Acta Vet. Brno 2025, 94: 203-214

https://doi.org/10.2754/avb202594030203

Characterisation of ESBL-producing E. coli isolated from healthy broilers in Tunisia

Fatma Nsibi1, Ghassan Tayh1, Kenza Chemli1, Aymen Mamlouk1, Omar Abbes2, Ismail Fliss3, Lilia Messadi1

1University of Manouba, National School of Veterinary Medicine, Department of Microbiology and Immunology, LR16AGR01, Sidi Thabet, Tunisia
2DICK Company, Poulina Group Holding, Ben Arous, Tunisia
3University of Laval, Department of Food Sciences and Nutrition, Québec City, Canada

Received February 16, 2025
Accepted September 11, 2025

References

1. Abbassi MS, Kilani H, Abid I, Sáenz Y, Hynds P, Lengliz S, Ben Chehida N, Boutiba-Ben Boubaker I 2021: Genetic background of antimicrobial resistance in multiantimicrobial-resistant Escherichia coli isolates from feces of healthy broiler chickens in Tunisia. Biomed Res Int 2021: 7 <https://doi.org/10.1155/2021/1269849>
2. Abdallah HM, Reuland EA, Wintermans BB, Al Naiemi N, Koek A, Abdelwahab AM, Ammar AM, Mohamed AA, Vandenbroucke-Grauls CM 2015: Extended-spectrum β-lactamases and/or carbapenemases-producing Enterobacteriaceae isolated from retail chicken meat in Zagazig, Egypt. PLoS One 10: e0136052 <https://doi.org/10.1371/journal.pone.0136052>
3. Abdel-Rahman MA, Hamed EA, Abdelaty MF, Sorour HK, Badr H, Hassan WM, Shalaby AG, Mohamed AA-E, Soliman MA, Roshdy H 2023: Distribution pattern of antibiotic resistance genes in Escherichia coli isolated from colibacillosis cases in broiler farms of Egypt. Vet World 16: 1 <https://doi.org/10.14202/vetworld.2023.1-11>
4. Akenten CW, Ofori LA, Khan NA, Mbwana J, Sarpong N, May J, Thye T, Obiri-Danso K, Paintsil EK, Fosu D 2023: Prevalence, characterization, and antimicrobial resistance of extended-spectrum beta-lactamase-producing Escherichia coli from domestic free-range poultry in Agogo, Ghana. Foodborne Pathog Dis 20: 59-66 <https://doi.org/10.1089/fpd.2022.0060>
5. Ali RI, El-Abdelaziz SA, Kamel MA, Murad SK, Abdallah HM, Salem GA 2024: Phenotypic and genotypic characterization of extended spectrum beta-lactamase producing E. coli harboring carbapenem and colistin-resistant genes from poultry farms in Egypt. Open Vet J 14: 459-469 <https://doi.org/10.5455/OVJ.2024.v14.i1.42>
6. Altalhi AD, Gherbawy YA, Hassan SA 2010: Antibiotic resistance in Escherichia coli isolated from retail raw chicken meat in Taif, Saudi Arabia. Foodborne Pathog Dis 7: 281-285 <https://doi.org/10.1089/fpd.2009.0365>
7. Batchelor M, Hopkins K, Threlfall E, Clifton-Hadley F, Stallwood A, Davies R, Liebana E 2005: bla CTX-M genes in clinical Salmonella isolates recovered from humans in England and Wales from 1992 to 2003. Antimicrob Agents Chemother 49: 1319-1322 <https://doi.org/10.1128/AAC.49.4.1319-1322.2005>
8. Ben Haj Yahia A, Tayh G, Landolsi S, Maamar E, Galai N, Landoulsi Z, Messadi L 2023: First report of OXA-48 and IMP genes among extended-spectrum beta-lactamase-producing Escherichia coli isolates from diarrheic calves in Tunisia. Microb Drug Resist 29: 150-162 <https://doi.org/10.1089/mdr.2022.0129>
9. Ceccarelli D, Hesp A, van der Goot J, Joosten P, Sarrazin S, Wagenaar JA, Dewulf J, Mevius DJ, Effort Consortium OBOT 2020: Antimicrobial resistance prevalence in commensal Escherichia coli from broilers, fattening turkeys, fattening pigs and veal calves in European countries and association with antimicrobial usage at country level. J Med Microbiol 69: 537-547 <https://doi.org/10.1099/jmm.0.001176>
10. D’Andrea MM, Arena F, Pallecchi L, Rossolini GM 2013: CTX-M-type β-lactamases: A successful story of antibiotic resistance. Int J Med Microbiol 303: 305-317 <https://doi.org/10.1016/j.ijmm.2013.02.008>
11. Das BJ, Singha KM, Wangkheimayum J, Chanda DD, Bhattacharjee A 2023: Emergence of carbapenem-resistant enterobacterales co-harboring bla(OXA-78) and bla(OXA-58) from India. Ann Clin Microbiol Antimicrob 22: 79 <https://doi.org/10.1186/s12941-023-00635-6>
12. Dawadi P, Bista S, Bista S 2021: Prevalence of colistin-resistant Escherichia coli from poultry in South Asian developing countries. Vet Med Int 11: 6398838
13. Di Francesco A, Salvatore D, Sakhria S, Catelli E, Lupini C, Abbassi MS, Bessoussa G, Ben Yahia S, Ben Chehida N 2021: High frequency and diversity of tetracycline resistance genes in the microbiota of broiler chickens in Tunisia. Animals 11: 377 <https://doi.org/10.3390/ani11020377>
14. Donado-Godoy P, Byrne BA, Castellanos R, Vanegas C, Coral A, Arevalo A, Clavijo V, Vargas M, Zuńiga JJR, Tafur M 2015: Prevalence, resistance patterns, and risk factors for antimicrobial resistance in bacteria from retail chicken meat in Colombia. J Food Prot 78: 751-759 <https://doi.org/10.4315/0362-028X.JFP-14-349>
15. Economou V, Zisides N, Gousia P, Petsios S, Sakkas H, Soultos N, Papadopoulou C 2015: Prevalence and antimicrobial profile of Campylobacter isolates from free-range and conventional farming chicken meat during a 6-year survey. Food Control 56: 161-168 <https://doi.org/10.1016/j.foodcont.2015.03.022>
16. Elshamy AA, Aboshanab KM 2020: A review on bacterial resistance to carbapenems: epidemiology, detection and treatment options. Future Sci OA 6: Fso438 <https://doi.org/10.2144/fsoa-2019-0098>
17. Ghodousi A, Bonura C, Di Noto AM, Mammina C 2015: Extended-spectrum β-lactamase, AmpC-producing, and fluoroquinolone-resistant Escherichia coli in retail broiler chicken meat, Italy. Foodborne Pathog Dis 12: 619-625 <https://doi.org/10.1089/fpd.2015.1936>
18. Grobbel M, Hammerl JA, Alt K, Irrgang A, Kaesbohrer A, Tenhagen B-A 2022: Comparison of antimicrobial resistances in Escherichia coli from conventionally and organic farmed poultry from Germany. Antibiotics (Basel) 11: 1282 <https://doi.org/10.3390/antibiotics11101282>
19. Hassen B, Abbassi MS, Ruiz-Ripa L, Mama OM, Ibrahim C, Benlabidi S, Hassen A, Torres C, Hammami S 2021: Genetic characterization of extended-spectrum β-lactamase-producing Enterobacteriaceae from a biological industrial wastewater treatment plant in Tunisia with detection of the colistin-resistance mcr-1 gene. FEMS Microbiol Ecol 97: fiaa231
20. Hatrongjit R, Kerdsin A, Akeda Y, Hamada S 2018: Detection of plasmid-mediated colistin-resistant and carbapenem-resistant genes by multiplex PCR. MethodsX 5: 532-536 <https://doi.org/10.1016/j.mex.2018.05.016>
21. Hussain A, Shaik S, Ranjan A, Nandanwar N, Tiwari SK, Majid M, Baddam R, Qureshi IA, Semmler T, Wieler LH 2017: Risk of transmission of antimicrobial resistant Escherichia coli from commercial broiler and free-range retail chicken in India. Front Microbiol 8: 2120 <https://doi.org/10.3389/fmicb.2017.02120>
22. Jacoby GA, Han P 1996: Detection of extended-spectrum beta-lactamases in clinical isolates of Klebsiella pneumoniae and Escherichia coli. J Clin Microbiol 34: 908-911 <https://doi.org/10.1128/jcm.34.4.908-911.1996>
23. Jansen W, van Hout J, Wiegel J, Iatridou D, Chantziaras I, De Briyne N 2022: Colistin use in European livestock: Veterinary field data on trends and perspectives for further reduction. Vet Sci 9: 650
24. Jerab J, Jansen W, Blackwell J, van Hout J, Palzer A, Lister S, Chantziaras I, Dewulf J, De Briyne N 2022: Real-world data on antibiotic group treatment in European livestock: Drivers, conditions, and alternatives. Antibiotics (Basel) 11: 1046 <https://doi.org/10.3390/antibiotics11081046>
25. Jouini A, Vinué L, Slama KB, Saenz Y, Klibi N, Hammami S, Boudabous A, Torres C 2007: Characterization of CTX-M and SHV extended-spectrum β-lactamases and associated resistance genes in Escherichia coli strains of food samples in Tunisia. J Antimicrob Chemother 60: 1137-1141 <https://doi.org/10.1093/jac/dkm316>
26. Jouy E, Haenni M, Le Devendec L, Le Roux A, Châtre P, Madec JY, Kempf I 2017: Improvement in routine detection of colistin resistance in E. coli isolated in veterinary diagnostic laboratories. J Microbiol Methods 132: 125-127 <https://doi.org/10.1016/j.mimet.2016.11.017>
27. Khong M, Snyder A, Magnaterra A, Young M, Barbieri N, Weimer S 2023: Antimicrobial resistance profile of Escherichia coli isolated from poultry litter. Poult Sci 102: 102305 <https://doi.org/10.1016/j.psj.2022.102305>
28. Koga VL, Rodrigues GR, Scandorieiro S, Vespero EC, Oba A, de Brito BG, de Brito KC, Nakazato G, Kobayashi RK 2015: Evaluation of the antibiotic resistance and virulence of Escherichia coli strains isolated from chicken carcasses in 2007 and 2013 from Paraná, Brazil. Foodborne Pathog Dis 12: 479-485 <https://doi.org/10.1089/fpd.2014.1888>
29. Koju P, Shrestha R, Shrestha A, Tamrakar S, Rai A, Shrestha P, Madhup SK, Katuwal N, Shrestha A, Shrestha A, Shrestha S, K CS, Karki P, Tamang P, Thekkur P, Shakya Shrestha S 2022: Antimicrobial resistance in E. coli isolated from chicken cecum samples and factors contributing to antimicrobial resistance in Nepal. Trop Med Infect Dis 7: 249 <https://doi.org/10.3390/tropicalmed7090249>
30. Lengliz S, Benlabidi S, Raddaoui A, Cheriet S, Ben Chehida N, Najar T, Abbassi M 2021: High occurrence of carbapenem‐resistant Escherichia coli isolates from healthy rabbits (Oryctolagus cuniculus): first report of blaIMI and blaVIM type genes from livestock in Tunisia. Lett Appl Microbiol 73: 708-717 <https://doi.org/10.1111/lam.13558>
31. Liu Z, Wang K, Zhang Y, Xia L, Zhao L, Guo C, Liu X, Qin L, Hao Z 2022: High prevalence and diversity characteristics of blaNDM, mcr, and blaESBLs harboring multidrug-resistant Escherichia coli from chicken, pig, and cattle in China. Front Cell Infect Microbiol 11: 755545 <https://doi.org/10.3389/fcimb.2021.755545>
32. Loqman S, Soraa N, Diene SM, Rolain J-M 2021: Dissemination of carbapenemases (OXA-48, NDM and VIM) producing Enterobacteriaceae isolated from the Mohamed VI University Hospital in Marrakech, Morocco. Antibiotics 10: 492 <https://doi.org/10.3390/antibiotics10050492>
33. Messaili C, Messai Y, Bakour R 2019: Virulence gene profiles, antimicrobial resistance and phylogenetic groups of fecal Escherichia coli strains isolated from broiler chickens in Algeria. Vet Ital 55: 35-46
34. Mezhoud H, Boyen F, Touazi L-H, Garmyn A, Moula N, Smet A, Haesbrouck F, Martel A, Iguer-Ouada M, Touati A 2015: Extended spectrum β-lactamase producing Escherichia coli in broiler breeding roosters: Presence in the reproductive tract and effect on sperm motility. Anim Reprod Sci 159: 205-211 <https://doi.org/10.1016/j.anireprosci.2015.06.021>
35. Mgaya FX, Matee MI, Muhairwa AP, Hoza AS 2021: Occurrence of multidrug resistant Escherichia coli in raw meat and cloaca swabs in poultry processed in slaughter slabs in Dar es Salaam, Tanzania. Antibiotics (Basel) 10: 343 <https://doi.org/10.3390/antibiotics10040343>
36. Mnif B, Ktari S, Rhimi F, Hammami A 2012: Extensive dissemination of CTX‐M‐1‐and CMY‐2‐producing Escherichia coli in poultry farms in Tunisia. Lett Appl Microbiol 55: 407-413 <https://doi.org/10.1111/j.1472-765X.2012.03309.x>
37. Mojtahedi A 2017): The presence of extended-spectrum β-lactamase as a risk factor for MDR in clinical isolation of Escherichia coli. Trop Biomed 34: 98-109
38. Mondal AH, Khare K, Saxena P, Debnath P, Mukhopadhyay K, Yadav D 2024: A review on colistin resistance: An antibiotic of last resort. Microorganisms 12: 772 <https://doi.org/10.3390/microorganisms12040772>
39. Murray M, Salvatierra G, Dávila-Barclay A, Ayzanoa B, Castillo-Vilcahuaman C, Huang M, Pajuelo MJ, Lescano AG, Cabrera L, Calderón M, Berg DE, Gilman RH, Tsukayama P 2021: Market chickens as a source of antibiotic-resistant Escherichia coli in a Peri-urban community in Lima, Peru. Front Microbiol 12: 635871 <https://doi.org/10.3389/fmicb.2021.635871>
40. Pavlickova S, Klancnik A, Dolezalova M, Mozina SS, Holko I 2017: Antibiotic resistance, virulence factors and biofilm formation ability in Escherichia coli strains isolated from chicken meat and wildlife in the Czech Republic. J Environ Sci Health B 52: 570-576 <https://doi.org/10.1080/03601234.2017.1318637>
41. Perestrelo S, Amaro A, Brouwer MSM, Clemente L, Ribeiro Duarte AS, Kaesbohrer A, Karpíšková R, Lopez-Chavarrias V, Morris D, Prendergast D, Pista A, Silveira L, Skarżyńska M, Slowey R, Veldman KT, Zając M, Burgess C, Alvarez J 2023: Building an International one health strain level database to characterise the epidemiology of AMR threats: ESBL-AmpC producing E. coli as an example-challenges and perspectives. Antibiotics (Basel) 12: 552 <https://doi.org/10.3390/antibiotics12030552>
42. Persoons D, Haesebrouck F, Smet A, Herman L, Heyndrickx M, Martel A, Catry B, Berge AC, Butaye P, Dewulf J 2011: Risk factors for ceftiofur resistance in Escherichia coli from Belgian broilers. Epidemiol Infect 139: 765-771 <https://doi.org/10.1017/S0950268810001524>
43. Pourhossein Z, Asadpour L, Habibollahi H, Shafighi ST 2020: Antimicrobial resistance in fecal Escherichia coli isolated from poultry chicks in northern Iran. Gene Rep 21: 100926 <https://doi.org/10.1016/j.genrep.2020.100926>
44. Rawat N, Anjali, Jamwal R, Devi PP, Yadav K, Kumar N, Rajagopal R 2022: Detection of unprecedented level of antibiotic resistance and identification of antibiotic resistance factors, including QRDR mutations in Escherichia coli isolated from commercial chickens from North India. J Appl Microbiol 132: 268-278 <https://doi.org/10.1111/jam.15209>
45. Saidani M, Messadi L, Chaouechi A, Tabib I, Saras E, Soudani A, Daaloul-Jedidi M, Mamlouk A, Ben Chehida F, Chakroun C, Madec J-Y, Haenni M 2019: High genetic diversity of Enterobacteriaceae clones and plasmids disseminating resistance to extended-spectrum cephalosporins and colistin in healthy chicken in Tunisia. Microb Drug Resist 25: 1507-1513 <https://doi.org/10.1089/mdr.2019.0138>
46. Selmi R, Tayh G, Srairi S, Mamlouk A, Chehida FB, Lahmar S, Bouslama M, Daaloul-Jedidi M, Messadi L 2022: Prevalence, risk factors and emergence of extended-spectrum β-lactamase producing-, carbapenem-and colistin-resistant Enterobacterales isolated from wild boar (Sus scrofa) in Tunisia. Microb Pathog 163: 105385 <https://doi.org/10.1016/j.micpath.2021.105385>
47. Seo KW, Kim YB, Jeon HY, Lim S-K, Lee YJ 2018: Comparative genetic characterization of third-generation cephalosporin-resistant Escherichia coli from chicken meat produced by integrated broiler operations in South Korea. Poult Sci 97: 2871-2879 <https://doi.org/10.3382/ps/pey127>
48. Sharifi-Yazdi M, Azimi C 1998: Comparison of the conventional biochemical tests recommended for the identification of Escherichia coli in water, in report 71, with the API 20E system. Iran J Public Health 27: 61-66
49. Smith HZ, Hollingshead CM, Kendall B 2024: Carbapenem-resistant Enterobacterales. StatPearls. StatPearls Publishing. Available at: https://www.ncbi.nlm.nih.gov/books/NBK551704/
50. Soufi L, Abbassi MS, Sáenz Y, Vinué L, Somalo S, Zarazaga M, Abbas A, Dbaya R, Khanfir L, Ben Hassen A, Hammami S, Torres C 2009: Prevalence and diversity of integrons and associated resistance genes in Escherichia coli isolates from poultry meat in Tunisia. Foodborne Pathog Dis 6: 1067-1073 <https://doi.org/10.1089/fpd.2009.0284>
51. Tang B, Ni J, Lin J, Sun Y, Lin H, Wu Y, Yang H, Yue M 2022: Genomic characterization of multidrug-resistance gene cfr in Escherichia coli recovered from food animals in Eastern China. Front Microbiol 13: 999778 <https://doi.org/10.3389/fmicb.2022.999778>
52. Vinueza-Burgos C, Ortega-Paredes D, Narváez C, De Zutter L, Zurita J 2019: Characterization of cefotaxime resistant Escherichia coli isolated from broiler farms in Ecuador. PLoS One 14: e0207567 <https://doi.org/10.1371/journal.pone.0207567>
53. Zhu F, Zhong X, Hu M, Lu L, Deng Z, Liu T 2014: In vitro reconstitution of mevalonate pathway and targeted engineering of farnesene overproduction in Escherichia coli. Biotechnol Bioeng 111: 1396-1405 <https://doi.org/10.1002/bit.25198>
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