Et Örneklerinden İzole Edilen Staphylococcus aureus'un Enterotoksin Üretimi ve Antibiyotik Direnç Profili

Amaç: Stafilokokal gıda zehirlenmesi, esas olarak enterotoksijenik Staphylococcus aureus tarafından üretilen stafilokokal enterotoksinlerle kontamine olmuş gıdanın yutulmasıyla ortaya çıkan önemli bir insan hastalığıdır. Bu çalışmanın amacı, Giresun ve Trabzon illerinde kasaplarda satılan çiğ et örneklerinde Staphylococcus aureus kontaminasyonu, izolatların enterotoksin kapasiteleri ve çeşitli antibiyotiklere dirençlilikleri bakımından taşıdığı halk sağlığı risklerini değerlendirmektir. Gereç ve Yöntem: Toplam 30 çiğ sığır eti ürünleri ve 38 çiğ tavuk eti ürünleri, mikrokok/stafilokok ve toplam stafilokok varlığı yönünden analiz edildi. İzolatların tanımlanmaları ve antibiyotik dirençlilikleri, VITEK 2 cihazı ile belirlenmiştir. Enzim bağlı immünolojik test tekniği kullanılarak stafilokok izolatlarındaki klasik tip enterotoksin varlıkları belirlenmiş ve tiplendirilmiştir. Bulgular: Mikrokok/stafilokok ve toplam stafilokok mikrobiyal yükleri sırasıyla 101-105 kob/g ve 101-105 kob/g arasında tespit edildi. Çalışılan 68 et örneğinden, toplam 171 adet stafilokok izole edildi. Elde edilen izolatlar içerisinde, çiğ tavuk etinde 1 adet Staphylococcus aureus (% 1.03) izolatı bulundu. Bu izolatın enterotoksin üretme ve E tipi enterotoksin üretme kabiliyetine sahip olduğu bulundu. Staphylococcus aureus izolatı, diğer antibiyotiklere duyarlı iken sadece benzilpenisiline dirençli olarak bulundu. Sonuç: Çalışmanın sonuçları, antibiyotiğe dirençli ve enterotoksijenik Staphylococcus aureus 'un tüketiciler için önemli bir hijyenik risk oluşturduğunu göstermiştir. Stafilokokal gıda zehirlenmesi vakaları açısından risk oluşturması ve zamanla halk sağlığını tehdit etmesi nedeniyle bu konuda kapsamlı çalışmalar yapılmalıdır.

Enterotoxin Production and Antibiotic Resistance Profile of Staphylococcus aureus Isolated from Meat Samples

Objective: Staphylococcal food poisoning is a major human disease that is causes by the ingestion of food contaminated by staphylococcal enterotoxins produced mainly by enterotoxigenic Staphylococcus aureus. The aim of this study was to evaluate the public health risks of the raw meat samples marketed in Giresun and Trabzon provinces regarding the contamination of Staphylococcus aureus, enterotoxin capacity of the isolates and their resistance to various antibiotics. Material and Method: A total of 30 raw bovine meat products and 38 raw chicken meat products were analyzed for micrococci/staphylococci and total staphylococci. The identification and antibiotic resistance of isolates were determined with the VITEK 2 device. Classical type enterotoxin presence in staphylococcal isolates was determined and typed using Enzyme-Linked ImmunoSorbent Assay technique. Results: The microbial loads of micrococci/staphylococci were 101 to 105 cfu/g and total staphylococci 101 to 105 cfu/g, respectively in 68 meat samples. A total of 171 staphylococci organisms were isolated from the studied 68 meat samples. Among the isolates obtained, one isolate (1.03%) detected in the raw chicken meat was found to be Staphylococcus aureus. This isolate was found to have the ability of producing enterotoxin and to produce E type enterotoxin. S.aureus isolate was resistant only to benzylpenicillin, while it was sensitive to other antibiotics. Conclusion: The results of the study indicated that antibiotic-resistant and enterotoxigenic Staphylococcus aureus poses a significant hygienic risk for consumers. Due to the posing a risk for staphylococcal food poisoning cases and threatening public health over time, extensive studies should be conducted on this subject.

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  • 1. Khorshed A, Ozbal Y. Identification of coagulase negative stephylococci isolated from blood cultures and determination and investigation of antibiotic susceptibility. Journal of Health Sciences 2012; 21(3): 153-163.
  • 2. Gonzalez-Martına M, Corberaa JA, Suarez-Bonnet A, Tejedor-Juncoa MT. Virulence factors in coagulase-positive staphylococci of veterinary interest other than Staphylococcus aureus. Veterinary Quarterly 2020; 40(1): 118–131.
  • 3. Erol I. Food Hygiene and Microbiology. First Edition. Ankara: Pozitif Publishing, 2007; 135-145.
  • 4. Bergdoll MS. Enterotoxins: Staphylococci and Staphylococcal Infections (SEA-E). New York: Academic Press, 1983: 559-598.
  • 5. Omoe K, Ishıkawa M, Shımoda Y, Hu DL, Ueda S, Shınagawa K. Detection of seg, seh, and sei genes in Staphylococcus aureus isolates and determination of the enterotoxin productivities of S. aureus isolates harboring seg, seh, or sei genes. Journal of Clinical Microbiology 2002; 40: 857-862.
  • 6. Liu D. Enterotoxin-Producing Staphylococcus aureus. In: Tang YW, Sussman M, Liu D, Poxton I, Schwartzman J editors. Molecular Medical Microbiology. Second Edition, USA: Elsevier, 2015. p. 979-995.
  • 7. Tang J, Tang C, Chen J, et al. Phenotypic characterization and prevalence of enterotoxin genes in Staphylococcus aureus isolates from outbreaks of ilness in Chengdu City. Foodborne Pathogens and Disease 2011; 8: 1317-1320.
  • 8. Yılmaz S 2009. The Investigation of Staphylococcus aureus and Enterotoxin Presence in Raw Milk Presented in Kayseri Region. Erciyes University Institute of Health Sciences, M.Sc. Thesis, 35 pp.
  • 9. Hennekinne JA, De Buyser ML, Dragacci S. Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiol Rev 2012; 36: 815– 836.
  • 10. De Boer E, Zwartkruis-Nahuis JTM, Wit B, Huijsdens XW. Prevalence of methicillin-resistant Staphylococcus aureus in meat. International journal of food microbiology 2009;134: 52–56.
  • 11. Hanson BM, Dressler AE, Harper AL et al. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa. Journal of Infection and Public Health 2011; 4: 169–174.
  • 12. Waters AE, Contente-Cuomo T, Buchhagen J et al. Multidrug-resistant Staphylococcus aureus in US meat and poultry. Clinical Infectious Diseases 2011; 52: 1227–1230. 13. Swartz MN. Use of antimicrobial agents and drug resistance. N. Engl. J. Med 1997; 337: 491–492.
  • 14. Pesavento G, Ducci B, Comodo N, Lonostro A et al. Antimicrobial resistance profile of Staphylococcus aureus isolated from raw meat: A research for methicillin resistant Staphylococcus aureus (MRSA). Food Control 2007; 18: 196-200.
  • 15. Normanno G, La Salandra G, Dambrosio A et al. Occurence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. International Journal of Food Microbiology 2007a: 115(3): 290-296.
  • 16. Morandi S, Brasca M, Andrighetto C, Lombardi A, Lodi R. Phenotypic and genotypic characterization of Staphylococcus aureus strains from Italian dairy products. International Journal of Microbiology 2009; 501362: 1-7.
  • 17. Baird RM, Lee WH. Media used in the detection and enumeration of Staphylococcus aureus. Journal of Food Protection 1995; 26: 15-24.
  • 18. Korpysa-Dzirba W, Osek J. Detection of classical genes and enterotoxins of Staphylococcus aureus isolated from raw milk in the south-east region of Poland. Bulletin of the Veterinary Institute in Pulawy 2014; 58 (4): 559-561.
  • 19. Nonhoff C, Rottiers S, Struelens MJ. Evaluation of the Vitek 2 system for identification and antimicrobial susceptibility testing of Staphylococcus spp. Clinical Microbiology and Infection 2005; 11: 150–153.
  • 20. Kılıç S, Küplülü Ö. Detection the enterotoxin producing capacity of coagulase positive Staphylococcus by EIA (Enzyme Immuno Assay) isolated from turkey meat. Ankara University Faculty of Veterinary Medicine Journal 2009; 56: 183-186.
  • 21. Bingöl EB, Çetin Ö, Çolak H, Hampikyan H. Presence of enterotoxin and verotoxin in Turkish cheeses sold in İstanbul. Turkish Journal of Veterinary Animal Science 2012; 36(4): 424-432.
  • 22. Kelman A, Soong YA, Dupuy N et al. Antimicrobial susceptibility of Staphylococcus aureus from retail ground meats. Journal of food protection 2011; 74: 1625–1629.
  • 23. Taşçı F, Şahindokuyucu F, Öztürk D. Detection of Staphylococcus species and staphylococcal enterotoxins by ELISA in ice cream and cheese consumed in Burdur Province. African Journal of Agricultural Research 2011; 6 (4), 937-942.
  • 24. Can HY, Çelik TH. Detection of enterotoxigenic and antimicrobial resistant S. aureus in Turkish cheeses. Food Control 2012; 24: 100-103.
  • 25. Martins I M, Kabuki DY, Miya NTN, Pereira JL. Occurrence and Characterization of Enterotoxigenic Potential of Staphylococcus Isolated from Dairy Products. Journal of Food Safety, 2014; 34 (3), 185-192.
  • 26. European Food Safety Authority (EFSA). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2014, 2015; 13(12):4329.
  • 27. Pu S, Wang F, Ge B. Characterization of toxin genes and antimicrobial susceptibility of Staphylococcus aureus isolates from Louisiana retail meats. Foodborne Pathog Dis 2011; 8: 299306.
  • 28. Argudín MA, Mendoza MC, González-Hevia MA, Bances M, Guerra B, Rodicioa MR. Genotypes, Exotoxin Gene Content, and Antimicrobial Resistance of Staphylococcus aureus Strains Recovered from Foods and Food Handlers. Applied and Environmental Microbiology 2012; 78 (8): 2930-2935.
  • 29. Park KM, Oh SK, Cha JO, Lee YS, Koo M. Characterization of Antibiotic Resistant Staphylococcus aureus Isolates from Ready-to-Eat Foods in Korea. Journal of the Korean Society for Applied Biological Chemistry 2014; 57 (3): 387−395.
  • 30. Savariraj WR, Ravindran NB, Kannan P, Rao, VA. Occurrence and enterotoxin gene profiles of Staphylococcus aureus isolated from retail chicken meat. Food Science and Technology International 2020; 1–7.
  • 31. Avsaroglu MD. Prevalence of Staphylococcus aureus Isolated From Various Foods of Animal Origin in Kırşehir, Turkey and Their Enterotoxigenicity. Turkish Journal of Agriculture - Food Science and Technology 2016; 4(12): 1179-1184.
  • 32. Ertas N, Gonulalan Z, Yildirim Y, Kum E. Detection of Staphylococcus aureus enterotoxins in sheep cheese and dairy desserts by multiplex PCR technique. Int J Food Microbiol 2010; 142:74–77.
  • 33. Guven K, Mutlu MB, Gulbandilar A, Cakir P. Occurrence and characterization of Staphylococcus aureus isolated from meat and dairy products consumed in Turkey. J Food Safety 2010; 30: 196212.
  • 34. Gücükoğlu A, Kevenk TO, Uyanik T, Çadirci Ö, Terzi G, Alişarli M. Detection of enterotoxigenic Staphylococcus aureus in raw milk and dairy products by multiplex PCR. J Food Sci 2012; 77: M620–M623.
  • 35. Pereira V, Lopes C, Castro A, Silva J, Gibbs P, Teixeira P. Characterization for enterotoxin production, virulence factors, and antibiotic susceptibility of Staphylococcus aureus isolates from various foods in Portugal. Food Microbiology 2009; 26 (3): 278-282.
  • 36. Medveďová A, Studeničová A, Valík L, Horváthová Z. Prevalence and Growth Dynamics of Enterotoxinogenic Staphylococcus aureus Isolates in Slovakian Dairy Products. Czech Journal of Food Science, 2014; 32 (4), 337–341.
  • 37. Uğur M, Nazlı B, Bostan K. Gıda Hijyeni. İstanbul: Teknik Yayınevi, 2001; 57-58 sy.
  • 38. Wang X, Li G, Xia X, Yang B, Xi M, Meng J. Antimicrobial Susceptibility and Molecular Typing of Methicillin-Resistant Staphylococcus aureus in Retail Foods in Shaanxi, China. Foodborne Pathogens and Disease 2014; 11 (4): 281-286.
  • 39. Li S, Wang P, Zhao J, Zhou L et al. Characterization of toxin genes and antimicrobial susceptibility of Staphylococcus aureus from retail raw chicken meat Journal of Food Protection, 2018; 81 (4): 528-533.
  • 40. Ali SS, Moawad SMS, Hussein MA et al. Efficacy of metal oxide nanoparticles as novel antimicrobial agents against multi-drug and multi-virulent Staphylococcus aureus isolates from retail raw chicken meat and giblets. International journal of food microbiology 2021; 344(2021) 109116.
  • 41. Karamatsu ML, Thorp AW, Brown L. Changes in community-associated methicillin-resistant Staphylococcus aureus skin and soft tissue infections presenting to the pediatric emergency department: comparing 2003 to 2008. Pediatr Emerg Care 2012; 28(2): 131–5.
  • 42. Claudia P. Vicetti M, Asuncion M, Amy L, Pablo J. Sanchez. A Decade of Antimicrobial Resistance in Staphylococcus Aureus: A Single Center Experience. PLoS One 2019 Feb 12;14(2):e0212029.
  • 43. Foster TJ. Antibiotic resistance in Staphylococcus aureus. Current status and future prospects. FEMS Microbiology Reviews 2017; 41: 430–449.
  • 44. Yunlei G, Guanghui S, Meiling S, Juan W, Yi W. Prevalence and Therapies of Antibiotic-Resistance in Staphylococcus aureus. Front Cell Infect Microbiol. 2020; 10: 107.
  • 45. Can HY, Elmalı M, Karagöz A. Molecular typing and antimicrobial susceptibility of Staphylococcus aureus strains isolated from raw milk, cheese, minced meat, and chicken meat samples. Korean Journal for Food Science of Animal Resources, 2017; 37(2), 175– 180.
  • 46. Darwish WS, Atia AS, Reda LM, Elhelaly AE, Thompson LA, Eldin WFS. Chicken giblets and wastewater samples as possible sources of methicillin-resistant Staphylococcus aureus Prevalence, enterotoxin production, and antibiotic susceptibility. J Food Safety 2018: 12478.
  • 47. Parvin S, Ali Y, Talukder S, Nahar A et al. Prevalence and Multidrug Resistance Pattern of Methicillin Resistant S. aureus Isolated from Frozen Chicken Meat in Bangladesh. Microorganisms 2021; 9(3): 636.