Detection of genes encoding enterotoxins (SEA-D) in Staphylococcus aureus strains isolated from workers’ nasal samples and creamy pastries of Shiraz confectioneries
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Abstract
Background and Objectives: Staphylococcus aureus is responsible for the majority of food poisoning all around the world. Nasal carriers of S. aureus and foodstuffs need for handling are important sources and vehicles to transmit this pathogen to ready-to-eat foods. According to hygienic standards, confectioners should not be contaminated with S. aureus. This study aimed to detect nasal carriers and creamy pastries contaminated with enterotoxigenic S. aureus in confectioneries of Shiraz, Iran.
Materials and Methods: From the confectioneries of Shiraz city, 27 places in the north, south, center, west, and east areas were selected randomly then 100 creamy pastries samples and 117 nasal swabs were collected. Bacteriological and biochemical tests were performed to isolate S. aureus. The polymerase chain reaction (PCR) test was used to identify the virulence and enterotoxins genes of the S. aureus isolates. Agar disk diffusion was performed to find out the antibiotic resistance of the isolates.
Results: Results revealed that 16.24 and 33 percent of workers and creamy pastries were contaminated with S. aureus respectively. Also, 100%, 37%, 58%, and 6% of nasal samples harbored femA, mecA, sea, and sec genes respectively. According to the results 97%, 70%, 54.5%, and 6% of creamy pastries isolates harbored femA, mecA, sea, and sec genes respectively. No isolate carried seb and sed genes. The results also showed that 41.5% of nasals and 5.5% of creamy pastry isolates harbored both sea and sec genes. The sea was the most common enterotoxin gene observed in nasal and creamy pastries. The results of the antimicrobial resistance test showed that 68.42% of nasal and 48.48% of creamy pastry isolates were resistant to cefocxitn (FOX) respectively. Both nasal (89%) and creamy pastry (82%) isolates presented the highest resistance to penicillin (P) and the most sensitivity to trimethoprim-sulphamethoxazole (SXT) (94%). Most of the isolates were sensitive to erythromycin (E), aztreonam (AZM), tetracycline (TE), trimethoprim (TMP), and ciprofloxacin (CP). Isolates of S. aureus harboring multi-enterotoxin genes were resistant to more antibiotics than others.
Conclusion: The presence of enterotoxigenic S. aureus in the workers’ nasal samples and creamy pastries of Shiraz confectioneries was high which is a potential public health hazard.
2. Lahou E, Jacxsens L, Daelman J, Van Landeghem F, Uyttendaele M. Microbiological performance of a food safety management system in a food service operation. J Food Prot 2012; 75: 706-716.
3. Lipcsei LE, Brown LG, Coleman EW, Kramer A, Masters M, Wittry BC, et al. Foodborne illness outbreaks at retail establishments—National Environmental Assessment Reporting System, 16 state and local health departments, 2014–2016. MMWR Surveill Summ 2019; 68: 1-20.
4. Jay JM, Loessner MJ, Golden DA. Modern Food Microbiology. Springer 2005.
5. Argaw S, Addis M. A review on staphylococcal food poisoning. Food Sci Qual Manag 2015; 40: 59-71.
6. Argudín MÁ, Mendoza MC, Rodicio MR. Food poisoning and Staphylococcus aureus enterotoxins. Toxins (Basel) 2010; 2: 1751-1773.
7. Grispoldi L, Karama M, Armani A, Hadjicharalambous C, Cenci-Goga BT. Staphylococcus aureus enterotoxin in food of animal origin and staphylococcal food poisoning risk assessment from farm to table. Ital J Anim Sci 2021; 20: 677-690.
8. Church NA, McKillip JK. Antibiotic resistance crisis: challenges and imperatives. Biologia 2021; 76: 1535-1550.
9. Parthasarathy AK, Chougale RA. Antibiotic resistant Staphylococcus aureus. Insights into drug resistance in Staphylococcus aureus. Intech Open 2021. pp. 114-139.
10. Sharifzadeh A, Hajsharifi-Shahreza M, Ghasemi-Dehkordi P. Evaluation of microbialcontamination and chemical qualities of cream-filled pastries in confectioneries of Chaharmahal Va Bakhtiari province (Southwestern Iran). Osong Public Health Res Perspect 2016; 7: 346-350.
11. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing. 28th ed. CLSI supplement M100. Wayne, PA: USA, 2018.
12. Mahfoozi A, Shirzad-Aski H, Kaboosi H, Ghaemi E. Identification of the classical enterotoxin genes of Staphylococcus aureus in various foods by multiplex PCR assay. Iran J Vet Res 2019; 20: 209-212.
13. Arabestani MR, Kamarehei F, Dini M, Aziz Jalilian F, Moradi A, Shokoohizadeh L. Characterization of Staphylococcus aureus isolates from pastry samples by rep-PCR and phage typing. Iran J Microbiol 2022; 14: 76-83.
14. Sami M, Nasri A, Bagheri M, Sharifi H. Microbiological and chemical qualities of cream-filled pastries sold in Kerman city confectioneries, southeast of Iran. Eurasian J Vet Sci 2013; 29: 138-142.
15. Aghalari Z, Hosseini SR, Jafarian S, Rezazadeh M, Mirzaei M, Esmaeili E, et al. Evaluation of chemical and microbial quality of food in northern Iran. J Health Popul Nutr 2021; 40: 40.
16. Aycicek H, Cakiroglu S, Stevenson TH. Incidence of Staphylococcus aureus in ready-to-eat meals from military cafeterias in Ankara, Turkey. Food Control 2005; 16: 531-534.
17. Rezaei A, Pajohi-Alamoti MR, Mohammadzadeh A, Mahmoodi P. Detection of gene encoding enterotoxin a in Staphylococcus aureus isolated from cream pastries. J Food Qual Hazards Control 2018; 5: 24-28.
18. Asgarpoor D, Bahrami M, Daneshamooz S, Ghasemi M. Identification of Staphylococcus aureus enterotoxin genes of SEA, SEB and SEC among healthy carriers in Ardabil city. Iran J Med Microbiol 2018; 11: 149-157.
19. Bencardino D, Amagliani G, Brandi G. Carriage of Staphylococcus aureus among food handlers: An ongoing challenge in public health. Food Control 2021; 130: 108362.
20. Machado V, Pardo L, Cuello D, Giudice G, Luna PC, Varela G, et al. Presence of genes encoding enterotoxins in Staphylococcus aureus isolates recovered from food, food establishment surfaces and cases of foodborne diseases. Rev Inst Med Trop Sao Paulo 2020; 62: e5.
21. Soltan Dallal MM, Abrishamchian Langroudi SM, Pourmoradian M, Asadpour S. Frequency distribution of methicillin-resistant Staphylococcus aureus isolated from foods on sale in the south of Tehran, Iran in 2018-19. J Sch Public Health Inst Public Health Res 2020; 18: 17-28.
22. Mirzababaei M, Soltan Dallal MM, Fard RMN, Asl HM, Pourmoradian M. Prevalence of SEA and SEB producing Staphylococcus aureus isolated from foodborne-outbreaks in Iran. African J Microbiol Res 2021; 15: 535-542.
23. Hashemi Z, Bonyadian M, Moshtaghi H. Evaluation of antibiotic resistance pattern of enterotoxin-producing Staphylococcus aureus isolated from creamy pastries in Shahrekord area. J Food Microbiol 2020; 8: 76-87.
24. Jassim SA, Kandala NJ. Molecular detection of enterotoxin genes of multiresistant Staphylococcus aureus isolates from different sources of food. Iraqi J Sci 2021; 62: 61-74.
25. da Silva AC, Rodrigues MX, Silva NCC. Methicillin-resistant Staphylococcus aureus in food and the prevalence in Brazil : a review. Braz J Microbiol 2020; 51: 347-356.
26. Fooladvand S, Sarmadian H, Habibi D, Van Belkum A, Ghaznavi-Rad E. High prevalence of methicillin resistant and enterotoxin gene-positive Staphylococcus aureus among nasally colonized food handlers in central Iran. Eur J Clin Microbiol Infect Dis 2019; 38: 87-92.
27. Islam MA, Parveen S, Rahman M, Huq M, Nabi A, Khan ZUM, et al. Occurrence and characterization of methicillin-resistant Staphylococcus aureus in processed raw foods and ready-to-eat foods in an urban setting of a developing country. Front Microbiol 2019; 10: 503.
| Files | ||
| Issue | Vol 15 No 2 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i2.12477 | |
| Keywords | ||
| Staphylococcus aureus; Creamy pastry; Enterotoxin genes; Antibiotic resistance | ||
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