Detection of classical enterotoxins of Staphylococcus aureus isolates from chicken nugget and ready to eat foods in Esfahan province by ELISA technique

Subject Areas : Food Science and Technology

هاجر  madahi ¹ (Msc Student of Food Science and Technology, College of Agriculture, Shahrekord Branch, Islamic Azad University, Shahrekord, Iran)
فاطمه  Rostami ² (Msc Student of Food Science and Technology, College of Agriculture, Shahrekord Branch, Islamic Azad University, Shahrekord, Iran.)
ابراهیم  Rahimi ³ (Associate Professor, Department of Food Hygiene and Public Health, College of Veterinary Medicine, Shahrekord Branch, Islamic AzadUniversity, Shahrekord, Iran.)
فرهاد  Safarpoor Dehkordi ⁴ (Member of Young Research Club, Shahrekord Branch, Islamic AzadUniversity, Shahrekord, Iran.)
محمد  Jalali ⁵ (Associate Professor, Infectious Disease and Tropical Medicine Research Center and School of Food Science and Nutrition, Isfahan University of Medical Sciences, Isfahan, Iran.)

Received: 2013-10-19 Accepted : 2014-06-23 Published : 2013-11-22

Keywords: Staphylococcus aureus, Elisa, Staphylococcal enterotoxins, Chicken nugget,

Abstract :

This study was conducted to detect the classical enterotoxins of Staphylococcus aureus isolated from chicken nugget and ready-to-eat foods in Esfahan province by ELISA technique. During summer 2012, a total number of 420 chicken nuggets was collected randomly from retails of Esfahan province. The samples were subjected to bacteriological examinations. The isolates were analyzed for the production of enterotoxins using ELISA techniques. The ability to synthesize Staphylococcal enterotoxins (SEs) was determined in 20 of 24 (83.3%) isolates, which SEA was the most common (40%) enterotoxin found in the isolates. Afterwards, SEC (15%) and SED (10%) were the most detected enterotoxins. Amongst, three strains were able to synthesize both of the SEA and SED and three isolates were able to synthesize both of SEA and SEC. However, no isolate was able to produced SEE. Results showed that chicken nugget and ready-to-eat foods can potentially be a source of staphylococcal food poisoning. Therefore, it is important to study the prevalence of enterotoxigenic S. aureus in the other food types.

References:

• اشراقی، سعید؛ صالحی‌پور، زهره؛ پورمند، محمدرضا؛ رحیمی فروشانی، عباس؛ زهرایی صالحی، محمدتقی؛ آقا امیری، سولماز؛ بختیاری، روناک و همکاران (1392). بررسی توزیع فراوانی ژن­های  tstبا ژن­های  entC، entA و entA/C در ایزوله‌های استافیلوکوکوس اورئوسهای جدا شده از مواد غذایی مختلف. مجله علوم پزشکی تهران، دوره 67، شماره 7، صفحات: 476-470.
  
  
  
  • Aycicek, H., Cakiroglu, S. and Stevenson, T.H. (2005). Incidence of S.aureus in ready-to-eat meals from military cafeterias in Ankara, Turkey. Food Control, 16: 531-534.
  
  
  • Aydin, A. and Sudagidan, M. (2011). Prevalence of staphylococcal enterotoxins, toxin genes and genetic-relatedness of foodborne Staphylococcus aureus strains isolated in the Marmara Region of Turkey. International Journal of Food Microbiology, 148: 99- 106.
  
  
  • Bostan, K. and Cetin, O. (2006). The presence of Staphylococcus aureus and taphylococcal enterotoxıns in ready-to-cook meatballs and whıte pıckled cheese. Journal of Faculty Veterinary Medical Istanbul University, 32: 31–39.
  
  
  • Chiang, Y.C., Liao, W.W., Fan, C.M., Pai, W.Y., Chiou, C.S. and Tsen, H.Y. (2008). PCR detection of Staphylococcal enterotoxins (SEs) N, O, P, Q, R, U, and survey of SE types in Staphylococcus aureus isolates from food-poisoning cases in Taiwan. International Journal of Food Microbiology, 15: 66-73.
  
  
  • Chomvarin, C., Chantarasuk, Y., Srigulbutr, S., Chareonsudjai, S. and Haicumpar, K. (2006). Enteropathogenic bacteria and enterotoxin-producing Staphylococcus aureus isolated from ready-to-eat foods in Khon Kaen, Thailand. Southeast Asian Journal of Tropic Medical Public Health, 37: 983-990.
  
  
  • Feizi, A., Nazeri, M. and Pilevar, A. (2012). Isolation of Staphylococcus spp. genera from broiler breeder flocks in East Azerbaijan Province of Iran: Prevalence and antimicrobial susceptibility. African Journal of Microbiology Research, 6: 5819-5823.
  
  
  • Fueyo, J.M., Mendoza, M.C. and Martin, M.C. (2005). Enterotoxins and toxic shock syndrometoxin in Staphylococcus aureus recovered from human nasal carriers and manually handled foods: epidemiological and genetic findings. Microbes and Infection, 7: 187-194.
  
  
  • Javadi, A. and Safarmashaei, S. (2011). Microbial profile of marketed broiler meat. Middle East Journal ofScience Research,9: 652-656.
  
  
  • Kiedrowski, M.R., Kavanaugh, J.S., Malone, C.L., Mootz, J.M., Voyich, J.M., Smeltzer, M.S., Bayles, K.W. and Horswil, A.R. (2011). Nuclease Modulates Biofilm Formation in Community Associated Methicillin-Resistant Staphylococcus aureus. Plose One, 6(11): 1-16.
  
  
  • Kluytmans, J.A. and Wertheim, H.F. (2005).Nasal carriage of Staphylococcus aureus and prevention of nosocomial infections, 33(1): 3-8.
  
  
  • Kwon, N.H., Park, K.T., Jung, W.K., Youn, H.Y., Lee, Y., Kim, S.H., et al. (2006). Characteristics of methicillin resistant Staphylococcus aureus isolated from chicken meat and hospitalized dogs in Korea and their epidemiological relatedness. Veterinary Microbiology, 117: 304–312.
  
  
  • Lim, S., Joo, Y., Moon, J., Lee, A., Nam, H., Wee, S., et al. (2004). Molecular typing of enterotoxigenic Staphylococcus aureus isolated from bovine mastitis in Korea. Journal of Veterinary Medical Science, 66: 581-584.
  
  
  • Lin, J., Yeh, K.S., Liu, H.T. and Lin, J.H. (2009). Staphylococcus aureus isolated from pork and chicken carcasses in Taiwan: prevalence and antimicrobial susceptibility. Journal of Food Protection, 72: 608-611.
  
  
  • Martin, M.C., Fueyo, J.M., Gonzalez-Hevia, M.A. and Mendoza, M.C. (2004). Genetic procedures for identification of enterotoxigenic strains of Staphylococcus aureus from three food poisoning outbreaks. International Journal of Food Microbiology, 94: 279-286.
  
  
  • McMahon, W.A., Aleo, V.A., Schultz, A.M., Horter, B.L. and Lindberg, K.G. (2003). 3 M Petrifilm Staph Express Count plate method for the enumeration of Staphylococcus aureus in selected types of meat, seafood, and poultry: collaborative study. Journal of AOAC International, 86: 947-953. .
  
  
  • Moon, J.S., Lee, A.R., Jaw, S.H., Kang, H.M., Joo, Y.S. and Park, Y.H. (2007). Comparison of antibiogram, staphylococcal enterotoxin productivity, and coagulase genotypes among Staphylococcus aureus isolated from animal and vegetable sources in Korea. Journal of Food Protection, 70: 2541–2548.
  
  
  • Ng, D.L.K. and Tay, L. (1993). Enterotoxigenic strains of coagulase-positive Staphylococcus aureus in drinks and ready-to-eat foods. Food Microbiology, 10: 317–320.
  
  
  • Normanno, G., Firinu, A., Virgilio, S., Mula, G., Dambrosio, A. and Poggiu, A. (2005). Coagulase-positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. International Journal of Food Microbiology, 98: 73–79.
  
  
  • Normanno, T.G. and La Salandra, G. (2007). Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. International Journal of Food Microbiology, 115: 290–296.
  
  
  • Oh, S.K., Lee, N., Cho, Y.S., Shin, D.B., Choi, S.Y. and Koo, M. (2007). Occurrence of toxigenic Staphylococcus aureus in ready-to-eat food in Korea. Journal of Food Protection, 70: 1153–1158.
  
  
  • Omoe, K. and Ishikawa, M. (2002). Detection of seg, she and sei genes in Staphylococcus aureus isolates and determination of enterotoxins productivities of S. aureus isolates harboring seg, she or sei genes. Journal of Clinical Microbiology, 40: 857-862.
  
  
  • Paciorek, M.L., Kochman, M., Piekarska, K., Grochowska, A. and Windyg, B. (2007). The distribution of enterotoxin and enterotoxin-like genes in Staphylococcus aureus strains isolated from nasal carriers and food samples. International Journal of Food Microbiology, 117(3): 319-323.
  
  
  • Redmond, E.C. and Griffith, C.J. (2003). Consumer food handling in the home: a review of food safety studies. Journal of Food Protectioon, 66: 130-161.
  
  
  • Reji, M.W. and Den Aantrekker, E.D. (2004).Recontamination as a source of pathogens inprocessed foods. International Journal of Food Microbiology, 91: 1-11.
  
  
  • Soltan-Dallal, M.M., Salehipour, Z. and Mehrabadi, Z.F. (2010). Molecular pidemiology of Staphylococcusaureus in food samples based on the protein A gene polymorphic region DNA sequence. Canadian Journal of Microbiology, 56(1): 18-21.
  
  
  • Soriano, J.M., Rico, H., Molto, J.C. and Mares, J. (2002). Effect of introduction of HACCP on the microbiological quality of some restaurant meals. Food Control, 13: 253-261.
  
  
  • Tavakoli, H.R. and Riazipour, M. (2008). Microbial quality of cooked meat foods in Tehran University’s restaurants. Pakistan Journal of Medical Science, 24: 595-599.