Journal of Veterinary Science

The Korean Society of Veterinary Science (대한수의학회)
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Meat ducks as carriers of antimicrobial-resistant Escherichia coli harboring transferable R plasmids

  • Zulqarnain Baqar (Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong) ;
  • Nuananong Sinwat (Departments of Farm Resources and Production Medicine, Faculty of Veterinary Medicine, Kasetsart University) ;
  • Rangsiya Prathan (Research Unit for Microbial Food Safety and Antimicrobial Resistance, Department of Veterinary Public Health, Faculty of Veterinary Science, Chulalongkorn University) ;
  • Rungtip Chuanchuen (Research Unit for Microbial Food Safety and Antimicrobial Resistance, Department of Veterinary Public Health, Faculty of Veterinary Science, Chulalongkorn University)
  • Received : 2024.02.24
  • Accepted : 2024.07.11
  • Published : 2024.09.30
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Abstract

Importance: Antimicrobial resistance (AMR) is a serious public health threat. AMR bacteria and their resistance determinants in food can be transmitted to humans through the food chain and by direct contact and disseminate directly to the environment. Objective: This study examined the AMR characteristics and transferable R plasmids in Escherichia coli isolated from meat ducks raised in an open-house system. Methods: One hundred seventy-seven (n = 177) commensal E. coli were examined for their antimicrobial susceptibilities and horizontal resistance transfer. The plasmids were examined by PCR-based plasmid replicon typing (PBRT) and plasmid multi-locus sequence typing (pMLST). Results: The highest resistance rate was found against ampicillin (AMP, 83.0%) and tetracycline (TET, 81.9%), and most isolates exhibited multidrug resistance (MDR) (86.4%). The R plasmids were conjugally transferred when TET (n = 4), AMP (n = 3), and chloramphenicol (n = 3) were used as a selective pressure. The three isolates transferred resistance genes either in AMP or TET. The blaCTX-M1 gene resided on conjugative plasmids. Five replicon types were identified, of which Inc FrepB was most common in the donors (n = 13, 38.4%) and transconjugants (n = 16, 31.2%). Subtyping F plasmids revealed five distinct replicons combinations, including F47:A-:B- (n = 2), F29:A-:B23 (n = 1), F29:A-:B- (n = 1), F18:A-B:- (n = 1), and F4:A-:B- (n = 1). The chloramphenicol resistance was significantly correlated with the other AMR phenotypes (p < 0.05). Conclusions and Relevance: The meat ducks harbored MDR E. coli and played an important role in the environmental dissemination of AMR bacteria and its determinants. This confirms AMR as a health issue, highlighting the need for routine AMR monitoring and surveillance of meat ducks.

Keywords

Acknowledgement

The authors thank the Department of Veterinary Public Health, Faculty of Veterinary Science, Chulalongkorn University, Bangkok, Thailand, and Chulalongkorn University One Healthy Research Cluster for laboratory provision and technical assistance.

References

  1. Pokharel S, Raut S, Adhikari B. Tackling antimicrobial resistance in low-income and middle-income countries. BMJ Glob Health. 2019;4(6):e002104.
  2. Chantharothaiphaichit T, Phongaran D, Angkittitrakul S, Aunpromma S, Chuanchuen R. Clinically healthy household dogs and cats as carriers of multidrug-resistant Salmonella enterica with variable R plasmids. J Med Microbiol. 2022;71(2):001488.
  3. Osman M, Al Mir H, Rafei R, Dabboussi F, Madec JY, Haenni M, et al. Epidemiology of antimicrobial resistance in Lebanese extra-hospital settings: An overview. J Glob Antimicrob Resist. 2019;17:123-129.
  4. Jalaludeen A, Churchil RR. Duck production: an overview. In: Jalaludeen A, Churchil RR, Baeza E, eds. Duck Production and Management Strategies. Springer Singapore; 2022: p1-55.
  5. Sinwat N, Witoonsatian K, Chumsing S, Suwanwong M, Kankuntod S, Jirawattanapong P, et al. Antimicrobial resistance phenotypes and genotypes of Salmonella spp. isolated from commercial duck meat production in Thailand and their minimal inhibitory concentration of disinfectants. Microb Drug Resist. 2021;27(12):1733-1741.
  6. Food and Agriculture Organization (FAO). Indigenous Duck Meat Production in the World. FAO; 2018.
  7. Charoensook R, Tartrakoon W, Incharoen T, Numthuam S, Pechrkong T, Nishibori M. Production system characterization of local indigenous chickens in lower Northern Thailand. Khon Kaen Agr J. 2021;49:1337-1350.
  8. Office of Agricultural Economic (OIE). Agricultural Statistics of Thailand 2015. OIE; 2016.
  9. Ministry of Agriculture and Cooperatives (MOAC). Announcement of Ministry of Agriculture and Cooperatives: Determining the Names, Types, Kinds, Characteristics, or Properties of Substances Prohibited from Use in Animal Feed. Royal Thai Government Gazette; 2015.
  10. Ministry of Agriculture and Cooperatives (MOAC). Announcement of Ministry of Agriculture and Cooperatives: Determination of Characteristics and Conditions of Animal Feed Mixed with Prohibited Substances. Royal Thai Government Gazette; 2018.
  11. Ministry of Agriculture and Cooperatives, Department of Livestock Development. Specify a List of Drugs That Must Not Be Mixed in Animal Feed for Prophylactic Purposes. Royal Thai Government Gazette; 2019.
  12. European Food Safety Authority (EFSA), Aerts M, Battisti A, Hendriksen R, Kempf I, Teale C, et al. Technical specifications on harmonised monitoring of antimicrobial resistance in zoonotic and indicator bacteria from food-producing animals and food. EFSA J. 2019;17(6):e05709.
  13. Madec JY, Haenni M. Antimicrobial resistance plasmid reservoir in food and food-producing animals. Plasmid. 2018;99:72-81.
  14. Moser AI, Kuenzli E, Campos-Madueno EI, Budel T, Rattanavong S, Vongsouvath M, et al. Antimicrobial-resistant Escherichia coli strains and their plasmids in people, poultry, and chicken meat in Laos. Front Microbiol. 2021;12:708182.
  15. Aworh MK, Kwaga JK, Hendriksen RS, Okolocha EC, Thakur S. Genetic relatedness of multidrug resistant Escherichia coli isolated from humans, chickens and poultry environments. Antimicrob Resist Infect Control. 2021;10(1):58.
  16. Wheeler NE, Price V, Cunningham-Oakes E, Tsang KK, Nunn JG, Midega JT, et al. Innovations in genomic antimicrobial resistance surveillance. Lancet Microbe. 2023;4(12):e1063-e1070.
  17. Rozwandowicz M, Brouwer MS, Fischer J, Wagenaar JA, Gonzalez-Zorn B, Guerra B, et al. Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. J Antimicrob Chemother. 2018;73(5):1121-1137.
  18. Carattoli A. Resistance plasmid families in Enterobacteriaceae. Antimicrob Agents Chemother. 2009;53(6):2227-2238.
  19. Carattoli A. Plasmids and the spread of resistance. Int J Med Microbiol. 2013;303(6-7):298-304.
  20. Trongjit S, Angkititrakul S, Tuttle RE, Poungseree J, Padungtod P, Chuanchuen R. Prevalence and antimicrobial resistance in Salmonella enterica isolated from broiler chickens, pigs and meat products in Thailand-Cambodia border provinces. Microbiol Immunol. 2017;61(1):23-33.
  21. Trongjit S, Angkittitrakul S, Chuanchuen R. Occurrence and molecular characteristics of antimicrobial resistance of Escherichia coli from broilers, pigs and meat products in Thailand and Cambodia provinces. Microbiol Immunol. 2016;60(9):575-585.
  22. Puangseree J, Prathan R, Srisanga S, Angkittitrakul S, Chuanchuen R. Plasmid profile analysis of Escherichia coli and Salmonella enterica isolated from pigs, pork and humans. Epidemiol Infect. 2022;150:e110.
  23. Pungpian C, Sinwat N, Angkititrakul S, Prathan R, Chuanchuen R. Presence and transfer of antimicrobial resistance determinants in Escherichia coli in pigs, pork, and humans in Thailand and Lao PDR border provinces. Microb Drug Resist. 2021;27(4):571-584.
  24. Authority EF. Report from the Task Force on Zoonoses Data Collection including guidance for harmonized monitoring and reporting of antimicrobial resistance in commensal Escherichia coli and Enterococcus spp. from food animals. EFSA J. 2008;6(4):141r.
  25. Feng P, Weagant SD, Grant MA, Burkhardt W, Shellfish M, Water B. BAM: enumeration of Escherichia coli and the Coliform bacteria. In: Bacteriological Analytical Manual. U.S. Food and Drug Administration; 2002: p1-13.
  26. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. CLSI; 2018.
  27. Levesque C, Piche L, Larose C, Roy PH. PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrob Agents Chemother. 1995;39(1):185-191.
  28. Hasman H, Mevius D, Veldman K, Olesen I, Aarestrup FM. β-Lactamases among extended-spectrum β-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. J Antimicrob Chemother. 2005;56(1):115-121.
  29. Dallenne C, Da Costa A, Decre D, Favier C, Arlet G. Development of a set of multiplex PCR assays for the detection of genes encoding important β-lactamases in Enterobacteriaceae. J Antimicrob Chemother. 2010;65(3):490-495.
  30. Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ. Identification of plasmids by PCR-based replicon typing. J Microbiol Methods. 2005;63(3):219-228.
  31. Carattoli A, Zankari E, Garcia-Fernandez A, Voldby Larsen M, Lund O, Villa L, et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58(7):3895-3903.
  32. Villa L, Garcia-Fernandez A, Fortini D, Carattoli A. Replicon sequence typing of IncF plasmids carrying virulence and resistance determinants. J Antimicrob Chemother. 2010;65(12):2518-2529.
  33. Kissinga HD, Mwombeki F, Said K, Katakweba AA, Nonga HE, Muhairwa AP. Antibiotic susceptibilities of indicator bacteria Escherichia coli and Enterococci spp. isolated from ducks in Morogoro Municipality, Tanzania. BMC Res Notes. 2018;11(1):87.
  34. Na SH, Moon DC, Choi MJ, Oh SJ, Jung DY, Sung EJ, et al. Antimicrobial resistance and molecular characterization of extended-spectrum β-lactamase-producing Escherichia coli isolated from ducks in South Korea. Foodborne Pathog Dis. 2019;16(12):799-806.
  35. Yassin AK, Gong J, Kelly P, Lu G, Guardabassi L, Wei L, et al. Antimicrobial resistance in clinical Escherichia coli isolates from poultry and livestock, China. PLoS One. 2017;12(9):e0185326.
  36. Van TT, Nguyen HN, Smooker PM, Coloe PJ. The antibiotic resistance characteristics of non-typhoidal Salmonella enterica isolated from food-producing animals, retail meat and humans in South East Asia. Int J Food Microbiol. 2012;154(3):98-106.
  37. Boonyasiri A, Tangkoskul T, Seenama C, Saiyarin J, Tiengrim S, Thamlikitkul V. Prevalence of antibiotic resistant bacteria in healthy adults, foods, food animals, and the environment in selected areas in Thailand. Pathog Glob Health. 2014;108(5):235-245.
  38. Lay KK, Koowattananukul C, Chansong N, Chuanchuen R. Antimicrobial resistance, virulence, and phylogenetic characteristics of Escherichia coli isolates from clinically healthy swine. Foodborne Pathog Dis. 2012;9(11):992-1001.
  39. Tong P, Sun Y, Ji X, Du X, Guo X, Liu J, et al. Characterization of antimicrobial resistance and extended-spectrum β-lactamase genes in Escherichia coli isolated from chickens. Foodborne Pathog Dis. 2015;12(4):345-352.
  40. Tansawai U, Walsh TR, Niumsup PR. Extended spectrum β-lactamase-producing Escherichia coli among backyard poultry farms, farmers, and environments in Thailand. Poult Sci. 2019;98(6):2622-2631.
  41. Ma J, Liu JH, Lv L, Zong Z, Sun Y, Zheng H, et al. Characterization of extended-spectrum β-lactamase genes found among Escherichia coli isolates from duck and environmental samples obtained on a duck farm. Appl Environ Microbiol. 2012;78(10):3668-3673.
  42. Jeamsripong S, Kuldee M, Thaotumpitak V, Chuanchuen R. Antimicrobial resistance, Extended-Spectrum β-Lactamase production and virulence genes in Salmonella enterica and Escherichia coli isolates from estuarine environment. PLoS One. 2023;18(4):e0283359.
  43. Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis. 2016;16(2):161-168.
  44. Xavier BB, Lammens C, Ruhal R, Kumar-Singh S, Butaye P, Goossens H, et al. Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016. Euro Surveill. 2016;21(27):30280.
  45. Song HJ, Kim SJ, Moon DC, Mechesso AF, Choi JH, Kang HY, et al. Antimicrobial resistance in Escherichia coli isolates from healthy food animals in South Korea, 2010-2020. Microorganisms. 2022;10(3):524.
  46. Bischoff KM, White DG, Hume ME, Poole TL, Nisbet DJ. The chloramphenicol resistance gene cmlA is disseminated on transferable plasmids that confer multiple-drug resistance in swine Escherichia coli. FEMS Microbiol Lett. 2005;243(1):285-291.
  47. Batchelor M, Hopkins K, Threlfall EJ, Clifton-Hadley FA, Stallwood AD, Davies RH, et al. blaCTX-M genes in clinical Salmonella isolates recovered from humans in England and Wales from 1992 to 2003. Antimicrob Agents Chemother. 2005;49(4):1319-1322.