Volume 7, Issue 4 (December 2020)                   J. Food Qual. Hazards Control 2020, 7(4): 188-195 | Back to browse issues page

XML Print

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

Momtaz Bokharaei N, Soltan Dallal M, Pourmand M, Rajabi Z. Antibiotic Resistance Pattern and Detection of mecA Gene in Staphylococcus aureus Isolated from Iranian Hamburger Samples. J. Food Qual. Hazards Control. 2020; 7 (4) :188-195
URL: http://jfqhc.ssu.ac.ir/article-1-584-en.html
Division of Food Microbiology, Department of Pathobiology, School of Public Health, Tehran University of Medical Science, Tehran, Iran , soltanda@sina.tums.ac.ir
Abstract:   (759 Views)
Background: Among the bacteria that cause food poisoning, Staphylococcus aureus is one of the most common causes of food poisoning worldwide. The aim of this study was to investigate the presence of S. aureus strains in Iranian hamburgers, analysis of their antibiotic resistance pattern, and molecular detection of mecA gene in isolated strains.
Methods: A total of 100 Iranian handmade (traditional) and packaged (factory-made) hamburger samples were investigated for the existence of S. aureus. The pattern of antibiotic resistance and the presence of mecA genes were investigated by disk diffusion and molecular methods, respectively. Data were statistically analyzed by SPSS software v. 24.
Results: The prevalence of S. aureus isolated in handmade hamburgers was significantly (p=0.008) higher than packaged ones. Most of 39 isolated S. aureus strains were susceptible to ciprofloxacin (31 isolate), chloramphenicol (27 isolate), and trimethoprim/sulfamethoxazole (37 isolate). The highest antibiotic resistance was observed for penicillin G followed by oxacillin and tetracycline. All isolates were found susceptible to vancomycin and gentamicin. Six S. aureus isolates which were evaluated for methicillin-resistance, contained the mecA gene.
Conclusion: The high presence of the S. aureus in Iranian hamburgers and the remarkable antibiotic resistance emphasize the need for policies which enforce hygienic practices within the food industry and fast food outlets.

DOI: 10.18502/jfqhc.7.4.4847
Full-Text [PDF 433 kb]   (437 Downloads)    
Type of Study: Original article | Subject: Special
Received: 19/10/19 | Accepted: 20/05/20 | Published: 20/12/24

1. Acco M., Ferreira F.S., Henriques J.A.P., Tondo E.C. (2003). Identification of multiple strains of Staphylococcus aureus colonizing nasal mucosa of food handlers. Food Microbiology. 20: 489-493. [DOI: 10.1016/S0740-0020(03)00049-2] [DOI:10.1016/S0740-0020(03)00049-2]
2. Al-Zu'bi E., Bdour S., Shehabi A.A. (2004). Antibiotic resistance patterns of mecA-positive Staphylococcus aureus isolates from clinical specimens and nasal carriage. Microbial Drug Resistance. 10: 321-324. [DOI: 10.1089/mdr.2004.10.321] [DOI:10.1089/mdr.2004.10.321] [PMID]
3. Anand K.B., Agrawal P., Kumar S., Kapila K. (2009). Comparison of cefoxitin disc diffusion test, oxacillin screen agar, and PCR for mecA gene for detection of MRSA. Indian Journal of Medical Microbiology. 27: 27-29.
4. Aycicek H., Cakiroglu S., Stevenson T.H. (2005). Incidence of Staphylococcus aureus in ready-to-eat meals from military cafeterias in Ankara, Turkey. Food Control. 16: 531-534. [DOI: 10.1016/j.foodcont.2004.04.005] [DOI:10.1016/j.foodcont.2004.04.005]
5. Baddour M.M., AbuElKheir M.M., Fatani A.J. (2007). Comparison of mecA polymerase chain reaction with phenotypic methods for the detection of methicillin-resistant Staphylococcus aureus. Current Microbiology. 55: 473-479. ]DOI: 10.1007/ s00284-007-9015-6[ [DOI:10.1007/s00284-007-9015-6] [PMID]
6. Berger-Bächi B. (1999). Genetic basis of methicillin resistance in Staphylococcus aureus. Cellular and Molecular Life Sciences. 56: 764-770. [DOI: 10.1007/s000180050023] [DOI:10.1007/s000180050023] [PMID]
7. Boşgelmez-Tınaz G., Ulusoy S., Arıdoğan B., Coşkun-Arı F. (2006). Evaluation of different methods to detect oxacillin-resistance in Staphylococcus aureus and their clinical laboratory utility. European Journal of Clinical Microbiology and Infectious Diseases. 25: 410-412. ]DOI: 10.1007/s10096-006-0153-8[ [DOI:10.1007/s10096-006-0153-8] [PMID]
8. Clinical and Laboratory Standards Institute (CLSI). (2015). Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement. CLSI document M100-S25. Wayne, PA.
9. Contreras C.P.Á., da Silva L.N.N., Ferreira D.C.G., dos Santos Ferreira J., de Castro Almeida R.C. (2015). Prevalence of methicillin-resistant Staphylococcus aureus in raw hamburgers and ready-to-eat sandwiches commercialized in supermarkets and fast food outlets in Brazil. Food and Nutrition Sciences. 6: 1324-1331. ]DOI: 10.4236/fns.2015.614138[ [DOI:10.4236/fns.2015.614138]
10. Deng Y., Liu J., Peters B.M., Chen L., Miao J., Li B., Li L., Chen D., Yu G., Xu Z., Shirtliff M.E. (2015). Antimicrobial resistance investigation on Staphylococcus strains in a local hospital in Guangzhou, China, 2001-2010. Microbial Drug Resistance. 21: 102-104. ]DOI: 10.1089/mdr.2014.0117[ [DOI:10.1089/mdr.2014.0117] [PMID] [PMCID]
11. Deresinski S. (2009). Vancomycin in combination with other antibiotics for the treatment of serious methicillin-resistant Staphylococcus aureus infections. Clinical Infectious Diseases. 49: 1072-1079. ]DOI: 10.1086/605572[ [DOI:10.1086/605572] [PMID]
12. Elhassan M.M., Ozbak H.A., Hemeg H.A., Elmekki M.A., Ahmed L.M. (2015). Absence of the mecA gene in methicillin-resistant Staphylococcus aureus isolated from different clinical specimens in Shendi city, Sudan. BioMed Research International. [DOI:10.1155/2015/895860[ [DOI:10.1155/2015/895860] [PMID] [PMCID]
13. Fernandes C.J., Fernandes L.A., Collignon P. (2005). Cefoxitin resistance as a surrogate marker for the detection of methicillin-resistant Staphylococcus aureus. Journal of Antimicrobial Chemotherapy. 55: 506-510. ]DOI: 10.1093/jac/ dki052[ [DOI:10.1093/jac/dki052] [PMID]
14. Gundogan N., Citak S., Turan E. (2006). Slime production, DNase activity and antibiotic resistance of Staphylococcus aureus isolated from raw milk, pasteurised milk and ice cream samples. Food Control. 17: 389-392. ]DOI:10.1016/j. foodcont.2005.01.006[ [DOI:10.1016/j.foodcont.2005.01.006]
15. Gundogan N., Citak S., Yucel N., Devren A. (2005). A note on the incidence and antibiotic-resistance of Staphylococcus aureus isolated from meat and chicken samples. Meat Science. 69: 807-810. ]DOI: 10.1016/j.meatsci.2004.10.011[ [DOI:10.1016/j.meatsci.2004.10.011] [PMID]
16. Hennekinne J.A., De Buyser M.L., Dragacci S. (2012). Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiology Reviews. 36: 815-836. ]DOI: 10.1111/j.1574-6976.2011.00311.x[ [DOI:10.1111/j.1574-6976.2011.00311.x] [PMID]
17. Iranian National Standardization Organization (INSO). (2016). Raw frozen hamburger-Specifications and test methods. No. 2304.
18. International Organization for Standardization (ISO). (2003). Microbiology of food and animal feeding stuffs-Horizontal method for the enumeration of coagulase-positive staphylococci. Staphylococcus aureus and other species. Part 3: Detection and MPN technique for low numbers. No. 6888-3
19. Lee J.W., Park K.S., Kim J.G., Oh S.H., Lee Y.S., Kim J.H., Byun M.W. (2005). Combined effects of gamma irradiation and rosemary extract on the shelf-life of a ready-to-eat hamburger steak. Radiation Physics and Chemistry. 72: 49-56. ]DOI: 10.1016/j.radphyschem.2004.01.003[ [DOI:10.1016/j.radphyschem.2004.01.003]
20. Mathews A.A., Thomas M., Appalaraju B., Jayalakshmi J. (2010). Evaluation and comparison of tests to detect methicillin-resistant S. aureus. Indian Journal of Pathology and Microbiology. 53: 79-82. ]DOI: 10.4103/0377-4929.59189[ [DOI:10.4103/0377-4929.59189] [PMID]
21. Matsuhashi M., Song M.D., Ishino F., Wachi M., Doi M., Inoue M., Ubukata K., Yamashita N., Konno M. (1986). Molecular cloning of the gene of a penicillin-binding protein supposed to cause high resistance to β-lactam antibiotics in Staphylococcus aureus. Journal of Bacteriology. 167: 975-980. ]DOI: 10. 1128/jb.167.3.975-980.1986[ [DOI:10.1128/JB.167.3.975-980.1986] [PMID] [PMCID]
22. Mimica M.J., Berezin E.N., Carvalho R.L.B., Mimica I.M., Mimica L.M.J., Sáfadi M.A.P., Schneider E., Caiaffa-Filho H.H. (2007). Detection of methicillin resistance in Staphylococcus aureus isolated from pediatric patients: is the cefoxitin disk diffusion test accurate enough? The Brazilian Journal of Infectious Diseases. 11: 415-417. ]DOI: 10.1590/S1413-86702007000400009[ [DOI:10.1590/S1413-86702007000400009] [PMID]
23. Nejad A.S.M., Shabani S., Bayat M., Hosseini S.E. (2014). Antibacterial effect of garlic aqueous extract on Staphylococcus aureus in hamburger. Jundishapur Journal of Microbiology. 7: e13134. ]DOI: 10.5812/jjm.13134[ [DOI:10.5812/jjm.13134] [PMID] [PMCID]
24. Prayson B., McMahon J.T., Prayson R.A. (2008). Fast food hamburgers: what are we really eating? Annals of Diagnostic Pathology. 12: 406-409. ]DOI: 10.1016/j.anndiagpath.2008. 06.002[ [DOI:10.1016/j.anndiagpath.2008.06.002] [PMID]
25. Quinn P. J., Markey B. K., Leonard F.C., FitzPatrick E., Fanning S., Hartigan P. (2011). Veterinary microbiology and microbial disease. 2nd edition .John Wiley & Sons, UK.
26. Raygada J.L., Levine D.P. (2009). Methicillin-resistant Staphylococcus aureus: a growing risk in the hospital and in the community. American Health and Drug Benefits. 2: 86-95.
27. Sakoulas G., Gold H.S., Venkataraman L., Degirolami P.C., Eliopoulos G.M., Qian Q. (2001). Methicillin-resistant Staphylococcus aureus: comparison of susceptibility testing methods and analysis of mecA-positive susceptible strains. Journal of Clinical Microbiology. 39: 3946-3951. [DOI: 10.1128/JCM.39.11.3946-3951.2001[ [DOI:10.1128/JCM.39.11.3946-3951.2001] [PMID] [PMCID]
28. Shahraz F., Dadkhah H., Khaksar R., Mahmoudzadeh M., Hosseini H., Kamran M., Bourke P. (2012). Analysis of antibiotic resistance patterns and detection of mecA gene in Staphylococcus aureus isolated from packaged hamburger. Meat Science. 90: 759-763. ]DOI: 10.1016/j.meatsci.2011.11. 009[ [DOI:10.1016/j.meatsci.2011.11.009] [PMID]
29. Sharifi-Yazdi M.K., Mazaheri Nezhad Fard R., Pourmand M.R., Rajabi Z., Soltan-Dallal M.M. (2016). SEA, SEB and TSST-1 Toxin gene prevalence in Staphylococcus aureus isolated from fish. Annals of Food Processing and Preservation. 1: 1007.
30. Shawish R.R., Al-Humam N.A. (2016). Contamination of beef products with staphylococcal classical enterotoxins in Egypt and Saudi Arabia. GMS Hygiene and Infection Control. 11: 1-6. ]DOI: 10.3205/dgkh000268[
31. Soltan-Dallal M.M., Foroushani A.R., Sharifi-Yazdi S., Sharifi-Yazdi M.K., Arfatahery N. (2015). Prevalence of Staphylococcus aureus in shrimps in Tehran during 2013. Journal of Medical Bacteriology. 4: 42-46.
32. Soltan-Dallal M.M., Khoramizadeh M.R., Agha Amiri S., Saboor Yaraghi A.A., Mazaheri Nezhad Fard R. (2016). Coagulase gene polymorphism of Staphylococcus aureus isolates: a study on dairy food products and other foods in Tehran, Iran. Food Science and Human Wellness. 5: 186-190. ]DOI: 10.1016/j. fshw.2016.09.004[ [DOI:10.1016/j.fshw.2016.09.004]
33. Soltan-Dallal M.M., Salehipour Z., Eshraghi S., Mehrabadi J.F., Bakhtiari R. (2010a). Occurrence and molecular characterization of Staphylococcus aureus strains isolated from meat and dairy products by PCR-RFLP. Annals of Microbiology. 60: 189-196. [DOI: 10.1007/s13213-010-0025-4] [DOI:10.1007/s13213-010-0025-4]
34. Soltan-Dallal M.M., Salehipour Z., Mehrabadi J.F. (2010b). Molecular epidemiology of Staphylococcus aureus in food samples based on the protein A gene polymorphic region DNA sequence. Canadian Journal of Microbiology. 56. ]DOI: 10. 1139/w09-111[ [DOI:10.1139/W09-111] [PMID]
35. Swenson J.M., Tenover F.C., Cefoxitin Disk Study Group. (2005). Results of disk diffusion testing with cefoxitin correlate with presence of mecA in Staphylococcus spp. Journal of Clinical Microbiology. 43: 3818-3823. ]DOI: 10.1128/JCM.43.8.3818-3823.2005[ [DOI:10.1128/JCM.43.8.3818-3823.2005] [PMID] [PMCID]
36. Unno H., Inada M., Nakamura A., Hashimoto M., Ito K., Hashimoto K., Nikaido M., Hayashi T., Hata E., Katsuda K., Kiku Y., Tagawa Y., et al. (2015). Improved rapid and efficient method for Staphylococcus aureus DNA extraction from milk for identification of mastitis pathogens. The Journal of Veterinary Medical Science. 77: 1007-1009. ]DOI: 10.1292/jvms.14-0159[ [DOI:10.1292/jvms.14-0159] [PMID] [PMCID]
37. Velasco D., del Mar Tomas M., Cartelle M., Beceiro A., Perez A., Molina F., Moure R., Villanueva R., Bou G. (2005). Evaluation of different methods for detecting methicillin (oxacillin) resistance in Staphylococcus aureus. Journal of Antimicrobial Chemotherapy. 55: 379-382. ]DOI: 10.1093/jac/ dki017[ [DOI:10.1093/jac/dki017] [PMID]

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

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

© 2022 CC BY-NC 4.0 | Journal of food quality and hazards control

Designed & Developed by : Yektaweb