Volume 13, Issue 1 (March 2026)                   J. Food Qual. Hazards Control 2026, 13(1): 40-46 | Back to browse issues page

Ethics code: Not applicable.


XML Print


Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:

Bagheri M, Ghanbarpour R, Amirpoorsaid Z, Mohseni P, Hesam-Arefi M, Jajarmi M. Turkey (Meleagris gallopavo f. domestica) Meat as a Potential Reservoir for Dissemination of Antimicrobial Resistant and Shigatoxigenic Escherichia coli Strains. J. Food Qual. Hazards Control 2026; 13 (1) :40-46
URL: http://jfqhc.ssu.ac.ir/article-1-1247-en.html
Department of Food Science and Technology, Bardsir Faculty of Agriculture, Shahid Bahonar University of Kerman, Kerman, Iran , ma.bagheri@uk.ac.ir
Abstract:   (63 Views)
Background: Enteropathogenic and Shiga toxin-producing Escherichia coli (E. coli) are the two main pathotypes capable of causing serious human infections, especially when resistant to antibiotics.
Methods: In this work, 95 turkey carcasses were swabbed in slaughterhouse over four months (June–September 2023). Antibiotic resistance was evaluated by a disk diffusion method named Kirby–Bauer against nine antimicrobial agents. Three virulence genes including stx1, stx2, eae, three resistance genes including blaTEM, blaSHV, blaCTX-M, and four phylogenetic markers (arpA, chuA, yjaA, TspE4.C2) were screened by Polymerase Chain Reaction (PCR) method. Data were analyzed using Microsoft Excel and SPSS (version 24), with the chi-square test at a significance level of p≤0.05.
Results: Out of 95 carcasses, 72 (75.78%) were E. coli-positive. Among the E. coli isolates, 63.89% were resistant to chloramphenicol, 59.72% to nalidixic acid, and 56.94% to florfenicol. One isolate, classified as extended-spectrum beta-lactamase positive, belonged to phylogroup D and showed simultaneous resistance to four antibiotics without harboring the resistance genes studied. Overall, 52.7% of the E. coli isolates were recognized as Multi-Drug Resistant (MDR). Profiles of resistance genes included blaTEM (23.61%), blaTEM/blaSHV (2.77%), and blaCTX-M (1.38%). Virulence genes were detected in six isolates: stx1 (4.17%), stx2 (1.39%), and eae (2.77%). Phylogenetic analysis revealed five groups: A (19.44%), B1 (36.11%), C (5.55%), D (13.8%), and E (15.27%), while 9.72% remained unclassified.
Conclusion: The occurrence of E. coli isolates harboring virulence and antibiotic-resistance genes in turkey carcasses underscores serious public health risks.
The significant frequency of Multi-Drug Resistant (MDR) E. coli isolates highlights the need for improved monitoring and control measures throughout the food chain.

DOI: 10.18502/jfqhc.13.1.21379
Full-Text [PDF 995 kb]   (18 Downloads)    
Type of Study: Original article | Subject: Special
Received: 24/07/17 | Accepted: 25/09/15 | Published: 26/03/20

References
1. AbdelRahman, M.A.A., Roshdy, H., Samir, A.H. and Hamed, E.A. (2020) 'Antibiotic resistance and extended-spectrum β-lactamase in Escherichia coli isolates from imported 1-day-old chicks, ducklings, and turkey poults', Veterinary World, 13(6), pp. 1037-1044. Available at: [DOI:10.14202/vetworld.2020.1037-1044]
2. Asadi, A., Salehi, T.Z., Jamshidian, M. and Ghanbarpour, R. (2018) 'ECOR phylotyping and determination of virulence genes in Escherichia coli isolates from pathological conditions of broiler chickens in poultry slaughter-houses of southeast of Iran', Veterinary Research Forum, 9(3), pp. 211-216. Available at: [DOI:10.30466/vrf.2018.30827]
3. Baran, A., Adıgüzel, M. and Yüksel, M. (2020) 'Prevalence of antibiotic-resistant and extended-spectrum beta-lactamase-producing Escherichia coli in chicken meat from eastern Turkey', Pakistan Veterinary Journal, 40(3), pp. 355-359. Available at: [DOI:10.29261/pakvetj/2020.047]
4. Beghain, J., Bridier-Nahmias, A., Le Nagard, H., Denamur, E. and Clermont, O. (2018) 'ClermonTyping: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping', Microbial Genomics, 4(7), p. e000192. Available at: [DOI:10.1099/mgen.0.000192]
5. Bohaychuk, V.M., Gensler, G.E., King, R.K., Manninen, K.I., Sorensen, O., Wu, J.T., Stiles, M.E. and McMullen, L.M. (2006) 'Occurrence of pathogens in raw and ready-to-eat meat and poultry products collected from the retail marketplace in Edmonton, Alberta, Canada', Journal of Food Protection, 69(9), pp. 2176–2182. Available at: [DOI:10.4315/0362028X-69.9.2176]
6. Bouzari, S., Farhang, E., Hosseini, S.M. and Alikhani, M.Y. (2018) 'Prevalence and antimicrobial resistance of Shiga toxin-producing Escherichia coli and enteropathogenic Escherichia coli isolated from patients with acute diarrhea', Iranian Journal of Microbiology, 10(3), pp. 151–157.
7. Clermont, O., Christenson, J.K., Denamur, E. and 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), pp. 58–65. Available at: [DOI:10.1111/1758-2229.12019]
8. Clinical and Laboratory Standards Institute (CLSI) (2021) Performance Standards for Antimicrobial Susceptibility Testing. 31st edn. CLSI supplement M100. Wayne, Pennsylvania, USA: Clinical and Laboratory Standards Institute.
9. Connolly, G. and Campbell, W.W. (2023) 'Poultry consumption and human cardiometabolic health-related outcomes: A narrative review', Nutrients, 15(16), p. 3550. Available at: [DOI:10.3390/nu15163550]
10. Davis, G.S., Waits, K., Nordstrom, L., Grande, H., Weaver, B., Papp, K., Horwinski, J., Koch, B., Hungate, B.A., Liu, C.M. and Price, L.B. (2018) 'Antibiotic-resistant Escherichia coli from retail poultry meat with different antibiotic use claims', BMC Microbiology, 18, p. 174. Available at: [DOI:10.1186/s12866-018-1322-5]
11. Egea, P., López-Cerero, L., Torres, E., Del Carmen Gómez-Sánchez, M., Serrano, L., Sánchez-Ortiz, M.D.N., Rodriguez-Baño, J. and Pascual, A. (2012) 'Increased raw poultry meat colonization by extended spectrum beta-lactamase-producing Escherichia coli in the south of Spain', International Journal of Food Microbiology, 159(2), pp. 69–73. Available at: [DOI:10.1016/j.ijfoodmicro.2012.08.002]
12. Eibach, D., Dekker, D., Boahen, K.G., Akenten, C.W., Sarpong, N., Campos, C.B., Berneking, L., Aepfelbacher, M., Krumkamp, R., Owusu-Dabo, E. and May, J. (2018) 'Extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in local and imported poultry meat in Ghana', Veterinary Microbiology, 217, pp. 7–12. Available at: [DOI:10.1016/j.vetmic.2018.02.023]
13. Eid, S. and Samir, A.H. (2019) 'Extended-spectrum beta-lactamase and Class 1 integrons in multidrug-resistant Escherichia coli isolated from turkeys', Veterinary World, 12(7), pp. 1167–1174. Available at: [DOI:10.14202/vetworld.2019.1167-1174]
14. Endale, H., Mathewos, M. and Abdeta, D. (2023) 'Potential causes of spread of antimicrobial resistance and preventive measures in one health perspective-a review', Infection and Drug Resistance, 16, pp. 7515–7545. Available at: [DOI:10.2147/IDR.S428837]
15. Foster-Nyarko, E. and Pallen, M.J. (2022) 'The microbial ecology of Escherichia coli in the vertebrate gut', FEMS Microbiology Reviews, 46(3), p. fuac008. Available at: [DOI:10.1093/femsre/fuac008]
16. Freedman, S.B., Van De Kar, N.C.A.J. and Tarr, P.I. (2023) 'Shiga toxin–producing Escherichia coli and the hemolytic–uremic syndrome', New England Journal of Medicine, 389(15), pp. 1402-1414. Available at: [DOI:10. 1056/NEJMra2108739]
17. Gholami-Ahangaran, M., Moravvej, A.H., Safizadeh, Z., Sadeghi Nogoorani, V., Zokaei, M. and Ghasemian, S.O. (2021) 'The evaluation of ESBL genes and antibiotic resistance rate in Escherichia coli strains isolated from meat and intestinal contents of turkey in Isfahan, Iran', Iranian Journal of Veterinary Research, 22(4), pp. 318–325. Available at: [DOI:10.22099/ijvr.2021.39493.5737]
18. Hessain, A.M., Al-Arfaj, A.A., Zakri, A.M., El-Jakee, J.K., Al-Zogibi, O.G., Hemeg, H.A. and Ibrahim, I.M. (2015) 'Molecular characterization of Escherichia coli O157: H7 recovered from meat and meat products relevant to human health in Riyadh, Saudi Arabia', Saudi Journal of Biological Sciences, 22(6), pp. 725–729. Available at: [DOI:10.1016/j.sjbs.2015.06.009]
19. Hoepers, P.G., Silva, P.L., Rossi, D.A., Valadares Júnior, E.C., Ferreira, B.C., Zuffo, J.P., Koerich, P.K. and Fonseca, B.B. (2018) 'The association between extended spectrum beta-lactamase (ESBL) and ampicillin C (AmpC) beta-lactamase genes with multidrug resistance in Escherichia coli isolates recovered from turkeys in Brazil', British Poultry Science, 59(4), pp. 396–401. Available at: [DOI:10.1080/00071668.2018.1468070]
20. Kaesbohrer, A., Schroeter, A., Tenhagen, B.-A., Alt, K., Guerra, B. and Appel, B. (2012) 'Emerging antimicrobial resistance in commensal Escherichia coli with public health relevance', Zoonoses and Public Health, 59, pp. 158–165. Available at: [DOI:10.1111/j.1863-2378.2011.01451.x]
21. Khaitsa, M.L., Oloya, J., Doetkott, D. and Kegode, R. (2008) 'Antimicrobial resistance and association with class 1 integrons in Escherichia coli isolated from turkey meat products', Journal of Food Protection, 71(8), pp. 1679–1684. Available at: [DOI:10.4315/0362-028X-71.8.1679]
22. Mare, A.D., Ciurea, C.N., Man, A., Tudor, B., Moldovan, V., Decean, L. and Toma, F. (2021) 'Enteropathogenic Escherichia coli—a Summary of the literature', Gastroenterology Insights, 12(1), pp. 28–40. Available at: [DOI:10.3390/gastroent12010004]
23. Markey, B., Leonard, F., Archambault, M., Cullinane, A. and Maguire, D. (2013) Clinical Veterinary Microbiology. 2nd edn. London, UK: Elsevier Health Sciences.
24. Martinez, J.L. (2009) 'The role of natural environments in the evolution of resistance traits in pathogenic bacteria', Proceedings of the Royal Society B: Biological Sciences, 276(1667), pp. 2521-2530. Available at: [DOI:10.1098/rspb.2009.0320]
25. Mayrhofer, S., Paulsen, P., Smulders, F.J.M. and Hilbert, F. (2004) 'Antimicrobial resistance profile of five major food-borne pathogens isolated from beef, pork and poultry', International Journal of Food Microbiology, 97(1), pp. 23–29. Available at: [DOI:10.1016/j.ijfoodmicro.2004.04.006]
26. Moawad, A.A., Hotzel, H., Neubauer, H., Ehricht, R., Monecke, S., Tomaso, H., Hafez, H.M., Roesler, U. and El-Adawy, H. (2018) 'Antimicrobial resistance in Enterobacteriaceae from healthy broilers in Egypt: emergence of colistin-resistant and extended-spectrum β-lactamase-producing Escherichia coli', Gut Pathogens, 10, p. 39. Available at: [DOI:10.1186/s13099-018-0266-5]
27. Mousavi, R., Rahimi, E. and Shakerian, A. (2020) 'Incidence and profiles of antibiotic resistance and virulence markers of the Escherichia coli O157 bacteria recovered from poultry meat', Egyptian Journal of Veterinary Sciences, 51(2), pp. 215–223. Available at: [DOI:10.21608/ejvs.2020.20516.1141]
28. Nwankwo, I.O., Ezenduka, E.V., Nwanta, J.A., Ogugua, A.J. and Audu, B.J. (2021) 'Prevalence of Campylobacter spp. and antibiotics resistant E. coli on poultry carcasses and handlers’ hands at Ikpa slaughter, Nsukka, Nigeria', Notulae Scientia Biologicae, 13(2), p. 10866. Available at: [DOI:10.15835/nsb13210866]
29. Pakbin, B., Brück, W.M. and Rossen, J.W.A. (2021) 'Virulence factors of enteric pathogenic Escherichia coli: a review', International Journal of Molecular Sciences, 22(18), p. 9922. Available at: [DOI:10.3390/ijms22189922]
30. Paton, A.W. and Paton, J.C. (2002) 'Direct detection and characterization of Shiga toxigenic Escherichia coli by multiplex PCR for stx1, stx2, eae, ehxA, and saa', Journal of Clinical Microbiology, 40(1), pp. 271–274. Available at: [DOI:10.1128/jcm.40.1.271-274.2002]
31. Roschanski, N., Fischer, J., Guerra, B. and Roesler, U. (2014) 'Development of a multiplex real-time PCR for the rapid detection of the predominant beta-lactamase genes CTX-M, SHV, TEM and CIT-type AmpCs in Enterobacteriaceae', PLoS One, 9(7), p. e100956. Available at: [DOI:10.1371/journal.pone.0100956]
32. Sebastian, S., Tom, A.A., Babu, J.A. and Joshy, M. (2021) 'Antibiotic resistance in Escherichia coli isolates from poultry environment and UTI patients in Kerala, India: a comparison study', Comparative Immunology, Microbiology and Infectious Diseases, 75, p. 101614. Available at: [DOI:10.1016/j.cimid.2021.101614]
33. Sheikh, A.A., Checkley, S., Avery, B., Chalmers, G., Bohaychuk, V., Boerlin, P., Reid-Smith, R. and Aslam, M. (2012) 'Antimicrobial resistance and resistance genes in Escherichia coli isolated from retail meat purchased in Alberta, Canada', Foodborne Pathogens and Disease, 9(7), pp. 625–631. Available at: [DOI:10.1089/fpd.2011.1078]
34. Shrestha, R.D., Agunos, A., Gow, S.P., Deckert, A.E. and Varga, C. (2022) 'Associations between antimicrobial resistance in fecal Escherichia coli isolates and antimicrobial use in Canadian turkey flocks', Frontiers in Microbiology, 13, p. 954123. Available at: [DOI:10.3389/fmicb.2022.954123]
35. Silva, H.O., Vidal, A.M.C. and Junior, O.D.R. (2017) 'Pathogenic bacteria in turkey meat: A review', Revista Brasileira de Higiene e Sanidade Animal, 11(3), pp. 338–353.
36. Sokolović, M., Šimpraga, B., Amšel-Zelenika, T., Berendika, M. and Krstulović, F. (2022) 'Prevalence and characterization of Shiga toxin producing Escherichia coli isolated from animal feed in Croatia', Microorganisms, 10(9), p. 1839. Available at: [DOI:10.3390/microorganisms10091839]
37. Stoppe, N.D.C., Silva, J.S., Carlos, C., Sato, M.I.Z., Saraiva, A.M., Ottoboni, L.M.M. and Torres, T.T. (2017) 'Worldwide phylogenetic group patterns of Escherichia coli from commensal human and wastewater treatment plant isolates', Frontiers in Microbiology, 8, p. 2512. Available at: [DOI:10.3389/fmicb.2017.02512]
38. Tenaillon, O., Skurnik, D., Picard, B. and Denamur, E. (2010) 'The population genetics of commensal Escherichia coli', Nature Reviews Microbiology, 8, pp. 207–217. Available at: [DOI:10.1038/nrmicro2298]
39. Van Boeckel, T.P., Pires, J., Silvester, R., Zhao, C., Song, J., Criscuolo, N.G., Gilbert, M., Bonhoeffer, S. and Laxminarayan, R. (2019) 'Global trends in antimicrobial resistance in animals in low-and middle-income countries', Science, 365(6459), p. eaaw1944. Available at: [DOI:10.1126/science.aaw1944]
40. Vázquez-Villanueva, J., Vázquez, K., Martínez-Vázquez, A.V., Wong-González, A., Hernández-Escareño, J., Cabrero-Martínez, O., Cruz-Pulido, W.L., Guerrero, A., Rivera, G. and Bocanegra-García, V. (2023) 'Molecular and antimicrobial susceptibility characterization of Escherichia coli isolates from bovine slaughterhouse process', Antibiotics, 12(2), p. 291. Available at: [DOI:10.3390/antibiotics12020291]
41. Wang, M., Jiang, M., Wang, Z., Chen, R., Zhuge, X. and Dai, J. (2021) 'Characterization of antimicrobial resistance in chicken-source phylogroup F Escherichia coli: similar populations and resistance spectrums between E. coli recovered from chicken colibacillosis tissues and retail raw meats in Eastern China', Poultry Science, 100(9), p. 101370. Available at: [DOI:10.1016/j.psj.2021.101370]
42. Wasyl, D., Hoszowski, A., Zając, M. and Szulowski, K. (2013) 'Antimicrobial resistance in commensal Escherichia coli isolated from animals at slaughter', Frontiers in Microbiology, 4, p. 221. Available at: [DOI:10.3389/fmicb.2013.00221]
43. Xie, H., Ogura, Y. and Suzuki, Y. (2022) 'Persistence of antibiotic-resistant Escherichia coli strains belonging to the B2 phylogroup in municipal wastewater under aerobic conditions', Antibiotics, 11(2), p. 202. Available at: [DOI:10.3390/antibiotics11020202]
44. Younis, G., Awad, A. and Mohamed, N. (2017) 'Phenotypic and genotypic characterization of antimicrobial susceptibility of avian pathogenic Escherichia coli isolated from broiler chickens', Veterinary World, 10(10), pp. 1167–1172. Available at: [DOI:10.14202/vetworld.2017.1167-1172]
45. Zarei, O., Shokoohizadeh, L., Hossainpour, H. and Alikhani, M.Y. (2021) 'The prevalence of Shiga toxin-producing Escherichia coli and enteropathogenic Escherichia coli isolated from raw chicken meat samples', International Journal of Microbiology, 2021, p. 3333240. Available at: [DOI:10.1155/2021/3333240]

Add your comments about this article : Your username or Email:
CAPTCHA

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

© 2026 CC BY-NC 4.0 | Journal of food quality and hazards control

Designed & Developed by : Yektaweb