THE INCIDENCE AND ANTIBIOTIC RESISTANCE OF COAGULASE POSITIVE STAPHYLOCOCCUS AUREUS IN SEAFOODS MARKETED IN IZMIR

Öz

The aims of this study are to check the prevalence of coagulase-positive Staphylococcus aureus in raw and ready-to-eat seafoods samples in İzmir and to determine the antibiotic resistance of the isolates. For this purpose, 50 samples of raw and ready-to-use seafoods were analyzed. As a result of the study, coagulase positive S. aureus was detected in 24 (58%) raw and 26 (46%) ready-to-eat seafoods. While all S. aureus isolates were susceptible to ceftazidime, gentamycin, clindamycin, nitrofurantoin, ofloxacin, oxacillin, rifampicin, vancomycin and amicasin, the isolates were resistance to amoxicillin-clavulanic acid and ciprofloxacin (7.7%), cephalotine (3.8%), meticillin (30.8%), penicillin (80.8%), linezolid (19.2%). Coagulase positive S. aureus is considered a potential hazard to consumers and food safety. Hygiene and sanitation conditions must be considered during production and sales areas in order to prevent the contamination of this bacterium with seafood.

Anahtar Kelimeler

• Seafoods,coagulase positive S. aureus,antibiotic resistance

İZMİR’DE SATIŞA SUNULAN SU ÜRÜNLERİNDE KOAGÜLAZ POZİTİF STAPHYLOCOCCUS AUREUS’UN İNSİDANSI VE ANTİBİYOTİK DİRENCİ

Öz

Bu çalışmanın amacı, İzmir’de satışa sunulan çiğ ve tüketime hazır su ürünlerinde koagülaz pozitif Staphylococcus aureus varlığının tespit edilerek, antibiyotik dirençlerinin belirlenmesidir. Bu amaçla çiğ ve tüketime hazır su ürünlerinden oluşan 50 örnek analiz edilmiştir. Araştırma sonucunda, 24 çiğ su ürününün %58’inde ve 26 tüketime hazır su ürününün %46’sında koagülaz pozitif S. aureus tespit edilmiştir. İzole edilen tüm S. aureus suşları, seftazidim, gentamisin, klindamisin, nitrofurantoin, ofloksasin, oksasilin, rifampisin, vankomisin ve amikasine duyarlı bulunurken, izolatların %7,7’si amoksisilin-klavulanik asit ve siprofloksasine, %3.8’i sefalotine, %30.8’i metisiline, %80.8 penisiline ve %19.2’si linezolide dirençli bulunmuştur. Koagülaz pozitif S. aureus tüketiciler ve gıda güvenliği için potansiyel bir tehlike olarak değerlendirilmektedir. Bu patojenin gıdalara bulaşmasını engellemek için, üretim ve satış alanlarında hijyen ve sanitasyon koşullarına dikkat etmek gerekmektedir. 

Anahtar Kelimeler

• Su ürünleri,koagülaz pozitif S. aureus,antibiyotik direnci

Kaynakça

1. Referans1 Abrahim, A., Sergelidis, D., Kirkoudis, I., Anagnostou, V., Kaitsa-Tsiopoulou, E., Kazila, P., Papa, A. (2010). Isolation and antimicrobial resistance of Staphylococcus spp. in freshwater fish and Greek marketplaces. J. Aquatic Food Prod. Tech. 19: 93–102, doi:10.1080/10498850.2010.491597.
2. Referans2 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 Microbiol, 20(5):489-493, doi:10.1016/S0740-0020(03)00049-2.
3. Referans3 Anonymous, 2000. Merck Gıda Mikrobiyolojisi ve Uygulamaları. Genişletilmiş 2. Baskı, Ankara Üniversitesi Ziraat Fakültesi Gıda Mühendisliği Bölümü Yayını, Sim Matbaası, Ankara, Türkiye, 522 s.
4. Referans4 Argudin, M.A., Mendoza, M.C., Rodicio, M.R. (2010). Food poisoning and Staphylococcus aureus enterotoxins. Toxins, 2(7):1751-1773, doi: 10.3390/toxins2071751.
5. Referans5 Arslan, S., Özdemir, F. (2017). Molecular characterization and detection of enterotoxins, methicillin resistance genes and antimicrobial resistance of Staphylococcus aureus from fish and ground beef. Pol J Vet Sci, 20(1):85-94, doi: 10.1515/pjvs-2017-0012.
6. Referans6 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(6),531-534, doi: 10 10.16/j.foodcont.2004.04.005.
7. Referans7 Ayulo, A.M.R., Machado, R.A., Scussel, V.M. (1994). Enterotoxigenic Escherichia coli and Staphylococcus aureus in fish and seafood from the southern region of Brazil. Int J Food Microbiol, 24(1-2):171-178, doi: 10.1016/0168-1605(94)90116-3.
8. Referans8 Beleneva, I.A. (2011). Incidence and characteristics of Staphylococcus aureus and Listeria monocytogenes from the Japan and South China seas. Mar Pollut Bull, 62(2):382-387, doi: 10.1016/j.marpolbul.2010.09.024.

9. Referans9 Bogdanovicova, K., Necidova, L., Harustiakova, D., Janstova, B. (2017). Milk powder risk assessment with Staphylococcus aureus toxigenic strains. Food Control, 73,2-7, doi: 10.1016/j.foodcont.2016.07.007.
10. Referans10 Byun, J.W., Park, S., Benno, Y. (1997). Probiotic effect of Lactobacillus sp. DS–12 in flounder (Paralichthys olivaceus). J Gen Appl Microbiol, 43, 305-308, doi: 10.2323/jgam.43.305.
11. Referans11 Çakıcı, N., Demirel Zorba, N. N., Akçalı, A. (2015). Food industry employees and staphylococcal food poisoning. Turk Hij Den Biyol Derg, 72(4):337-350, doi: 10.5505/TurkHijyen.2016.21704.
12. Referans12 Demirci, M., Tombul, F., Yiğin, A., Altun, S.K. (2017). Investigation of Staphylococcus aureus enterotoxins A to E via real-time PCR from various food samples in Turkey. Pak Vet J, 37(1):100-104.
13. Referans13 Erol, İ., İşeri, Ö. (2004). Stafilokokal enterotoksinler. Ankara Üniv Vet Fak Derg, 51,239-245.
14. Referans14 Fetsch, A., Contzen, M., Hartelt, K., Kleiser, A., Maassen, S., Rau, J., Kraushaar, B., Layer F., Strommenger, B. (2014). Staphylococcus aureus food-poisoning outbreak associated with the consumption of ice-cream. Int J Food Microbiol, 187,1-6, doi: 10.1016/j.ijfoodmicro.2014.06.017.
15. Referans15 Fijałkowski, K., Peitler, D., Karakulska, J. (2016). Staphylococci isolated from ready-to-eat meat-Identification, antibiotic resistance and toxin gene profile. Int J Food Microbiol, 238,113-120, doi: 10.1016/j.ijfoodmicro.2016.09.001.
16. Referans16 Gomez-Gil, B., Roque, A., Turnbull, J.F. (2000). The use and selection of probiotic bacteria for use in the culture of larval aquatic organisms. Aquaculture, 191, 259-270, doi: 10.1016/S0044-8486(00)00431-2.
17. Referans17 Grigoryan, K., Badalyan, G., Andriasyan, D. (2010). Prevalence of Staphylococcus aureus in fish processing factory. Potravinarstvo 4(2):25–28, doi:10.5219/47.
18. Referans18 Gündoğan, 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: doi.org/10.1016/j.foodcont.2005.01.006.
19. Referans19 Hammad, A.M., Watanabe, W., Fujii, T., Shimamoto, T. (2012). Occurrence and characteristics of methicillin-resistant and-susceptible Staphylococcus aureus and methicillin-resistant coagulase-negative staphylococci from Japanese retail ready-to-eat raw fish. Int J Food Microbiol, 156(3):286-289, doi: 10.1016/j.ijfoodmicro.2012.03.022.
20. Referans20 Herrera, F.C., Santos, J.A., Otero, A., García‐López, M.L. (2006). Occurrence of foodborne pathogenic bacteria in retail prepackaged portions of marine fish in Spain. J Appl Microbiol, 100(3):527-536, doi: 10.1111/j.1365-2672.2005.02848.x.
21. Referans21 Koluman, A., Unlu, T., Dikici, A., Tezel, A., Akcelik, E.N., Burkan, Z.T. (2011). Presence of Staphylococcus aureus and staphylococcal enterotoxins in different foods. Kafkas Univ Vet Fak Derg, 17 (Suppl A),55-60.
22. Referans22 Kumar, L.R., Kasim, A.K., Lekshmi, M., Nayak, B.B., Kumar, S. (2016). Incidence of methicillin-resistant staphylococci in fresh seafood. Adv Microbiol, 6(06):399-406, doi: 10.4236/aim.2016.66039.
23. Referans23 Küçükçetin, A., Milci, S. (2008). Staphylococcus aureus ile kontamine olan peynirlerden kaynaklanan gıda zehirlenmeler, Gıda, 33(3):129-135.
24. Referans24 Le Loir, Y., Baron, F., Gautier, M. (2003). Staphylococcus aureus and food poisoning. Genet Mol Res, 2(1):63-76.
25. Referans25 Murray, R.J. (2005). Recognition and management of Staphylococcus aureus toxin‐mediated disease. Intern Med J, 35(2):106-119, doi: 10.1111/j.1444-0903.2005.00984.x.
26. Referans26 National Committee for Clinical and Laboratory Standards Institute. 2008. Performance Standards for Antimicrobial Susceptibility Testing; Eighteenth Informational Supplement (M100-S18).Wayne, PA: Clinical and Laboratory Standards Institute.
27. Referans27 Normanno, G., Firinu, A., Virgilio, S., Mula, G., Dambrosio, A., Poggiu, A., Decastelli, L., Mioni, R., Scuota, S., Bolzoni, G., Di Giannatale, E., Salinetti, A.P., La Salandra, G., Bartoli, M., Zuccon, F., Pirino, T., Sias, S., Parisi, A., Quaglia, N.C., Celano, G.V. (2005). Coagulase-positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. Int J Food Microbiol, 98(1):73-79, doi: 10.1016/j.ijfoodmicro.2004.05.008.
28. Referans28 Normanno, G., La Salandra, G., Dambrosio, A., Quaglia, N. C., Corrente, M., Parisi, A., Santagada, G., Firinu, A., Crisetti, E., Celano, G.V. (2007). Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. Int J Food Microbiol, 115(3):290-296, doi: 10.1016/j.ijfoodmicro.2006.10.049.
29. Referans29 Oh, S.K., Lee, N., Cho, Y.S., Shin, D.B., Choi, S.Y., Koo, M. (2007). Occurrence of toxigenic Staphylococcus aureus in ready-to-eat food in Korea. J Food Prot, 70(5):1153-1158.
30. Referans30 Onmaz, N.E., Abay, S., Karadal, F., Hizlisoy, H., Telli, N., Al, S. (2015). Occurence and antimicrobial resistance of Staphylococcus aureus and Salmonella spp. in retail fish samples in Turkey. Mar Pollut Bull, 90(1):242-246, doi: 10.1016/j.marpolbul.2014.10.046.
31. Referans31 Peles, F., Wagner, M., Varga, L., Hein, I., Rieck, P., Gutser, K., Keresztúri, P., Kardos, G.,Turcsányi, I., Béri, B., Szabó, A. (2007). Characterization of Staphylococcus aureus strains isolated from bovine milk in Hungary. Int J Food Microbiol, 118, 186–193, doi: 10.1016/j.ijfoodmicro.2007.07.010.
32. Referans32 Pereira, V., Lopes, C., Castro, A., Silva, J., Gibbs, P., Teixeira, P. (2009). Characterization for enterotoxin production, virulence factors, and antibiotic susceptibility of Staphylococcus aureus isolates from various foods in Portugal. Food Microbiol, 26(3):278-282, doi: 10.1016/j.fm.2008.12.008.
33. Referans33 Pesavento, G., Ducci, B., Comodo, N., Lo-Nostro, A. (2007). Antimicrobial resistance profile of Staphylococcus aureus isolated from raw meat: a research for methicillin resistant Staphylococcus aureus (MRSA). Food Control, 18, 196–200, doi: doi.org/10.1016/j.foodcont.2005.09.013.
34. Referans34 Rhee, C.H., Woo, G.J. (2010). Emergence and characterization of foodborne methicillin-resistant Staphylococcus aureus in Korea. J Food Prot, 73(12): 2285-2290.
35. Referans35 Saito, E., Yoshida, N., Kawano, J., Shimizu, A., Igimi, S. (2011). Isolation of Staphylococcus aureus from raw fish in relation to culture methods. J. Vet. Med. Sci. 73, 287–292, doi: 10.1292/jvms.10-0198.
36. Referans36 Simon, S.S., Sanjeev, S. (2007). Prevalence of enterotoxigenic Staphylococcus aureus in fishery products and fish processing factory workers. Food control, 18(12):1565-1568, doi: 10.1016/j.foodcont.2006.12.007.
37. Referans37 Siriken, B., Yildirim, T., Erol, I., Durupinar, B., Ciftci, A., Onuk, E.E. (2013). Prevalence and characterization of coagulase positive staphylococci isolated from salted anchovy. J Aquat Food Prod T, 22(4):339-352, doi: 10.1080/10498850.2011.651773.
38. Referans38 Sokari, T. (1991). Distribution of enterotoxigenic Staphylococcus aureus in ready-to-eat foods in eastern Nigeria. Int J Food Microbiol, 12(2-3):275-280, doi: 10.1016/0168-1605(91)90079-5.
39. Referans39 Stewart, C.M., Cole, M.B., Schaffner, D.W. (2003). Managing the risk of staphylococcal food poisoning from cream-filled baked goods to meet a food safety objective. J Food Prot, 66(7):1310-1325, doi: 10.4315/0362-028X-66.7.1310.
40. Referans40 Sutherland, J., Varnam, A. (2002). Enterotoxin-producing Staphylococcus, Shigella, Yersinia, Vibrio, Aeromonas and Plesiomonas. Foodborne pathogens, 384-415.
41. Referans41 Terzi, G., Gücükoğlu, A., Çadırcı, Ö., Uyanik, T., Alişarlı, M. (2015). Serotyping and antibiotic susceptibility of Listeria monocytogenes isolated from ready-to-eat foods in Samsun, Turkey. Turk J Vet Anim Sci, 39(2):211-217, doi: 10.3906/vet-1407-15.
42. Referans42 Tong, S.Y., Davis, J.S., Eichenberger, E., Holland, T.L., Fowler, V.G. (2015). Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev, 28(3):603-661, doi: 10.1128/CMR.00134-14.
43. Referans43 Vazquez-Sanchez, D., Lopez-Cabo, M., Saa-Ibusquiza, P., Rodriguez-Herrera, J.J. (2012). Incidence and characterization of Staphylococcus aureus in fishery products marketed in Galicia (Northwest Spain). Int J Food Microbiol, 157(2):286-296, doi, 10.1016/j.ijfoodmicro.2012.05.021
44. Referans44 World Health Organization. 2002. Use of Antimicrobials Outside Human Medicine and Resultant Antimicrobial Resistance in Humans (Fact Sheet No. 268). Geneva, Switzerland: Author.
45. Referans45 Zaheer, Z. (2017). Methicillin-resistant Staphylococcus aureus in poultry-an emerging concern related to future epidemic. Matrix Sci Medica, 1(1):15-18.
46. Referans46 Zarei, M., Maktabi, S., Ghorbanpour, M. (2012). Prevalence of Listeria monocytogenes, Vibrio parahaemolyticus, Staphylococcus aureus, and Salmonella spp. in seafood products using Multiplex Polymerase Chain Reaction. Foodborne Pathog Dis, 9(2):108-112, doi: 10.1089/fpd.2011.0989.