova V. 2015. ESBL-producing bacteria and MRSA isolated from poultry and turkey products imported from Italy. Czech Journal of Food Sciences, 33(2): 97–102. DOI: 10.17221/428/2014-CJFS
Čižman M. 2003. The use and resistance to antibiotics in the community. International Journal of Antimicrobial Agents, 21(4): 297–307. DOI: 10.1016/S0924-8579(02)00394-1
CLSI. 2015. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-fifth informational supplement, Document M100-S25. Clinical and Laboratory Standards Institute, Wayne, PA.
Dube N & Mbanga J. 2018. Molecular characterization and antibiotic resistance patterns of avian fecal Escherichia coli from turkeys, geese, and ducks. Veterinary World, 11(6): 859–867. DOI: 10.14202/vetworld.2018.859-867
FDA. 2014. National antimicrobial resistance monitoring system. http://www.fda.gov/AnimalVeterinary/SafetyHealth/AntimicrobialResistance/NationalAntimicrobialResistanceMonitoring System/default.htm [accessed on 10 November (2020)]
Hamid MA, Rahman MA, Ahmed S & Hossain KM. 2016. Status of poultry industry in Bangladesh and the role of private sector for its development. Asian Journal of Poultry Science, 11(1): 1–13. DOI: 10.3923/ajpsaj.2017.1.13
Jain P, Bepari AK, Sen PK, Rafe T, Imtiaz R, Hossain M & Reza HM. 2021. High prevalence of multiple antibiotic resistance in clinical E. coli isolates from Bangladesh and prediction of molecular resistance determinants using WGS of an XDR isolate. Scientific Reports, 11(1): 22859. DOI: 10.1038/s41598-021-02251-w
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. DOI: 10.1128/AEM.00599-11
Kissinga HD, Mwombeki F, Said K, Katakweba AAS, Nonga HE & Muhairwa AP. 2018. Antibiotic susceptibilities of indicator bacteria Escherichia coli and Enterococci spp. isolated from ducks in Morogoro Municipality, Tanzania. BMC Research Notes, 11(1): 4–9. DOI: 10.1186/s13104-018-3201-4
Lanz R, Kuhnert P & Boerlin P. 2003. Antimicrobial resistance and resistance gene determinants in clinical Escherichia coli from different animal species in Switzerland. Veterinary Microbiology, 91(1): 73–84. DOI: 10.1016/S0378-1135(02)00263-8
Layman DK & Rodriguez NR. 2009. Egg protein as a source of power, strength, and energy. Nutrition Today, 44(1): 43–48. DOI: 10.1097/NT.0b013e3181959cb2
Li B, Ma L, Li Y, Jia H, Wei J, Shao D, Liu, K, Shi Y, Qiu Y & Ma Z. 2017. Antimicrobial resistance of Campylobacter species isolated from broilers in live bird markets in shanghai, China. Foodborne Pathogens and Disease, 14(2): 96–102. DOI: 10.1089/fpd.2016.2186
McEwen SA, Aarestrup FM & Jordan D. 2019. Monitoring of Antimicrobial Resistance in Animals: Principles and Practices. Antimicrobial Resistance in Bacteria of Animal Origin, 388: 397–413. DOI: 10.1128/9781555817534.ch23
Mishra M, Patel AK & Behera N. 2013. Prevalence of multidrug resistant E. coli in the river Mahanadi of Sambalpur. Current Research in Microbiology and Biotechnology, 1(5): 239-244.
Ng LK, Martin I, Alfa M & Mulvey M. 2001. Multiplex PCR for the detection of tetracycline resistant genes. Molecular and Cellular Probes, 15(4): 209–215. DOI: 10.1006/mcpr.2001.0363
Paul S, Bezbaruah RL, Roy MK & Ghosh AC. 1997. Multiple antibiotic resistance (MAR) index and its reversion in Pseudomonas aeruginosa. Letters in Applied Microbiology, 24(3): 169-71. DOI: 10.1046/j.1472-765x.1997.00364.x
Rahman MM, Bashar T, Rahman M, Rabbi FA & Noor R. 2011. Enterotoxin profiling and antibiogram of Escherichia coli isolated from poultry feces in Dhaka district of Bangladesh. Stamford Journal of Microbiology, 1(1): 51–57. DOI: 10.3329/sjm.v1i1.9134
Sánchez S, Martínez R, García A, Benítez JM, Blanco J, Blanco JE, Dahbi G, López C, Mora A & Alonso JM. 2010. Variation in the prevalence of non-O157 Shiga toxin-producing Escherichia coli in four sheep flocks during a 12-month longitudinal study. Small Ruminant Research, 93(2-3): 144-148. DOI: 10.1016/j.smallrumres.2010.05.014
Sarker MS, Mannan MS, Ali MY, Bayzid M, Ahad A & Bupasha ZB. 2019a. Antibiotic resistance of Escherichia coli isolated from broilers sold at live bird markets in Chattogram, Bangladesh. Journal of Advanced Veterinary and Animal Research, 6(3): 272–277. DOI: 10.5455/javar.2019.f344
Sarker MS, Ahad A, Ghosh, SK, Mannan MS, Sen A, Islam S & Bayzid M, Bupasha ZB. 2019b. Antibiotic-resistant Escherichia coli in deer and nearby water sources at Safari parks in Bangladesh. Veterinary World, 12(10): 1578–1583. DOI: 10.14202/vetworld.2019.1578-1583
Seidavi A, Mirhosseini SZ, Shivazad M, Chamani M, Sadeghi AA & Pourseify R. 2010. Detection and investigation of Escherichia coli in contents of duodenum, jejunum, ileum and cecum of broilers at different ages by PCR. Asia Pacific Journal of Molecular Biology and Biotechnology, 18: 321-326.
Siddiky NA, Sarker MS, Khan MSR, Begum R, Kabir ME, Karim MR, Rahman MT, Mahmud A & Samad MA. 2021. Virulence and antimicrobial resistance profiles of salmonella enterica serovars isolated from chicken at wet markets in Dhaka, Bangladesh. Microorganisms, 9: 952. DOI: 10.3390%2Fmicroorganisms9050952
Singh A, Khan MSR, Saha S, Hassan J & Roy U. 2013. Isolation and detection of antibiotic sensitivity pattern of escherichia coli from ducks in Bangladesh and Nepal. Microbes and Health, 1(1): 6–8. DOI: 10.3329/mh.v1i1.13704
Sunde M. 2005. Prevalence and characterization of class 1 and class 2 integrons in Escherichia coli isolated from meat and meat products of Norwegian origin. Journal of Antimicrobial Chemotherapy, 56(6): 1019–1024. DOI: 10.1093/jac/dki377
Tao R, Ying GG, Su HC, Zhou HW & Sidhu JPS. 2010. Detection of antibiotic resistance and tetracycline resistance genes in Enterobacteriaceae isolated from the Pearl rivers in South China. Environmental Pollution,  158(6): 2101–2109. DOI: 10.1016/j.envpol.2010.03.004
Thenmozhi S, Rajeswari P, Kumar BS, Saipriyanga V, Kalpana M. 2014. Multi-drug resistant patterns of biofilm forming Aeromonas hydrophila from urine samples. International Journal of Pharmaceutical Sciences and Research, 5(7): 2908. DOI: 10.13040/IJPSR.0975-8232.5(7). 2908-18
van den Bogaard AE, London N, Driessen C & Stobberingh EE. 2001. Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. Journal of Antimicrobial Chemotherapy, 47(6): 763–771. DOI: 10.1093/jac/47.6.763
Yang B, Qu D, Zhang X, Shen J, Cui S, Shi Y & Wang D. 2010. Prevalence and characterization of Salmonella serovars in retail meats of marketplace in Shaanxi, China. International Journal of Food Microbiology, 141(1–2): 63–72. DOI: 10.1016/j.ijfoodmicro.2010.04.015
Zhong CY, Cheng AC, Wang MS, Zhu DK, Luo QH, De Zhong C, et al. 2009. Antibiotic susceptibility of riemerella anatipestifer field isolates. Avian Diseases, 53(4): 601–607. DOI: 10.1637/8552-120408-ResNote.1
Zhu Y, Lai H, Zou L, Yin S, Wang C, Han X, Xia X, Hu K, He L, Zhou K & Chen S. 2017. Antimicrobial resistance and resistance genes in Salmonella strains isolated from broiler chickens along the slaughtering process in China. International journal of food microbiology, 259: 43-51. DOI: 10.1016/j.ijfoodmicro.2017.07.023