Alper BARAN, Ahmet ERDOĞAN, Tamer TURGUT, Mehmet ADIGÜZEL

Peynirde Staphylococcus aureus varlığının incelenmesi üzerine bir derleme

Stafilokokal Enterotoksin’lere ait bugüne kadar 24 farklı antijenik serotip tanımlanmıştır fakat stafilokokal gıda zehirlenmelerinin % 95’inden klasik enterotoksinler (A, B, C, D ve E) sorumlu tutulmaktadır. Staphlyococcus aureus (S. aureus), gıdada bulunan toksinlerinin alınımını takiben 2-4 saat sonra abdominal kramplar, bulantı, kusma ve diyare gibi zehirlenme semptomlarına neden olan ubiquiter özelliğe sahip bir mikroorganizmadır. Peynir, yüksek seviyedeki besinsel içeriğinden ötürü S. aureus’un gelişimi için uygun bir substrattır. S. aureus’un peynirde ortaya çıkışının sebebi olarak yüksek miktarda S. aureus içeren mastitisli sütlerin pastörize edilmeden peynire işlenmesi, kullanılan starter kültür aktivitesinin yetersiz olması, sütün pastörizasyon sonrası kontaminasyonu ile ürünün işlenmesi ve depolanması sırasındaki uygun olmayan şartlar düşünülmektedir. Birçok peynir türünün üretimi ve olgunlaşması sırasında S. aureus’un gelişimi ve bazı vakalarda enterotoksin üretimi, sanitasyon öneminden dolayı bazı araştırmacılar tarafından incelenmiştir. Bu çalışmada S. aureus’un genel karakteristikleri, peynirdeki varlığı, epidemiyolojisi ve koruma-mücadele yöntemleri derlenmiştir.

Anahtar Kelimeler:

Peynir, Staphylococcus aureus, enterotoksin

A review on the presence of Staphylococcus aureus in cheese

Up to now, 24 different antigenic serotypes of Staphylococcal enterotoxins have been described, but classical enterotoxins (A, B, C, D and E) are responsible for 95% of staphylococcal food poisonings. Staphlyococcus aureus (S. aureus) is an ubiquitous microorganism that cause symptoms of poisoning such as abdominal cramps, nausea, vomiting and diarrhea after 2-4 hours following ingestion of toxins present in food. Cheese is a suitable substrate for the development of S. aureus due to its high nutritional content. The reason for the emergence of S. aureus in cheese are the inability to pasteurize the milk of animals exposed to mastitis infection with high amounts of S. aureus, the inadequate starter culture activity, the post-pasteurisation contamination and the unfavorable conditions for product processing and storage. During the production and maturation of many cheese species, the development of S. aureus and the production of enterotoxin in some cases have been investigated by some researchers for its importance of sanitation. In this study, the general characteristics of S. aureus, the presence in cheese, epidemiology and protection-fighting methods have been compiled.

Keywords:

Cheese, Staphylococcus aureus, enterotoxin,

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[1] Mäkinen O.E., Wanhalinna V., Zannini E., Arendt E.K., Foods for special dietary needs: Non-dairy plant-based milk substitutes and fermented dairy-type products, Crit Rev Food Sci Nutr, 56 (3), 339-349, 2016.
[2] Fox P.F., Guinee T.P., Cogan T.M., McSweeney P.L., Overview of cheese manufacture, Fundamentals of cheese science, Springer, 11-25, 2017.
[3] Szabolcs E., Evaluating the benefits and risks of organic raw milk cheese. Challenges in the production of organic cheeses mad from raw milk. Department of Food Science (Master Thesis), Denmark, 2014.
[4] Fox P.F., Guinee T.P., Cogan T.M., McSweeney P.L., Microbiology of cheese ripening, Fundamentals of Cheese Science, Springer, USA, 333-390, 2017.
[5] Arqués J.L., Rodríguez E., Langa S., Landete J.M., Medina M., Antimicrobial activity of lactic acid bacteria in dairy products and gut: effect on pathogens, BioMed Res Int, 2015, 1-9, 2015.
[6] Landgraf M., Destro M.T., Foodborne Infections and Intoxications: Chapter 28. Staphylococcal Food Poisoning, Elsevier Inc. Chapters, USA, 2013.
[7] Tong S.Y., Davis J.S., Eichenberger E., Holland T.L., Fowler V.G., Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management, Clin Microbiol Rev, 28 (3), 603-661, 2015.
[8] Carfora V., Caprioli A., Marri N., Sagrafoli D., Boselli C., Giacinti G., Giangolini G., Sorbara L., Dottarelli S., Battisti A., Enterotoxin genes, enterotoxin production, and methicillin resistance in Staphylococcus aureus isolated from milk and dairy products in Central Italy, Int Dairy J, 42, 12-15, 2015.
[9] da Silva S.d.S.P., Cidral T.A., Soares M.J.d.S., de Melo M.C.N., Enterotoxin-encoding genes in Staphylococcus spp. from food handlers in a university restaurant, Foodborne Pathog Dis, 12 (11), 921-925, 2015.
[10] Johler S., Tichaczek-Dischinger P.S., Rau J., Sihto H.-M., Lehner A., Adam M., Stephan R., Outbreak of Staphylococcal food poisoning due to SEA-producing Staphylococcus aureus, Foodborne Pathog Dis, 10 (9), 777-781, 2013.
[11] Paulin S., Horn B., Hudson J.A., Factors influencing staphylococcal enterotoxin production in dairy products, Ministry for primary industries, 2012.
[12] Masoud W., Vogensen F.K., Lillevang S., Al-Soud W.A., Sørensen S.J., Jakobsen M., The fate of indigenous microbiota, starter cultures, Escherichia coli, Listeria innocua and Staphylococcus aureus in Danish raw milk and cheeses determined by pyrosequencing and quantitative real time (qRT)-PCR, Int J Food Microbiol, 153 (1), 192-202, 2012.
[13] TFC, Türk Gıda Kodeksi Mikrobiyolojik Kriterler Tebliği, Resmi Gazete, Ankara, 2011.
[14] Shupi R.A., Effect of Exposure Time, Cell Concentration and Culture Age on the Microbial Adhesion of Staphylococcus Aureus and Saccharomyces Cerevisiae on the Glass Surface, Universiti Malaysia Pahang Faculty of Chemical Engineering & Natural Resources (Master Thesis), Malaysia, 2014.
[15] Halsey C.R., Lei S., Wax J.K., Lehman M.K., Nuxoll A.S., Steinke L., Sadykov M., Powers R., Fey P.D., Amino Acid Catabolism in Staphylococcus aureus and the Function of Carbon Catabolite Repression, mBio, 8 (1), e01434-01416, 2017.
[16] Doyle M.P., Buchanan R.L., Food microbiology: fundamentals and frontiers, American Society for Microbiology Press, USA, 2012.
[17] Podkowik M., Park J., Seo K., Bystroń J., Bania J., Enterotoxigenic potential of coagulase-negative staphylococci, Int J Food Microbiol, 163 (1), 34-40, 2013.
[18] Becker K., Heilmann C., Peters G., Coagulase-negative staphylococci, Clin Microbiol Rev, 27 (4), 870-926, 2014.
[19] Tong S.Y.C., Schaumburg F., Ellington M.J., Corander J., Pichon B., Leendertz F., Bentley S.D., Parkhill J., Holt D.C., Peters G., Giffard P.M., Novel staphylococcal species that form part of a Staphylococcus aureus-related complex: the non-pigmented Staphylococcus argenteus sp. nov. and the non-human primate-associated Staphylococcus schweitzeri sp. nov, Int J Syst Evol Microbiol, 65 (Pt 1), 15-22, 2015.
[20] Kadariya J., Smith T.C., Thapaliya D., Staphylococcus aureus and Staphylococcal Food-Borne Disease: An Ongoing Challenge in Public Health, BioMed Res Int, 2014:827965 827-965, 2014.
[21] Part A., A Risk Profile of Dairy Products in Australia, 2006.
[22] Küçükçetin A. M.S., Food Poisonings by Cheese Contaminated with Staphylococcus aureus, The Food, 33 (3), 129-135, 2008.
[23] Ünlütürk A., Üçüncü M., Turantaş F., Öztürk G.F., Survival of Salmonella typhimurium and Staphylococcus aureus in Turkish white cheese., Chem. Mikrobiol. Technol. Lebensm., 16 (1-2), 3-7, 1994.
[24] Selçuk N., Beyaz Peynir Üretiminde Starter Kültür İlavesinin, Değişik Salamura Konsantrasyonlarının ve Olgunlaşma Sürelerinin Staphylococcus aureus’un Çoğalmasına Etkisi. Fen Bilimleri Enstitüsü, Gıda Mühendisliği Anabilim Dalı (Yüksek Lisans Tezi), Erzurum, 1991.
[25] Çolaklar M., Lactobacillus plantarumun Beyaz Peynirlerde Staphylococcus aureus Gelişimi Üzerine Etkisi. Fen Bilimleri Enstitüsü, Gıda Mühendisliği Anabilim Dalı (Yüksek Lisans Tezi), Ankara, 2012.
[26] Yücebay M., Pediococcus pentosaceus ve Lactobacillus brevisin Beyaz Peynirlerde Staphylococcus aureus Gelişimi Üzerine Etkisi. Fen Bilimleri Enstitüsü, Gıda Mühendisliği Anabilim Dalı (Yüksek Lisans tezi), Ankara, 2012.
[27] Tunç K., Hoş A., Investigation of Survival of Staphylococcus aureus During Maturing of White Cheese, Turkish Journal of Science & Technology, 7 (1), 55-60, 2012.
[28] Muehlhoff E., Bennett A., McMahon D., Milk and dairy products in human nutrition, Food and Agriculture Organization of the United Nations (FAO), 2013.
[29] Baran A., Erdoğan A., Atasever M., Effects of storage temperatures on survival and enterotoxin production of Staphylococcus aureus in Turkish white pickled cheese, Malaysian Journal of Microbiology, In press 2017.
[30] Akkaya L., Sancak Y.C., Growth abilities and enterotoxin production of Staphylococcus aureus strains in herby cheese, Bull Vet Inst Pulawy, 51 (3), 401, 2007.
[31] Masatcıoğlu T.M., Avşar Y.K., Effects of flavorings, storage conditions, and storage time on survival of Staphylococcus aureus in Sürk cheese, Journal of food protection, 68 (7), 1487-1491, 2005.
[32] Ozer B.H., Uraz G., Beyzi‐Yilmaz E., Ferit Atasoy A., The effects of brine concentration and scalding on survival of some pathogens in urfa cheese: a traditional white‐brined turkish cheese, Int J Food Sci Technol, 39 (7), 727-735, 2004.
[33] Vernozy-rozand C., Meyrand A., Mazuy C., Delignette-muller M.-L., Jaubert G., Perrin G., Lapeyre C., Richard Y., Behaviour and enterotoxin production by Staphylococcus aureus during the manufacture and ripening of raw goats' milk lactic cheeses, J Dairy Res, 65 (2), 273-281, 1998.
[34] Tuckey S., Stiles M., Ordal Z.J., Witter L., Relation of Cheese-Making Operations to Survival and Growth of Staphylococcus aureus in Different Varieties of Cheese, J Dairy Sci, 47 (6), 604-611, 1964.
[35] Gaya P., Medina M., Bautista L., Nuñez M., Influence of lactic starter inoculation, curd heating and ripening temperature on Staphylococcus aureus behaviour in Manchego cheese, Int J Food Microbiol, 6 (3), 249-257, 1988.
[36] Meyrand A., Boutrand‐Loei S., Ray‐Gueniot S., Mazuy C., Gaspard C., Jaubert G., Perrin G., Lapeyre C., Vernozy‐Rozand C., Growth and enterotoxin production of Staphylococcus aureus during the manufacture and ripening of Camembert‐type cheeses from raw goats’ milk, J Appl Microbiol, 85 (3), 537-544, 1998.
[37] Hasalliu R., Beli E., Terpollari J., The influence of storage temperature of cheese on the incidence of Staphylococcus aureus in some markets in Albania, Res J Agric & Biol Sci, 41 (2), 270-273, 2009.
[38] Ahmed A.a., Moustafa M.K., Marth E.H., Growth and survival of Staphylococcus aureus in Egyptian Domiati cheese, J Food Prot, 46 (5), 412-415, 1983.
[39] Hamama A., El Hankouri N., El Ayadi M., Fate of enterotoxigenic Staphylococcus aureus in the presence of nisin-producing Lactococcus lactis strain during manufacture of Jben, a Moroccan traditional fresh cheese, Int Dairy J, 12 (11), 933-938, 2002.
[40] Santos E.c.d., Genigeorgis C., Survival and growth of Staphylococcus aureus in commercially manufactured Brazilian Minas cheese, J Food Prot, 44 (3), 177-184, 1981.
[41] Delbes C., Alomar J., Chougui N., Martin J.-F., Montel M.-C., Staphylococcus aureus growth and enterotoxin production during the manufacture of uncooked, semihard cheese from cows' raw milk, J Food Prot, 69 (9), 2161-2167, 2006.
[42] Spanu V., Spanu C., Virdis S., Cossu F., Scarano C., De Santis E.P.L., Virulence factors and genetic variability of Staphylococcus aureus strains isolated from raw sheep's milk cheese, International J Food Microbiol, 153 (1), 53-57, 2012.
[43] Nunes R.S.C., de Souza C.P., Pereira K.S., Del Aguila E.M., Paschoalin V.M.F., Identification and molecular phylogeny of coagulase-negative staphylococci isolates from Minas Frescal cheese in southeastern Brazil: Superantigenic toxin production and antibiotic resistance, J Dairy Sci, 99 (4), 2641-2653, 2016.
[44] Fox P.F., Guinee T.P., Cogan T.M., McSweeney P.L., Bacteriology of cheese milk, Fundamentals of Cheese Science, Springer, USA, 105-120, 2017.
[45] Bergdoll M.S., Staphylococcal intoxications, Foodborne infections and intoxications, 2, 443-494, 1979.
[46] Simeão do Carmo L., Dias R.S., Linardi V.R., José de Sena M., Aparecida dos Santos D., Eduardo de Faria M., Pena E.C., Jett M., Heneine L.G., Food poisoning due to enterotoxigenic strains of Staphylococcus present in Minas cheese and raw milk in Brazil, Food Microbiology, 19 (1), 9-14, 2002.
[47] Ostyn A., De Buyser M., Guillier F., Groult J., Felix B., Salah S., Delmas G., Hennekinne J., First evidence of a food poisoning outbreak due to staphylococcal enterotoxin type E, France, 2009, Euro Surveill, 15 (13), 1-4, 2010.
[48] Le Loir Y., Baron F., Gautier M., Staphylococcus aureus and food poisoning, Genet Mol Res, 2 (1), 63-76, 2003.
[49] Yücel N., Anıl Y., Identification and Antimicrobial Susceptibility of Staphylococcus aureus and Coagulase Negative Staphylococci Isolated from Raw Milk and Cheese Samples, Turk Hij Den Biyol Derg, 68 (2), 73-78, 2011.
[50] Gökmen M., Gürbüz Ü., Torlak E., İnal M., Identification of Staphylococcus spp. isolated in different production stages of white cheese and detection of enterotoxin, Kocatepe Veterinary Journal, 6 (2), 7-11, 2013.
[51] Sancak Y., Alisarli M., Akkaya L., Otlu peynirlerde enterotoksijenik Staphylococcus aureus suşlari ve enterotoksin varlıgi uzerine bir arastirma, YYU Saglik Bil. Derg, 9 (1), 218-225, 2006.
[52] Bhatia A., Zahoor S., Staphylococcus aureus enterotoxins: a review, J Clin Diag Res, 3 (1), 188-197, 2007.
[53] Kadariya J., Smith T.C., Thapaliya D., Staphylococcus aureus and Staphylococcal Food-Borne Disease: An Ongoing Challenge in Public Health, BioMed Research International, 2014:827965, 827-865, 2014.
[54] Labbé R.G., García S., Guide to foodborne pathogens, John Wiley & Sons, USA, 2013.