Volume 8, Issue 2 (June 2021)
J. Food Qual. Hazards Control 2021, 8(2): 78-86 |
Back to browse issues page
Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
Amir M, Riaz M, Chang Y, Ismail A, Hameed A, Ahsin M. Antibiotic Resistance in Diarrheagenic Escherichia coli Isolated from Broiler Chickens in Pakistan. J. Food Qual. Hazards Control 2021; 8 (2) :78-86
URL: http://jfqhc.ssu.ac.ir/article-1-804-en.html
URL: http://jfqhc.ssu.ac.ir/article-1-804-en.html
Institute of Food Science and Nutrition, Bahauddin Zakariya University, Multan 60800, Pakistan , riaz@bzu.edu.pk
Abstract: (1073 Views)
Background: Diarrheagenic Escherichia coli (DEC) strains are predominant cause of gastrointestinal tract illnesses. The main objective of the study was to determine antibiotic resistance in various types of DEC isolated from chicken broilers farmed in Pakistan.
Methods: A total of 200 feces and 200 meat samples from broiler chickens were collected from the slaughtering shops in Southern Punjab, Pakistan. The confirmed fecal (n=150) and meat (n=150) E. coli isolates were investigated against 16 antibiotics. Fourteen virulence genes specific for Enteropathogenic (EPEC), Shiga Toxin-producing (STEC), Enteroinvasive (EIEC), Enteroaggregative (EAEC), and Enterotoxigenic (ETEC) E. coli were identified using Polymerase Chain Reaction.
Results: EPEC was the most detected pathotype in both feces (76%) and meat (90%) samples, followed by STEC, EIEC, and ETEC. The highest resistance (40-90%) was observed against penicillin, oxytetracycline, and nalidixic acid in fecal isolates. More than 50% EPEC and EAEC fecal isolates, and 60% EAEC meat isolates were simultaneously resistant to 6 or more antibiotics.
Conclusion: Conclusively, the broiler meat sold in open markets of Pakistan was considerably contaminated with multi-drug resistant DEC. To mitigate the issue, the government should regulate the use of antibiotics at poultry farms and monitor slaughtering practices in slaughterer houses.
DOI: 10.18502/jfqhc.8.2.6472
Methods: A total of 200 feces and 200 meat samples from broiler chickens were collected from the slaughtering shops in Southern Punjab, Pakistan. The confirmed fecal (n=150) and meat (n=150) E. coli isolates were investigated against 16 antibiotics. Fourteen virulence genes specific for Enteropathogenic (EPEC), Shiga Toxin-producing (STEC), Enteroinvasive (EIEC), Enteroaggregative (EAEC), and Enterotoxigenic (ETEC) E. coli were identified using Polymerase Chain Reaction.
Results: EPEC was the most detected pathotype in both feces (76%) and meat (90%) samples, followed by STEC, EIEC, and ETEC. The highest resistance (40-90%) was observed against penicillin, oxytetracycline, and nalidixic acid in fecal isolates. More than 50% EPEC and EAEC fecal isolates, and 60% EAEC meat isolates were simultaneously resistant to 6 or more antibiotics.
Conclusion: Conclusively, the broiler meat sold in open markets of Pakistan was considerably contaminated with multi-drug resistant DEC. To mitigate the issue, the government should regulate the use of antibiotics at poultry farms and monitor slaughtering practices in slaughterer houses.
DOI: 10.18502/jfqhc.8.2.6472
Type of Study: Original article |
Subject:
Special
Received: 20/08/17 | Accepted: 21/02/01 | Published: 21/06/17
Received: 20/08/17 | Accepted: 21/02/01 | Published: 21/06/17
References
1. Ahmed B., Shakoori F.R., Ali S.S., Shakoori A.R. (2009). Antimicrobial resistance pattern and plasmid analysis of Escherichia coli from patients suffering from acute diarrhoea in Azad Kashmir, Pakistan. Pakistan Journal of Zoology. 41: 371-380.
2. Alonso M.Z., Lucchesi P.M.A., Rodríguez E.M., Parma A.E., Padola N.L. (2012). Enteropathogenic (EPEC) and Shigatoxigenic Escherichia coli (STEC) in broiler chickens and derived products at different retail stores. Food Control. 23: 351-355. [DOI: 10.1016/j.foodcont.2011.07.030] [DOI:10.1016/j.foodcont.2011.07.030]
3. Amir M., Riaz M., Chang Y.-F., Akhtar S., Yoo S.H., Sheikh A.S., Kashif M. (2017). Impact of unhygienic conditions during slaughtering and processing on spread of antibiotic resistant Escherichia coli from poultry. Microbiology Research. 8: 7330. [DOI: 10.4081/mr.2017.7330] [DOI:10.4081/mr.2017.7330]
4. Bielaszewska M., Köck R., Friedrich A.W., Von Eiff C., Zimmerhacki L.B., Karch H., Mellmann A. (2007). Shiga toxin-mediated hemolytic uremic syndrome: time to change the diagnostic paradigm?. PLoS One 2: e1024. [DOI: 10.1371/journal.pone.0001024] [DOI:10.1371/journal.pone.0001024] [PMID] [PMCID]
5. Bokhari H., Shah M.A., Asad S., Akhtar S., Akram M., Wren B.W. (2013). Escherichia coli pathotypes in Pakistan from consecutive floods in 2010 and 2011. The American Journal of Tropical Medicine and Hygiene. 88: 519-525. [DOI: 10.4269/ ajtmh.12-0365] [DOI:10.4269/ajtmh.12-0365]
6. Braykov N.P., Eisenberg J.N.S., Grossman M., Zhang L., Vasco K., Cevallos W., Muñoz D., Acevedo A., Moser K.A., Marrs C.F., Foxman B., Trostle J., et al. (2016). Antibiotic resistance in animal and environmental samples associated with small-scale poultry farming in Northwestern Ecuador. Applied and Environmental Science. 1: e00021-15. [DOI: 10.1128/ mSphere.00021-15.] [DOI:10.1128/mSphere.00021-15] [PMID] [PMCID]
7. Byarugaba D.K. (2004). Antimicrobial resistance in developing countries and responsible risk factors. International Journal of Antimicrobial Agents. 24: 105-110. [DOI: 10.1016/j. ijantimicag.2004.02.015] [DOI:10.1016/j.ijantimicag.2004.02.015] [PMID]
8. Byomi A., Zidan S., Diab M., Reddy G., Adesiyun A., Abdela W. (2017). Characterization of diarrheagenic Escherichia coli serotypes isolated from poultry and humans. SOJ Veterinary Sciences. 3: 1-8. [DOI:10.15226/2381-2907/3/1/00122]
9. Canizalez-Roman A., Gonzalez-Nuñez E., Vidal J.E., Flores-Villaseñor H., León-Sicairos N. (2013). Prevalence and antibiotic resistance profiles of diarrheagenic Escherichia coli strains isolated from food items in northwestern Mexico. International Journal of Food Microbiology. 164: 36-45. [DOI: 10.1016/j.ijfoodmicro.2013.03.020] [DOI:10.1016/j.ijfoodmicro.2013.03.020] [PMID]
10. Chaslus-Dancla E., Gerbaud G., Lagorce M., Lafont J.P., Courvalin P. (1987). Persistence of an antibiotic resistance plasmid in intestinal Escherichia coli of chickens in the absence of selective pressure. Antimicrobial Agents and Chemotherapy. 31: 784-788. [DOI: 10.1128/AAC.31.5.784] [DOI:10.1128/AAC.31.5.784] [PMID] [PMCID]
11. Chellapandi K., Dutta T.K., Sharma I., De Mandal S., Kumar N.S., Ralte L. (2017). Prevalence of multi drug resistant enteropathogenic and enteroinvasive Escherichia coli isolated from children with and without diarrhea in Northeast Indian population. Annals of Clinical Microbiology and Antimicrobials. 16: 49. [DOI: 10.1186/s12941-017-0225-x] [DOI:10.1186/s12941-017-0225-x] [PMID] [PMCID]
12. Chokoshvili O., Lomashvili K., Malakmadze N., Geleishvil M., Brant J., Imnadze P., Chitadze N., Tevzadze L., Chanturia G., Tevdoradze T., Tsertsvadze T., Talkington D., et al. (2014). Investigation of an outbreak of bloody diarrhea complicated with hemolytic uremic syndrome. Journal of Epidemiology and Global Health. 4: 249-259. [DOI: 10.1016/j.jegh.2014.03. 004] [DOI:10.1016/j.jegh.2014.03.004] [PMID] [PMCID]
13. Chopra I., Roberts M. (2001). Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiology and Molecular Biology Reviews. 65: 232-260. [DOI: 10.1128/MMBR.65.2.232-260. 2001] [DOI:10.1128/MMBR.65.2.232-260.2001] [PMID] [PMCID]
14. Clinical and Laboratory Standards Institute (CLSI). (2014). M100-S24 performance standards for antimicrobial susceptibility testing; twenty-fourth informational supplement.
15. Currie A., Macdonald J., Ellis A., Siushansian J., Chui L., Charlebois M., Peermohamed M., Everett D., Fehr M., NG L.K. (2007). Outbreak of Escherichia coli O157:H7 infections associated with consumption of beef donair. Journal of Food Protection. 70: 1483-1488. [DOI: 10.4315/0362-028X-70.6.1483] [DOI:10.4315/0362-028X-70.6.1483] [PMID]
16. Da Costa P.M., Oliveira M., Bica A., Vaz-Pires P., Bernardo F. (2007). Antimicrobial resistance in Enterococcus spp. and Escherichia coli isolated from poultry feed and feed ingredients. Veterinary Microbiology. 120: 122-131. [DOI: 10.1016/j.vetmic.2006.10.005] [DOI:10.1016/j.vetmic.2006.10.005] [PMID]
17. De Been M., Lanza V.F., De Toro M., Scharringa J., Dohmen W., Du Y., Hu J., Lei Y., Li N., Tooming-Klunderud A., Heederik D.J.J., Fluit A.C., et al. (2014). Dissemination of cephalosporin resistance genes between Escherichia coli strains from farm animals and humans by specific plasmid lineages. PLoS Genetics. 10: e1004776. [DOI: 10.1371/ journal.pgen.1004776] [DOI:10.1371/journal.pgen.1004776] [PMID] [PMCID]
18. Diarrassouba F., Diarra M.S., Bach S., Delaquis P., Pritchard J., Topp E., Skura B.J. (2007). Antibiotic resistance and virulence genes in commensal Escherichia coli and Salmonella isolates from commercial broiler chicken farms. Journal of Food Protection. 70: 1316-1327. [DOI: 10.4315/0362-028X-70.6. 1316] [DOI:10.4315/0362-028X-70.6.1316] [PMID]
19. Ewers C., Antão E.M., Diehl I., Philipp H.C., Wieler L.H. (2009). Intestine and environment of the chicken as reservoirs for extraintestinal pathogenic Escherichia coli strains with zoonotic potential. Applied and Environmental Microbiology. 75: 184-192. [DOI: 10.1128/AEM.01324-08] [DOI:10.1128/AEM.01324-08] [PMID] [PMCID]
20. Farooq S., Hussain I., Mir M.A., Bhat M.A., Wani S.A. (2009). Isolation of atypical enteropathogenic Escherichia coli and shiga toxin 1 and 2f-producing Escherichia coli from avian species in India. Letters in Applied Microbiology. 48: 692-697. [DOI: 10.1111/j.1472-765X.2009.02594.x] [DOI:10.1111/j.1472-765X.2009.02594.x] [PMID]
21. Germani Y., Bégaud E., Le Bouguénec C. (1997). Detection of the Escherichia coli attaching and effacing gene (eaeA) in enteropathogenic strains by polymerase chain reaction. Research in Microbiology. 148: 177-181. [DOI: 10.1016/ S0923-2508(97)87648-6] [DOI:10.1016/S0923-2508(97)87648-6]
22. Gomes T.A.T., Elias W.P., Scaletsky I.C.A., Guth B.E.C., Rodrigues J.F., Piazza R.M.F., Ferreira L.C.S., Martinez M.B. (2016). Diarrheagenic Escherichia coli. Brazilian Journal of Microbiology. 47: 3-30. [DOI: 10.1016/j.bjm.2016.10.015] [DOI:10.1016/j.bjm.2016.10.015] [PMID] [PMCID]
23. Guiral E., Mendez-Arancibia E., Soto S.M., Salvador P., Fàbrega A., Gascón J., Vila J. (2011). CTX-M-15-producing enteroaggregative Escherichia coli as cause of travelers' diarrhea. Emerging Infectious Diseases. 17: 1950-1953. [DOI: 10.3201/eid1710.110022] [DOI:10.3201/eid1710.110022] [PMID] [PMCID]
24. Islam M.M., Islam M.N., Sharifuzzaman, Fakhruzzaman M. (2014). Isolation and identification of Escherichia coli and Salmonella from poultry litter and feed. International Journal of Natural and Social Sciences. 1: 1-7.
25. Jay M.T., Garrett V., Mohle-Boetani J.C., Barros M., Farrar J.A., Rios R., Abbott S., Sowadsky R., Komatsu K., Mandrell R., Sobel J., Werner S.B. (2004). A multistate outbreak of Escherichia coli O157:H7 infection linked to consumption of beef tacos at a fast-food restaurant chain. Clinical Infectious Diseases. 39: 1-7. [DOI: 10.1086/421088] [DOI:10.1086/421088] [PMID]
26. Jensen B.H., Olsen K.E.P., Struve C., Krogfelt K.A., Petersen A.M. (2014). Epidemiology and clinical manifestations of enteroaggregative Escherichia coli. Clinical Microbiology Reviews. 27: 614-630. [DOI: 10.1128/CMR.00112-13] [DOI:10.1128/CMR.00112-13] [PMID] [PMCID]
27. Kagambèga A., Martikainen O., Lienemann T., Siitonen A., Traoré A.S., Barro N., Haukka K. (2012a). Diarrheagenic Escherichia coli detected by 16-plex PCR in raw meat and beef intestines sold at local markets in Ouagadougou, Burkina Faso. International Journal of Food Microbiology. 153: 154-158. [DOI: 10.1016/j.ijfoodmicro.2011.10.032] [DOI:10.1016/j.ijfoodmicro.2011.10.032] [PMID]
28. Kagambèga A., Martikainen O., Siitonen A., Traoré A.S., Barro N., Haukka K. (2012b). Prevalence of diarrheagenic Escherichia coli virulence genes in the feces of slaughtered cattle, chickens, and pigs in Burkina Faso. Microbiology Open. 1: 276-284. [DOI: 10.1002/mbo3.30] [DOI:10.1002/mbo3.30] [PMID] [PMCID]
29. Kaper J.B., Nataro J.P., Mobley H.L.T. (2004). Pathogenic Escherichia coli. Nature Reviews Microbiology. 2: 123-140. [DOI: 10.1038/nrmicro818] [DOI:10.1038/nrmicro818] [PMID]
30. Khalil U., Younus M., Asghar N., Siddiqui F., Gómez-Duarte O.G., Wren B.W., Bokhari H. (2016). Phenotypic and genotypic characterization of enteroaggregative Escherichia coli isolates from pediatric population in Pakistan. Journal of Pathology, Microbiology and Immunology. 124: 872-880. [DOI: 10.1111/ apm.12577] [DOI:10.1111/apm.12577] [PMID]
31. Lan R., Alles M.C., Donohoe K., Martinez M.B., Reeves P.R. (2004). Molecular evolutionary relationships of enteroinvasive Escherichia coli and Shigella spp. Infection and Immunity. 72: 5080-5088. [DOI: 10.1128/IAI.72.9.5080-5088.2004] [DOI:10.1128/IAI.72.9.5080-5088.2004] [PMID] [PMCID]
32. Lorenz T.C. (2012). Polymerase chain reaction: basic protocol plus troubleshooting and optimization strategies. Journal of Visualized Experiments. 63: e3998. [DOI: 10.3791/3998] [DOI:10.3791/3998] [PMID] [PMCID]
33. Miles T.D., McLaughlin W., Brown P.D. (2006). Antimicrobial resistance of Escherichia coli isolates from broiler chickens and humans. BMC Veterinary Research. 2: 7. [DOI: 10.1186/ 1746-6148-2-7] [DOI:10.1186/1746-6148-2-7] [PMID] [PMCID]
34. Mo S.S., Sunde M., IIag H.K., Langsrud S., Heir E. (2017). Transfer potential of plasmids conferring extended-spectrum-cephalosporin resistance in Escherichia coli from poultry. Applied and Environmental Microbiology. 83: e00654-17. [DOI: 10.1128/AEM.00654-17] [DOI:10.1128/AEM.00654-17]
35. Mohsin M., Hussain A., Butt M.A., Bashir S., Tariq A., Babar S., Ali A., Haque A., Sarwar Y., Haque A. (2007). Prevalence of shiga toxin-producing Escherichia coli in diarrheal patients in Faisalabad region of Pakistan as determined by multiplex PCR. Journal of Infection in Developing Countries. 1: 164-169.
36. Müller E.E., Ehlers M.M., Grabow W.O.K. (2001). The occurrence of E. Coli O157:H7 in South African water sources intended for direct and indirect human consumption. Water Research. 35: 3085-3088. [DOI: 10.1016/S0043-1354(00)00597-2] [DOI:10.1016/S0043-1354(00)00597-2]
37. Müller D., Greune L., Heusipp G., Karch H., Fruth A., Tschäpe H., Schmidt M.A. (2007). Identification of unconventional intestinal pathogenic Escherichia coli isolates expressing intermediate virulence factor profiles by using a novel single-step multiplex PCR. Applied and Environmental Microbiology. 73: 3380-3390. [DOI: 10.1128/AEM.02855-06] [DOI:10.1128/AEM.02855-06] [PMID] [PMCID]
38. Ochoa T.J., Barletta F., Contreras C., Mercado E. (2008). New insights into the epidemiology of enteropathogenic Escherichia coli infection. Transactions of the Royal Society of Tropical Medicine and Hygiene. 102: 852-856. [DOI: 10.1016/j.trstmh.2008.03.017] [DOI:10.1016/j.trstmh.2008.03.017] [PMID] [PMCID]
39. Oh J.-Y., Kang M.-S., An B.-K., Shin E.-G., Kim M.-J., Kim Y.-J., Kwon Y.-K. (2012). Prevalence and characteristics of intimin-producing Escherichia coli strains isolated from healthy chickens in Korea. Poultry Science. 91: 2438-2443. [DOI: 10.3382/ps.2012-02301] [DOI:10.3382/ps.2012-02301] [PMID]
40. Sacristán C., Esperón F., Herrera-León S., Iglesias I., Neves E., Nogal V., Muñoz M.J., De La Torre A. (2014). Virulence genes, antibiotic resistance and integrons in Escherichia coli strains isolated from synanthropic birds from Spain. Avian Pathology. 43: 172-175. [DOI: 10.1080/03079457.2014. 897683] [DOI:10.1080/03079457.2014.897683] [PMID]
41. Sartz L., De Jong B., Hjertqvist M., Plym-Forshell L., Alsterlund R., Lofdahl S., Osterman B., Stahl A., Eriksson E., Hansson H.-B., Karpman D. (2008). An outbreak of Escherichia coli O157:H7 infection in southern Sweden associated with consumption of fermented sausage; aspects of sausage production that increase the risk of contamination. Epidemiology and Infection. 136: 370-380. [DOI: 10.1017/ S0950268807008473] [DOI:10.1017/S0950268807008473] [PMID] [PMCID]
42. Vidal M., Kruger E., Durán C., Lagos R., Levine M., Prado V., Toro C., Vidal R. (2005). Single multiplex PCR assay to identify simultaneously the six categories of diarrheagenic Escherichia coli associated with enteric infections. Journal of Clinical Microbiology. 43: 5362-5365. [DOI: 10.1128/JCM. 43.10.5362-5365.2005] [DOI:10.1128/JCM.43.10.5362-5365.2005] [PMID] [PMCID]
43. Wang L., Zhang S., Zheng D., Fujihara S., Wakabayashi A., Okahata K., Suzuki M., Saeki A., Nakamura H., Hara-Kudo Y., Kage-Nakadai E., Nishikawa Y. (2017). Prevalence of diarrheagenic Escherichia coli in foods and fecal specimens obtained from cattle, pigs, chickens, asymptomatic carriers, and patients in Osaka and Hyogo, Japan. Japanese Journal of Infectious Diseases. 70: 464-469. [DOI: 10.7883/yoken.JJID. 2016.486] [DOI:10.7883/yoken.JJID.2016.486] [PMID]
| Rights and permissions | |
 |
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
