Prevalence of antibiotic resistance and enterotoxin genes in Staphylococcus aureus producing biofilm isolated from meat and meat products
Subject Areas : Food microbiologyکبری عباسی 1 , Manouchehr Momeni-Shahraki 2
1 - 1. گروه میکروبیولوژی، دانشکده علوم پایه، دانشگاه آزاد اسلامی، واحد شهرکرد، شهرکرد، ایران
2 - گروه بهداشت مواد غذایی، دانشکده دامپزشکی، دانشگاه آزاد شهرکرد، ایران.
Keywords: Staphylococcus aureus, Biofilm, Enterotoxin, Meat,
Abstract :
Staphylococcus aureus is one of the pathogens that can easily infect meat. The present study was performed to evaluate the antimicrobial resistance and distribution of enterotoxin genes in Staphylococcus aureus isolates isolated from raw meat and meat products. 440 samples of raw meat and meat products were collected from suppliers in Shahrekord city and the presence of Staphylococcus aureus was examined using biochemical and molecular tests. The most common enterotoxin genes and genes encoding antibiotic resistance were examined in the presence of specific primers. In this study, out of 440 samples, 61 samples (13.86%) were positive for Staphylococcus aureus. Biofilm reaction was observed in 56 isolates (91.8%). The highest resistance to penicillin (83.60%) and the lowest resistance to vancomycin (0%). The frequency of the presence of sea, seb, sec and sed genes in the studied isolates were reported 39.34%, 27.86%, 26.22% and 37.70%, respectively. Considering that there was a statistically significant relationship between antibiotic resistance genes and biofilm production, it is clear that antibiotic resistance in strains that are able to produce biofilm compared to strains that are not able to produce biofilms are more
1. Wu, D., Li, X., Yang, Y., Zheng, Y., Wang, C., Deng, L., and et al. 2011. Superantigen gene profiles and presence of exfoliative toxin genes in community-acquired meticillin-resistant Staphylococcus aureus isolated from Chinese children. J Med Microb. 60 (1): 35- 45.
2. Momtaz, H., Dehkordi, F.S., Rahimi, E., Asgarifar, A., and Momeni, M. 2013. Virulence genes and antimicrobial resistance profiles of Staphylococcus aureus isolated from chicken meat in Isfahan province, Iran. J Appl Poult Res. 22(4): 913–921.
3. Steinberg, J.P., Clark, C.C., and Hackman, B.O. 1996. Nosocomial and community acquired Staphylococcus aureus bacteremias from 1980 to 1993: impact of intravascular devices and methicillin resistance. Clin Infect Di. 23(2): 255-259.
4. Eftekhar, F., Rezaee, R., Azad, M., Azimi, H., Goudarzi, H., and Goudarzi., M. 2017. Distribution of adhesion and toxin genes in staphylococcus aureus strains recovered from hospitalized patients admitted to the ICU. Arch Pediatr Infect Dis. 5(1):1-8.
5. Imani-Fooladi, A.A., Riazipour, M., and Sattari, M. 2010. Molecular and serological detection of enterotoxigenic Staphylococcus aureus from traditionally dairy products. J Shahrekord Uni Med Sci. 11: 19-26.
6. Zhang, K., Sparling, J., Chow, B.L., Elsayed, S., Hussain, Z., Church, D.L., and et al. 2004. New Quadriplex PCR Assay for Detection of Methicillin and Mupirocin Resistance and Simultaneous Discrimination of Staphylococcus aureus from Coagulase-Negative Staphylococci. J Clin Microbiol. 42(11): 4947-455.
7. Aydin, A., Sudagidan, M., and Muratoglu, K. 2011. Prevalence of staphylococcal enterotoxins, toxin genes and genetic-relatedness of foodborne Staphylococcus aureus strains isolated in the Marmara Region of Turkey. Int J Food Microbiol. 148 (2): 99-106.
8. Hoffman, L.R., Argenio, D.A., MacCoss, M.J., Zhang, Z., Jones, R.A., and Miller, S.L. 2005. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature, 436: 1171–1175.
9. CLSI. 2017. Performance standards for antimicrobial susceptibility testing; twentyfifth informational supplement. CLSI document M100-S25. Wayne: Clinical and Laboratory Standards Institute
10. Kaplan, J.B. 2011. Antibiotic-induced biofilm formation. Int J Artif Organs. 34: 737–751.
11. Katsande, S., Matope, M.N., and Pfukenyi, D.M. 2013. Prevalence of mastitis in dairy cows from smallholder farms in Zimbabwe. J Vet Res. 80: 523-527.
12. Kateete, D.P., Kabugo, U., Baluku, H., Nyakarahuka, L., Kyobe, S., and Okee, M. 2013. Prevalence and antimicrobial susceptibility patterns of bacteria from milkmen and cow with clinical mastitis in and around Kampala, Uganda. PLoS ONE. 8: e63413.
13. Eshraghi, S., Salehipour, Z., Pourmand, M.R., Bakhtyari, R., Mardani, N., Amiri, S., and et al. 2009. Prevalence of tst, entC, entA and entA/C genes in staphylococcus aureus strains isolated from different foods. Tehran Univ Med Sci. 67(7): 1145-1152.
14. Mashouf, R.Y., Hosseini, S.M., Mousavi, S.M., and Arabestani, M.R. 2015. Prevalence of enterotoxin genes and antibacterial susceptibility pattern of Staphylococcus aureus strains isolated from animal originated foods in West of Iran. Oman Med J. 30: 283-290.
15. Hosseini, S.M., Arabestani, M.R., Mahmoodi, H., and Farhangara, E. 2015. Prevalence of G, H, I, J enterotoxin genes and antibacterial susceptibility pattern in Staphylococcus aureus strains isolated from different foods. J Mazandaran Univ Med Sci. 25(123): 1-10.
16. Mack, D., Beckerb, P., Chatterjeec, I., Dobinskya, S., Knoblocha, JKM., and Petersb G. 2004. Mechanisms biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: functional molecules, regulatory circuits, and adaptive responses. Int J Med Microbiol. 294(2): 203–212.
17. Shojaei, M., Karimi, D.H., and Javadi., A. 2014. Distribution of genes encoding
biofilm production in S. aureus isolated from raw milk in Kurdistan. J Food
Hygiene. 14;4(14):1-8.
18. Khoramian, B., Emaneini, M.E., Bolourchi, M.,and Eslampour, MA. 2009. Evaluation of the biofilm-forming ability of Staphylococcus aureus isolates from bovine mastitis in Iran. J Comp Pathobiol; 6(4):109-114
19. Normanno, G., Corrente, M.L., and Salandra, G. 2007. Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animal origin product in Italy. Int J Food Microbiol. 2007; 219-22.
20. Founou, L.L., Founou, R.C., Essack, S.Y.2016.. Antibiotic resistance in the food chain: a developing country-perspective. Frontiers microbiol. 15;7:1881-1890.
21. Chang, Q., Wang, W., Regev‐Yochay, G., and Lipsitch, M. 2015. Antibiotics in agriculture and the risk to human health: how worried should we be? Evolutionary applications.8:240-247.
22. Ge B., Mukherjee, S., Hsu, C.H., Davis., J.A, Tran., T.T.T., and Yang Q. 2017. MRSA and multidrug-resistant Staphylococcus aureus in US retail meats, 2010-2011. Food Microbiol. 62:289-297.
23. Tang., Y, Larsen., J, Kjeldgaard., J, Andersen., P.S., Skov., R, and Ingmer., H. 2017. Methicillin-resistant and-susceptible Staphylococcus aureus from retail meat in Denmark. Int j Food Microbiol. 2017; 249:72- 276.
24. Wu., S, Huang., J, Wu., Q, Zhang., J, Zhang., F, and Yang., X. 2018. Staphylococcus aureus isolated from retail meat and meat products in China: incidence, antibiotic resistance and genetic diversity. Frontiers Microbiol.9 (2):2767-2783.
25. Xing., X, Li., G., Zhang, W., Wang, X., Xia, X., and Yang. 2014. Prevalence, antimicrobial susceptibility, and enterotoxin gene detection of Staphylococcus aureus isolates in ready to-eat foods in Shaanxi, People's Republic of China. Journal of food protection. 2014;77:331-334.
26. عزیزخانی، مریم.، و توریان، فهیمه. (1398). ارزیابی فراوانی ژن¬های انتروتوکسین زای استافیلوکوکوس اورئوس جدا شده از نمونه¬¬های گوشت چرخ شده اغذیه فروشی¬های استان مازندران. مجله تحقیقات دامپزشکی. 74 (1): 65-72.