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İzmir Tulum Peynirinde Koagülaz Pozitif Stafilokokların Yaygınlığı, Antibiyotik Direnci ve Biyofilm Oluşumu

Year 2025, Volume: 9 Issue: 1, 239 - 251, 17.03.2025
https://doi.org/10.31015/2025.1.26

Abstract

Koagülaz-pozitif stafilokoklar (CPS), stafilokokal gıda zehirlenmelerinde başlıca bakteriyel etkenler olup, insanlarda ve hayvanlarda enfeksiyonlara neden olarak önemli bir halk sağlığı riski oluştururlar. Bu çalışmada, İzmir ilindeki çeşitli perakende satış noktalarından toplam 100 İzmir Tulum Peyniri örneği toplanmıştır. Peynir örneklerinden standart kültürel yöntemler kullanılarak CPS izolatları elde edilmiştir. CPS izolatlarının fenotipik antibiyotik dirençleri agar disk difüzyon testi ile, biyofilm oluşturma kapasiteleri ise kolorimetrik yöntemle belirlenmiştir. Çalışmada, analiz edilen 100 İzmir Tulum Peyniri örneğinin 30'unda (%30) CPS izole edilmiş ve bu örneklerin 27’sinde (%27), Türk Gıda Kodeksi Mikrobiyolojik Kriterler Yönetmeliği'nde belirtilen maksimum CPS sınırı olan 10³ CFU/g’nin üzerinde CPS düzeyleri tespit edilmiştir. Antimikrobiyal direnç testi sonucunda, 30 CPS izolatının %90’ının penisiline dirençli olduğu belirlenmiştir; diğer yaygın antibiyotiklere direnç oranları ise %83,3 klindamisin, %56,7 siprofloksasin ve %53,3 tetrasiklin olarak tespit edilmiştir. Ayrıca, izolatların %76,7’sinin çoklu ilaç direncine sahip olduğu, yani farklı antibiyotiklerle kolayca öldürülemediği ve bu durumun tedavi seçeneklerini sınırladığı belirlenmiştir. Bunun yanı sıra, CPS izolatlarının %83,3’ünün biyofilm oluşturma kapasitesine sahip olduğu tespit edilerek, bunun gıda güvenliği üzerindeki olumsuz etkisi vurgulanmıştır. Elde edilen bulgular, süt ürünlerinde biyofilm oluşumuna karşı yenilikçi stratejilerin yanı sıra daha sıkı hijyen protokolleri ve kontrollü antibiyotik kullanımının gerekliliğini ortaya koymaktadır.

References

  • Akyol, N., Gündoğ, D. A., Özkaya, Y., Güngör, C., & Onmaz, N. E. (2023). Kasap Dükkanları ve Şarküterilerde Gıda ile Temas Eden Yüzeylerden Elde Edilen Staphylococcus aureus İzolatlarında Biyofilm Üretiminin Fenotipik ve Genotipik Karakterizasyonu. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, 20(3), 198,205. https://doi.org/10.32707/ercivet.1389025 (in Turkish)
  • André, M. C. D., Campos, M. R. H., Borges, L. J., Kipnis, A., Pimenta, F. C., & Serafini, A. B. (2008). Comparison of Staphylococcus aureus isolates from food handlers, raw bovine milk and Minas Frescal cheese by antibiogram and pulsed, field gel electrophoresis following SmaI digestion. Food Control, 19(2), 200,207. https://doi.org/10.1016/j.foodcont.2007.03.010
  • Angulo, F. J., LeJeune, J. T., & Rajala, Schultz, P. J. (2009). Unpasteurized milk: a continued public health threat. Clinical Infectious Diseases, 48(1), 93,100. https://doi.org/10.1086/595007
  • Anonymous. (2025). Türk Gıda Kodeksi Mikrobiyolojik Kriterler Yönetmeliği. Resmî Gazete, 13 Şubat 2025, Sayı: 32812.https://kms.kaysis.gov.tr/Home/Kurum/24308110 (in Turkish)
  • Arefi, F., Mohsenzadeh, M., & Razmyar, J. (2014). Isolation, antimicrobial susceptibility and mecA gene analysis of methicillin-resistant Staphylococcus aureus. Iranian Journal of Veterinary Research, 15(2), 127-131. https://doi.org/10.22099/ijvr.2014.2351
  • Aslim, B., & Yucel, N. (2008). In vitro antimicrobial activity of essential oil from endemic Origanum minutiflorum on ciprofloxacin, resistant Campylobacter spp. Food chemistry, 107(2), 602,606. https://doi.org/10.1016/j.foodchem.2007.08.048
  • Aydin, A., Muratoglu, K., Sudagidan, M., Bostan, K., Okuklu, B., & Harsa, S. (2011). Prevalence and antibiotic resistance of foodborne Staphylococcus aureus isolates in Turkey. Foodborne pathogens and disease, 8(1), 63,69. https://doi.org/10.1089/fpd.2010.0613
  • Bacanlı, M., & Başaran, N. (2019). Importance of antibiotic residues in animal food. Food and Chemical Toxicology, 125, 462-466.https://doi.org/10.1016/j.fct.2019.01.033
  • Balaban, N., & Rasooly, A. (2000). Staphylococcal enterotoxins. International journal of food microbiology, 61(1), 1,10. https://doi.org/10.1016/S0168,1605(00)00377,9
  • Barton, M. D. (2000). Antibiotic use in animal feed and its impact on human health. Nutrition research reviews, 13(2), 279,299. https://doi.org/10.1079/095442200108729106
  • Borelli, B. M., Ferreira, E. G., Lacerda, I. C., Santos, D. A., Carmo, L. S., Dias, R. S., ... & Rosa, C. A. (2006). Enteroxigenic Staphylococcus spp. and other microbial contaminants during production of Canastra cheese, Brazil. Brazilian Journal of Microbiology, 37, 545,550. https://doi.org/10.1590/S1517,83822006000400026
  • Büyükyörük, S., & Soyutemiz, G. E. (2010). Geleneksel Olarak Üretilmiş İzmir Tulum Peynirinden Lactococcus lactis (Lactococcus lactis alttür lactis ve alttür cremoris) Suşlarının İzolasyonu, Fenotipik ve Moleküler Teknikler ile İdentifikasyonu. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, 7(2), 81,87 (in Turkish)
  • Calahorrano-Moreno, M. B., Ordoñez, Bailon, J. J., Baquerizo, Crespo, R. J., Dueñas,Rivadeneira, A. A., Montenegro, M. C. B., & Rodríguez,Díaz, J. M. (2022). Contaminants in the cow's milk we consume? Pasteurization and other technologies in the elimination of contaminants. F1000Research, 11. doi: 10.5256/f1000research.120201.r121005
  • Can, H. Y., Elmalı, M., & Karagöz, A. (2017). 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, 37(2), 175. doi: 10.5851/kosfa.2017.37.2.175
  • Capurro, A., Aspàn, A., Unnerstad, H. E., Waller, K. P., & Artursson, K. (2010). Identification of potential sources of Staphylococcus aureus in herds with mastitis problems. Journal of dairy science, 93(1), 180,191. https://doi.org/10.3168/jds.2009,2471
  • Castro, R. D., Pedroso, S. H. S. P., Sandes, S. H. C., Silva, G. O., Luiz, K. C. M., Dias, R. S., ... & Souza, M. R. (2020). Virulence factors and antimicrobial resistance of Staphylococcus aureus isolated from the production process of Minas artisanal cheese from the region of Campo das Vertentes, Brazil. Journal of dairy science, 103(3), 2098,2110. https://doi.org/10.3168/jds.2019,17138
  • Cha, J. O., Yoo, J. I., Yoo, J. S., Chung, H. S., Park, S. H., Kim, H. S., ... & Chung, G. T. (2013). Investigation of biofilm formation and its association with the molecular and clinical characteristics of methicillin, resistant Staphylococcus aureus. Osong public health and research perspectives, 4(5), 225,232. https://doi.org/10.1016/j.phrp.2013.09.001
  • Chavant, P., Gaillard, Martinie, B., Talon, R., Hébraud, M., & Bernardi, T. (2007). A new device for rapid evaluation of biofilm formation potential by bacteria. Journal of microbiological methods, 68(3), 605,612. https://doi.org/10.1016/j.mimet.2006.11.010
  • CLSI. (2020). M100 Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute. 30th Ed. Wayne, PA.
  • Coelho, M. C., Malcata, F. X., & Silva, C. C. (2022). Lactic acid bacteria in raw,milk cheeses: From starter cultures to probiotic functions. Foods, 11(15), 2276. https://doi.org/10.3390/foods11152276
  • Cruzado-Bravo, M. L. M., Silva, N. C. C., Rodrigues, M. X., Silva, G. O. E., Porto, E., & Sturion, G. L. (2019). Phenotypic and genotypic characterization of Staphylococcus spp. isolated from mastitis milk and cheese processing: Study of adherence and biofilm formation. Food research international, 122, 450,460. https://doi.org/10.1016/j.foodres.2019.04.017
  • da Silva Abreu, A. C., Matos, L. G., da Silva Cândido, T. J., Barboza, G. R., de Souza, V. V. M. A., Nuñez, K. V. M., & Silva, N. C. C. (2021). Antimicrobial resistance of Staphylococcus spp. isolated from organic and conventional Minas Frescal cheese producers in São Paulo, Brazil. Journal of Dairy Science, 104(4), 4012,4022. https://doi.org/10.3168/jds.2020,19338
  • de Souza Paiva, W., de Souza Neto, F. E., Brasil,Oliveira, L. L., Bandeira, M. G. L., de Souza Paiva, E., & de Lima Batista, A. C. (2021). Staphylococcus aureus: a threat to food safety. Research, Society and Development, 10(14), e372101422186, e372101422186. https://doi.org/10.33448/rsd,v10i14.22186
  • dos Santos Goncalves, M., Delattre, C., Balestrino, D., Charbonnel, N., Elboutachfaiti, R., Wadouachi, A., ... & Forestier, C. (2014). Anti, biofilm activity: a function of Klebsiella pneumoniae capsular polysaccharide. PLoS One, 9(6), e99995. https://doi.org/10.1371/journal.pone.0099995
  • Demirsıkan, S., & Tuncer, Y. (2021). Tulum Peynirinde Staphylococcus aureus Yaygınlığı ve Antibiyotik Direnç Profillerinin ve Direnç Genlerinin Belirlenmesi. Mühendislik Bilimleri ve Tasarım Dergisi, 9(3), 822,832. https://doi.org/10.21923/jesd.918230 (in Turkish)
  • Di Ciccio, P., Vergara, A., Festino, A. R., Paludi, D., Zanardi, E., Ghidini, S., & Ianieri, A. (2015). Biofilm formation by Staphylococcus aureus on food contact surfaces: Relationship with temperature and cell surface hydrophobicity. Food Control, 50, 930,936. https://doi.org/10.1016/j.foodcont.2014.10.048
  • Endres, C. M., Moreira, E., de Freitas, A. B., Castel, A. P. D., Graciano, F., Mann, M. B., ... & Frazzon, J. (2023). Evaluation of Enterotoxins and Antimicrobial Resistance in Microorganisms Isolated from Raw Sheep Milk and Cheese: Ensuring the Microbiological Safety of These Products in Southern Brazil. Microorganisms, 11(6), 1618. https://doi.org/10.3390/microorganisms11061618
  • Enright, M. C. (2003). The evolution of a resistant pathogen–the case of MRSA. Current opinion in pharmacology, 3(5), 474,479. https://doi.org/10.1016/S1471,4892(03)00109,7
  • Esemu, S. N., Njoh, S. T., Ndip, L. M., Keneh, N. K., Kfusi, J. A., & Njukeng, A. P. (2023). Ready‐to‐Eat Foods: A Potential Vehicle for the Spread of Coagulase‐Positive Staphylococci and Antimicrobial‐Resistant Staphylococcus aureus in Buea Municipality, South West Cameroon. Canadian Journal of Infectious Diseases and Medical Microbiology, 2023(1), 9735319. https://doi.org/10.1155/2023/9735319
  • Fernandes, A., Ramos, C., Monteiro, V., Santos, J., & Fernandes, P. (2022). Virulence potential and antibiotic susceptibility of S. aureus strains isolated from food handlers. Microorganisms, 10(11), 2155. https://doi.org/10.3390/microorganisms10112155
  • Ferreira, M. A., Bernardo, L. G., Neves, L. S., Campos, M. R. H., Lamaro,Cardoso, J., & André, M. C. P. (2016). Virulence profile and genetic variability of Staphylococcus aureus isolated from artisanal cheese. Journal of Dairy Science, 99(11), 8589,8597. https://doi.org/10.3168/jds.2015,10732
  • Flemming, H. C., & Wingender, J. (2010). The biofilm matrix. Nature reviews microbiology, 8(9), 623,633. https://doi.org/10.1038/nrmicro2415
  • Gajewska, J., & Chajęcka, Wierzchowska, W. (2020). Biofilm formation ability and presence of adhesion genes among coagulase-negative and coagulase-positive staphylococci isolates from raw cow’s milk. Pathogens, 9(8), 654. https://doi.org/10.3390/pathogens9080654
  • Gökmen, M., Ektik, N., & Çıbık, R. (2017). The prevalence and antibiotic resistance of methicillin, resistant Staphylococcus aureus (MRSA) in milk and dairy products in Balikesir, Turkey. https://doi.org/10.12681/jhvms.16062
  • Götz, F., Bannerman, T., & Schleifer, K. H. (2006). The genera staphylococcus and macrococcus. The prokaryotes, 5. doi: 10.1007/0,387,30744,3_1
  • Grecelle, C. B. Z., Mascitti, A. K., da Silva, L., Lunge, V. R., & da Costa, M. (2020). Characterization of Staphylococcus species isolated in production stages of Brazilian Colonial cheese. Revista de Patologia Tropical/Journal of Tropical Pathology, 49(1), 1,10. https://doi.org/10.5216/rpt.v49i1.60380
  • Gundogan, N., & Ataol, O. (2013). Biofilm, protease and lipase properties and antibiotic resistance profiles of staphylococci isolated from various foods. African Journal of Microbiology Research, 7(28), 3582,3588. doi:10.5897/AJMR2012.2316
  • Gundogan, N., & Avci, E. (2014). Occurrence and antibiotic resistance of E scherichia coli, S taphylococcus aureus and B acillus cereus in raw milk and dairy products in Turkey. International journal of dairy technology, 67(4), 562-569.https://doi.org/10.1111/1471-0307.12149
  • Güngören, A,, Demircioğlu, A., Saytekin, A.M. (2022). Beyaz Peynir Örneklerinden Staphylococcus aureus Suşlarının İzolasyonu, Makrolid-Linkozamid-Streptogramin B (MLSB) Direnç Fenotipleriyle, Metisilin ve Vankomisin Duyarlılıklarının Belirlenmesi. Harran Üniversitesi Veteriner Fakültesi Dergisi, 11(1), 100-106. doi:10.31196/huvfd.1070069.
  • Hayaloglu, A. A., Cakmakci, S., Brechany, E. Y., Deegan, K. C., & McSweeney, P. L. H. (2007). Microbiology, biochemistry, and volatile composition of Tulum cheese ripened in goat's skin or plastic bags. Journal of Dairy Science, 90(3), 1102,1121. https://doi.org/10.3168/jds.S0022,0302(07)71597,7
  • Heilmann, C. (2011). Adhesion mechanisms of staphylococci. Bacterial Adhesion: Chemistry, Biology and Physics, 105,123. https://doi.org/10.1007/978,94,007,0940,9_7
  • Hızlısoy, H., Onmaz, N. E., Karadal, F., Serhat, A. L., Yıldırım, Y., Gonulalan, Z., & Kılıc, H. Antibiotic Resistance Gene Profiles of Staphylococcus Aureus Isolated from Foods of Animal Origin. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 24(2). DOI: 10.9775/kvfd.2017.18772.
  • ISO 6888,1:2003: Microbiology of food and animal feeding stuffs — Horizontal method for the enumeration of coagulase,positive staphylococci — Part 1: Technique using Baird,Parker agar medium. International Organization for Standardization.
  • Kayili, E., & Sanlibaba, P. (2020). Prevalence, characterization and antibiotic resistance of Staphylococcus aureus isolated from traditional cheeses in Turkey. International Journal of Food Properties, 23(1), 1441-1451.https://doi.org/10.1080/10942912.2020.1814323.
  • Kasnowski, M. C., Mantilla, S. P. S., Oliveira, L. A. T., & Franco, R. M. (2010). Formação de biofilme na indústria de alimentos e métodos de validação de superfícies. Revista Científica Eletrônica de Medicina Veterinária, 8(15), 1-23.
  • Kim, S. J., Moon, D. C., Park, S. C., Kang, H. Y., Na, S. H., & Lim, S. K. (2019). Antimicrobial resistance and genetic characterization of coagulase, negative staphylococci from bovine mastitis milk samples in Korea. Journal of dairy science, 102(12), 11439,11448. https://doi.org/10.3168/jds.2019,17028
  • Kizanlik, P. K., & Goksoy, E. O. (2024). The prevalence, enterotoxigenic properties and antimicrobial susceptibility of Staphylococcus aureus isolated from various foods of animal origin. Veterinarski arhiv, 94(1), DOI: 10.24099/vet.arhiv.1987
  • Koca, N. (1996). Çeşitli starter kültür kombinasyonlarının İzmir teneke tulum peynirinin nitelikleri üzerine etkileri (Master's thesis,). https://tez.yok.gov.tr/UlusalTezMerkezi/tezDetay.jsp?id=asHph,04QXvH,q9nAmAXCg&no=asHph,04QXvH,q9nAmAXCg (in Turkish).
  • Kousta, M., Mataragas, M., Skandamis, P., & Drosinos, E. H. (2010). Prevalence and sources of cheese contamination with pathogens at farm and processing levels. Food control, 21(6), 805,815. https://doi.org/10.1016/j.foodcont.2009.11.015
  • Kroning, I. S., Iglesias, M. A., Sehn, C. P., Gandra, T. K. V., Mata, M. M., & da Silva, W. P. (2016). Staphylococcus aureus isolated from handmade sweets: biofilm formation, enterotoxigenicity and antimicrobial resistance. Food microbiology, 58, 105-111.https://doi.org/10.1016/j.fm.2016.04.001.
  • Kupczyński, R., Bednarski, M., Sokołowski, M., Kowalkowski, W., & Pacyga, K. (2024). Comparison of Antibiotic Use and the Frequency of Diseases Depending on the Size of Herd and the Type of Cattle Breeding. Animals, 14(13), 1889. https://doi.org/10.3390/ani14131889
  • Kürekci, C. (2016). Prevalence, antimicrobial resistance, and resistant traits of coagulase, negative staphylococci isolated from cheese samples in Turkey. Journal of dairy science, 99(4), 2675,2679. https://doi.org/10.3168/jds.2015,10725
  • Larkin, E. A., Carman, R. J., Krakauer, T., & Stiles, B. G. (2009). Staphylococcus aureus: the toxic presence of a pathogen extraordinaire. Current medicinal chemistry, 16(30), 4003,4019. https://doi.org/10.2174/092986709789352321
  • Li, R. C., & Tang, M. C. (2004). Post, antibiotic effect induced by an antibiotic combination: influence of mode, sequence and interval of exposure. Journal of Antimicrobial Chemotherapy, 54(5), 904,908. https://doi.org/10.1093/jac/dkh435
  • Mahdavi, S., & Isazadeh, A. R. (2019). Investigation of contamination rate and determination of pattern of antibiotic resistance in coagulase positive staphylococcus aureus isolated from domestic cheeses in Maragheh, Iran. Pathobiology Research, 22(2), 85,89. https://mjms.modares.ac.ir/article,30,18965,en.html
  • Medeiros Filho, M. I. M. (2019). NA, Jordano R, et al. Occurrence of staphylococcus aureus and its toxins in cheeses from the region of Andalusia, Spain. J Dairy Vet Anim Res, 8(1), 33-36.https://doi.org/10.15406/jdvar.2019.08.00239.
  • Morar, A., Ban, Cucerzan, A., Herman, V., Tîrziu, E., Sallam, K. I., Abd, Elghany, S. M., & Imre, K. (2021). Multidrug resistant coagulase- positive Staphylococcus aureus and their enterotoxins detection in traditional cheeses marketed in Banat Region, Romania. Antibiotics, 10(12), 1458. https://doi.org/10.3390/antibiotics10121458
  • Morar, A., Imre, K., Nichita, I., David, C., Stoica, F., & Sala, C. (2013). Staphylococcus spp. isolated from cheese commercialized in marketplace. https://www.cabidigitallibrary.org/doi/full/10.5555/20133335002
  • Neculai-Valeanu, A. S., Ariton, A. M., Radu, C., Porosnicu, I., Sanduleanu, C., & Amariții, G. (2024). From herd health to public health: Digital tools for combating antibiotic resistance in dairy farms. Antibiotics, 13(7), 634. https://doi.org/10.3390/antibiotics13070634
  • Normanno, G., Firinu, A., Virgilio, S., Mula, G., Dambrosio, A., Poggiu, A., ... & Celano, G. V. (2005). Coagulase, positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. International journal of food microbiology, 98(1), 73,79. https://doi.org/10.1016/j.ijfoodmicro.2004.05.008
  • Özpinar, N., & Gümüşsoy, KS. (2013). Phenotypic and genotypic determination of antibiotic resistant and biofilm forming Staphylococcus aureus isolated in Erzincan tulum cheese. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 19(3). DOI: 10.9775/kvfd.2012.8216
  • Pajohesh, R., Tajbakhsh, E., Momtaz, H., & Rahimi, E. (2022). Relationship between biofilm formation and antibiotic resistance and adherence genes in Staphylococcus aureus strains isolated from raw cow milk in Shahrekord, Iran. International Journal of Microbiology, 2022(1), 6435774. https://doi.org/10.1155/2022/6435774
  • Papadopoulos, P., Papadopoulos, T., Angelidis, A. S., Kotzamanidis, C., Zdragas, A., Papa, A., ... & Sergelidis, D. (2019). Prevalence, antimicrobial susceptibility and characterization of Staphylococcus aureus and methicillin,resistant Staphylococcus aureus isolated from dairy industries in north,central and north,eastern Greece. International journal of food microbiology, 291, 35,41. https://doi.org/10.1016/j.ijfoodmicro.2018.11.007
  • Penna, A. L. B., Gigante, M. L., & Todorov, S. D. (2021). Artisanal Brazilian cheeses—history, marketing, technological and microbiological aspects. Foods, 10(7), 1562. https://doi.org/10.3390/foods10071562
  • Pereira, G. d. N., Rosa, R. d. S., Dias, A. é A., Gonçalves, D. J. ún. S., Seribelli, A. A., Pinheiro-Hubinger, L., Eller, L. K. W., de Carvalho, T. B., & Pereira, V. C. (2022). Characterization of the virulence, agr typing and antimicrobial resistance profile of Staphylococcus aureus strains isolated from food handlers in Brazil. Brazilian Journal of Infectious Diseases: An Official Publication of the Brazilian Society of Infectious Diseases, 26(5), 102698. https://doi.org/10.1016/j.bjid.2022.102698.
  • Radoslava, S. R., Nemanja, Z., & Branko, V. (2020). Occurrence and characterization of enterotoxigenic Staphylococci isolated from soft cheeses in Serbia. Acta Veterinaria, 70(2), 238,254. https://doi.org/10.2478/acve,2020,0017
  • Ryan K.J. and Ray C.G. (2004). Sherris Medical Microbiology: An Introduction to Infectious Diseases, 4th Ed. New York: McGraw McGraw‐Hill Publisher
  • Rodrigues, M. X., Silva, N. C. C., Trevilin, J. H., Cruzado, M. M. B., Mui, T. S., Duarte, F. R. S., ... & Porto, E. (2017). Molecular characterization and antibiotic resistance of Staphylococcus spp. isolated from cheese processing plants. Journal of Dairy Science, 100(7), 5167,5175. https://doi.org/10.3168/jds.2016,12477
  • Rola, J. G., Czubkowska, A., Korpysa, Dzirba, W., & Osek, J. (2016). Occurrence of Staphylococcus aureus on farms with small scale production of raw milk cheeses in Poland. Toxins, 8(3), 62. https://doi.org/10.3390/toxins8030062
  • Rosengren, Å., Fabricius, A., Guss, B., Sylvén, S., & Lindqvist, R. (2010). Occurrence of foodborne pathogens and characterization of Staphylococcus aureus in cheese produced on farm,dairies. International journal of food microbiology, 144(2), 263,269. https://doi.org/10.1016/j.ijfoodmicro.2010.10.004
  • Samaržija, D., Damjanović, S., & Pogačić, T. (2007). Staphylococcus aureus u siru. Mljekarstvo: časopis za unaprjeđenje proizvodnje i prerade mlijeka, 57(1), 31,48. https://hrcak.srce.hr/11764
  • Spellberg, B., Guidos, R., Gilbert, D., Bradley, J., Boucher, H. W., Scheld, W. M., ... & Infectious Diseases Society of America. (2008). The epidemic of antibiotic-resistant infections: a call to action for the medical community from the Infectious Diseases Society of America. Clinical infectious diseases, 46(2), 155-164. https://doi.org/10.1086/524891
  • Savage, V. J., Chopra, I., & O'Neill, A. J. (2013). Staphylococcus aureus biofilms promote horizontal transfer of antibiotic resistance. Antimicrobial agents and chemotherapy, 57(4), 1968,1970. https://doi.org/10.1128/aac.02008,12
  • Silva, N. C., Guimaraes, F. F., de P. Manzi, M., Gómez-Sanz, E., Gómez, P., Araújo-Júnior, J. P., ... & Torres, C. (2014). Characterization of methicillin-resistant coagulase-negative staphylococci in milk from cows with mastitis in Brazil. Antonie Van Leeuwenhoek, 106, 227-233.https://doi.org/10.1007/s10482-014-0185-5.
  • Sospedra, I., Marín, R., Mañes, J., & Soriano, J. M. (2012). Rapid whole protein quantification of staphylococcal enterotoxin B by liquid chromatography. Food chemistry, 133(1), 163,166. https://doi.org/10.1016/j.foodchem.2011.12.083
  • Sylejmani, D., Hamidi, A., & Robaj, A. (2015). Occurrence of staphylococcus aureus and Coagulase positive Staph. Aureus in Artisanal cheese in Kosovo. Agriculture and Food, 3(1).
  • Şen, C., Doğan, M. A., & Yuceer, Y. (2023). Teneke Tulum Peynirlerinin Bazı Fizikokimyasal ve Duyusal Özelliklerinin Belirlenmesi. Gıda, 48(6), 1160,1171. https://doi.org/10.15237/gida.GD23048 (in Turkish).
  • Taşçıoğlu. A. (2022). Aydın ilinde çeşitli noktalarda satışa sunulan tulum ve beyaz peynirlerde staphylococcus aureus varlığının ve klasik enterotoksin genlerinin belirlenmesi (Doctoral Thesis) http://adudspace.adu.edu.tr:8080/xmlui/handle/11607/4759 (in Turkish)
  • Tilocca, B., Costanzo, N., Morittu, V. M., Spina, A. A., Soggiu, A., Britti, D., ... & Piras, C. (2020). Milk microbiota: Characterization methods and role in cheese production. Journal of Proteomics, 210, 103534. https://doi.org/10.1016/j.jprot.2019.103534
  • Tiseo, K., Huber, L., Gilbert, M., Robinson, T. P., & Van Boeckel, T. P. (2020). Global trends in antimicrobial use in food animals from 2017 to 2030. Antibiotics, 9(12), 918.https://doi.org/10.3390/antibiotics9120918.
  • Uddin, T. M., Chakraborty, A. J., Khusro, A., Zidan, B. R. M., Mitra, S., Emran, T. B., ... & Koirala, N. (2021). Antibiotic resistance in microbes: History, mechanisms, therapeutic strategies and future prospects. Journal of infection and public health, 14(12), 1750-1766.https://doi.org/10.1016/j.jiph.2021.10.020
  • Unal Turhan, E. (2019). The presence of pathogenic bacteria in traditional cheese sold in local market in Hatay province, Turkey. Applied Ecology and Environmental Research, 17(3), 7135,45. http://dx.doi.org/10.15666/aeer/1703_71357145
  • Vanderhaeghen, W., Cerpentier, T., Adriaensen, C., Vicca, J., Hermans, K., & Butaye, P. (2010). Methicillin, resistant Staphylococcus aureus (MRSA) ST398 associated with clinical and subclinical mastitis in Belgian cows. Veterinary microbiology, 144(1,2), 166,171. https://doi.org/10.1016/j.vetmic.2009.12.044
  • Williams, A. G., & Withers, S. E. (2010). Microbiological characterisation of artisanal farmhouse cheeses manufactured in Scotland. International journal of dairy technology, 63(3), 356,369. https://doi.org/10.1111/j.1471,0307.2010.00596.x
  • Yang, L., Liu, Y., Wu, H., Song, Z., Høiby, N., Molin, S., & Givskov, M. (2012). Combating biofilms. FEMS Immunology & Medical Microbiology, 65(2), 146-157.https://doi.org/10.1111/j.1574-695X.2011.00858.x
  • Yao, H., Liu, J., Jiang, X., Chen, F., Lu, X., & Zhang, J. (2021). Analysis of the clinical effect of combined drug susceptibility to guide medication for carbapenem-resistant klebsiella pneumoniae patients based on the kirby–bauer disk diffusion method. Infection and drug resistance, 79-87. https://doi.org/10.2147/IDR.S282386
  • Yerlikaya, O., & Akbulut, N. (2019). Potential use of probiotic Enterococcus faecium and Enterococcus durans strains in Izmir Tulum Cheese as adjunct culture. Journal of Food Science and Technology, 56, 2175,2185. https://doi.org/10.1007/s13197,019,03699,5
  • Yıldırım, T., Sırıken, B., & Yavuz, C. (2016). Çiğ süt ve peynirlerde koagulaz pozitif stafilokoklar. Veteriner Hekimler Derneği Dergisi, 87(2), 3-12 (in Turkish)
  • Yılmaz, Ö. (2020). Laktik Asit Bakterileri ve Hücresiz Süpernatantlarının Yara Enfeksiyonlarına Yol Açan Önemli Patojenlere Karşı Potansiyel Probiyotik Etkilerinin Araştırılması. (Doktora Tezi, Aydın Adnan Menderes Üniversitesi Sağlık Bilimleri Enstitüsü). http://adudspace.adu.edu.tr:8080/xmlui/handle/11607/3884 (in Turkish).
  • Yücel, N., & Anıl, Y. (2011). Çiğ süt ve peynir örneklerinden Staphylococcus aureus ve koagülaz negatif stafilokokların identifikasyonu ve antibiyotik duyarlılığı. Türk Hijyen ve Deneysel Biyoloji Dergisi, 68(2), 73,78. DOI ID: 10.5505/TurkHijyen.2011.58070. (in Turkish).

Prevalence, antibiotic resistance, and biofilm formation of coagulase-positive staphylococci in Izmir Tulum Cheese

Year 2025, Volume: 9 Issue: 1, 239 - 251, 17.03.2025
https://doi.org/10.31015/2025.1.26

Abstract

Coagulase-positive staphylococci (CPS) are the main causative bacterial agents of staphylococcal food intoxication, posing a significant public health risk and causing infections in humans and animals. In this study, a hundred Izmir Tulum Cheese samples were collected from various retail outlets in the Izmir province. CPS isolates from cheese samples were identified using standard cultural methods. The phenotypic antibiotic resistance of CPS isolates was determined using the agar disk diffusion test method, while their biofilm formation capacity was assessed using the colorimetric method. In the study, CPS was isolated from 30 out of 100 analyzed Izmir Tulum Cheese samples (30%), and it was determined that 27 of these samples (27%) had CPS levels exceeding the maximum acceptable limit of 10³ CFU/g set by the Turkish Food Codex Microbiological Criteria Regulation. Antimicrobial resistance analysis revealed that among the 30 CPS isolates, 90% were resistant to penicillin, while resistance rates to other commonly used antibiotics were 83.3% for clindamycin, 56.7% for ciprofloxacin, and 53.3% for tetracycline. Additionally, 76.7% of the isolates were multidrug-resistant, meaning they were not easily killed by different antibiotics, which limits treatment options. Furthermore, 83.3% of the CPS isolates had the capacity for biofilm formation, highlighting its impact on food safety. These findings emphasize the need for stricter hygiene protocols, controlled antibiotic use, and innovative strategies to combat biofilms in dairy production.

References

  • Akyol, N., Gündoğ, D. A., Özkaya, Y., Güngör, C., & Onmaz, N. E. (2023). Kasap Dükkanları ve Şarküterilerde Gıda ile Temas Eden Yüzeylerden Elde Edilen Staphylococcus aureus İzolatlarında Biyofilm Üretiminin Fenotipik ve Genotipik Karakterizasyonu. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, 20(3), 198,205. https://doi.org/10.32707/ercivet.1389025 (in Turkish)
  • André, M. C. D., Campos, M. R. H., Borges, L. J., Kipnis, A., Pimenta, F. C., & Serafini, A. B. (2008). Comparison of Staphylococcus aureus isolates from food handlers, raw bovine milk and Minas Frescal cheese by antibiogram and pulsed, field gel electrophoresis following SmaI digestion. Food Control, 19(2), 200,207. https://doi.org/10.1016/j.foodcont.2007.03.010
  • Angulo, F. J., LeJeune, J. T., & Rajala, Schultz, P. J. (2009). Unpasteurized milk: a continued public health threat. Clinical Infectious Diseases, 48(1), 93,100. https://doi.org/10.1086/595007
  • Anonymous. (2025). Türk Gıda Kodeksi Mikrobiyolojik Kriterler Yönetmeliği. Resmî Gazete, 13 Şubat 2025, Sayı: 32812.https://kms.kaysis.gov.tr/Home/Kurum/24308110 (in Turkish)
  • Arefi, F., Mohsenzadeh, M., & Razmyar, J. (2014). Isolation, antimicrobial susceptibility and mecA gene analysis of methicillin-resistant Staphylococcus aureus. Iranian Journal of Veterinary Research, 15(2), 127-131. https://doi.org/10.22099/ijvr.2014.2351
  • Aslim, B., & Yucel, N. (2008). In vitro antimicrobial activity of essential oil from endemic Origanum minutiflorum on ciprofloxacin, resistant Campylobacter spp. Food chemistry, 107(2), 602,606. https://doi.org/10.1016/j.foodchem.2007.08.048
  • Aydin, A., Muratoglu, K., Sudagidan, M., Bostan, K., Okuklu, B., & Harsa, S. (2011). Prevalence and antibiotic resistance of foodborne Staphylococcus aureus isolates in Turkey. Foodborne pathogens and disease, 8(1), 63,69. https://doi.org/10.1089/fpd.2010.0613
  • Bacanlı, M., & Başaran, N. (2019). Importance of antibiotic residues in animal food. Food and Chemical Toxicology, 125, 462-466.https://doi.org/10.1016/j.fct.2019.01.033
  • Balaban, N., & Rasooly, A. (2000). Staphylococcal enterotoxins. International journal of food microbiology, 61(1), 1,10. https://doi.org/10.1016/S0168,1605(00)00377,9
  • Barton, M. D. (2000). Antibiotic use in animal feed and its impact on human health. Nutrition research reviews, 13(2), 279,299. https://doi.org/10.1079/095442200108729106
  • Borelli, B. M., Ferreira, E. G., Lacerda, I. C., Santos, D. A., Carmo, L. S., Dias, R. S., ... & Rosa, C. A. (2006). Enteroxigenic Staphylococcus spp. and other microbial contaminants during production of Canastra cheese, Brazil. Brazilian Journal of Microbiology, 37, 545,550. https://doi.org/10.1590/S1517,83822006000400026
  • Büyükyörük, S., & Soyutemiz, G. E. (2010). Geleneksel Olarak Üretilmiş İzmir Tulum Peynirinden Lactococcus lactis (Lactococcus lactis alttür lactis ve alttür cremoris) Suşlarının İzolasyonu, Fenotipik ve Moleküler Teknikler ile İdentifikasyonu. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, 7(2), 81,87 (in Turkish)
  • Calahorrano-Moreno, M. B., Ordoñez, Bailon, J. J., Baquerizo, Crespo, R. J., Dueñas,Rivadeneira, A. A., Montenegro, M. C. B., & Rodríguez,Díaz, J. M. (2022). Contaminants in the cow's milk we consume? Pasteurization and other technologies in the elimination of contaminants. F1000Research, 11. doi: 10.5256/f1000research.120201.r121005
  • Can, H. Y., Elmalı, M., & Karagöz, A. (2017). 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, 37(2), 175. doi: 10.5851/kosfa.2017.37.2.175
  • Capurro, A., Aspàn, A., Unnerstad, H. E., Waller, K. P., & Artursson, K. (2010). Identification of potential sources of Staphylococcus aureus in herds with mastitis problems. Journal of dairy science, 93(1), 180,191. https://doi.org/10.3168/jds.2009,2471
  • Castro, R. D., Pedroso, S. H. S. P., Sandes, S. H. C., Silva, G. O., Luiz, K. C. M., Dias, R. S., ... & Souza, M. R. (2020). Virulence factors and antimicrobial resistance of Staphylococcus aureus isolated from the production process of Minas artisanal cheese from the region of Campo das Vertentes, Brazil. Journal of dairy science, 103(3), 2098,2110. https://doi.org/10.3168/jds.2019,17138
  • Cha, J. O., Yoo, J. I., Yoo, J. S., Chung, H. S., Park, S. H., Kim, H. S., ... & Chung, G. T. (2013). Investigation of biofilm formation and its association with the molecular and clinical characteristics of methicillin, resistant Staphylococcus aureus. Osong public health and research perspectives, 4(5), 225,232. https://doi.org/10.1016/j.phrp.2013.09.001
  • Chavant, P., Gaillard, Martinie, B., Talon, R., Hébraud, M., & Bernardi, T. (2007). A new device for rapid evaluation of biofilm formation potential by bacteria. Journal of microbiological methods, 68(3), 605,612. https://doi.org/10.1016/j.mimet.2006.11.010
  • CLSI. (2020). M100 Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute. 30th Ed. Wayne, PA.
  • Coelho, M. C., Malcata, F. X., & Silva, C. C. (2022). Lactic acid bacteria in raw,milk cheeses: From starter cultures to probiotic functions. Foods, 11(15), 2276. https://doi.org/10.3390/foods11152276
  • Cruzado-Bravo, M. L. M., Silva, N. C. C., Rodrigues, M. X., Silva, G. O. E., Porto, E., & Sturion, G. L. (2019). Phenotypic and genotypic characterization of Staphylococcus spp. isolated from mastitis milk and cheese processing: Study of adherence and biofilm formation. Food research international, 122, 450,460. https://doi.org/10.1016/j.foodres.2019.04.017
  • da Silva Abreu, A. C., Matos, L. G., da Silva Cândido, T. J., Barboza, G. R., de Souza, V. V. M. A., Nuñez, K. V. M., & Silva, N. C. C. (2021). Antimicrobial resistance of Staphylococcus spp. isolated from organic and conventional Minas Frescal cheese producers in São Paulo, Brazil. Journal of Dairy Science, 104(4), 4012,4022. https://doi.org/10.3168/jds.2020,19338
  • de Souza Paiva, W., de Souza Neto, F. E., Brasil,Oliveira, L. L., Bandeira, M. G. L., de Souza Paiva, E., & de Lima Batista, A. C. (2021). Staphylococcus aureus: a threat to food safety. Research, Society and Development, 10(14), e372101422186, e372101422186. https://doi.org/10.33448/rsd,v10i14.22186
  • dos Santos Goncalves, M., Delattre, C., Balestrino, D., Charbonnel, N., Elboutachfaiti, R., Wadouachi, A., ... & Forestier, C. (2014). Anti, biofilm activity: a function of Klebsiella pneumoniae capsular polysaccharide. PLoS One, 9(6), e99995. https://doi.org/10.1371/journal.pone.0099995
  • Demirsıkan, S., & Tuncer, Y. (2021). Tulum Peynirinde Staphylococcus aureus Yaygınlığı ve Antibiyotik Direnç Profillerinin ve Direnç Genlerinin Belirlenmesi. Mühendislik Bilimleri ve Tasarım Dergisi, 9(3), 822,832. https://doi.org/10.21923/jesd.918230 (in Turkish)
  • Di Ciccio, P., Vergara, A., Festino, A. R., Paludi, D., Zanardi, E., Ghidini, S., & Ianieri, A. (2015). Biofilm formation by Staphylococcus aureus on food contact surfaces: Relationship with temperature and cell surface hydrophobicity. Food Control, 50, 930,936. https://doi.org/10.1016/j.foodcont.2014.10.048
  • Endres, C. M., Moreira, E., de Freitas, A. B., Castel, A. P. D., Graciano, F., Mann, M. B., ... & Frazzon, J. (2023). Evaluation of Enterotoxins and Antimicrobial Resistance in Microorganisms Isolated from Raw Sheep Milk and Cheese: Ensuring the Microbiological Safety of These Products in Southern Brazil. Microorganisms, 11(6), 1618. https://doi.org/10.3390/microorganisms11061618
  • Enright, M. C. (2003). The evolution of a resistant pathogen–the case of MRSA. Current opinion in pharmacology, 3(5), 474,479. https://doi.org/10.1016/S1471,4892(03)00109,7
  • Esemu, S. N., Njoh, S. T., Ndip, L. M., Keneh, N. K., Kfusi, J. A., & Njukeng, A. P. (2023). Ready‐to‐Eat Foods: A Potential Vehicle for the Spread of Coagulase‐Positive Staphylococci and Antimicrobial‐Resistant Staphylococcus aureus in Buea Municipality, South West Cameroon. Canadian Journal of Infectious Diseases and Medical Microbiology, 2023(1), 9735319. https://doi.org/10.1155/2023/9735319
  • Fernandes, A., Ramos, C., Monteiro, V., Santos, J., & Fernandes, P. (2022). Virulence potential and antibiotic susceptibility of S. aureus strains isolated from food handlers. Microorganisms, 10(11), 2155. https://doi.org/10.3390/microorganisms10112155
  • Ferreira, M. A., Bernardo, L. G., Neves, L. S., Campos, M. R. H., Lamaro,Cardoso, J., & André, M. C. P. (2016). Virulence profile and genetic variability of Staphylococcus aureus isolated from artisanal cheese. Journal of Dairy Science, 99(11), 8589,8597. https://doi.org/10.3168/jds.2015,10732
  • Flemming, H. C., & Wingender, J. (2010). The biofilm matrix. Nature reviews microbiology, 8(9), 623,633. https://doi.org/10.1038/nrmicro2415
  • Gajewska, J., & Chajęcka, Wierzchowska, W. (2020). Biofilm formation ability and presence of adhesion genes among coagulase-negative and coagulase-positive staphylococci isolates from raw cow’s milk. Pathogens, 9(8), 654. https://doi.org/10.3390/pathogens9080654
  • Gökmen, M., Ektik, N., & Çıbık, R. (2017). The prevalence and antibiotic resistance of methicillin, resistant Staphylococcus aureus (MRSA) in milk and dairy products in Balikesir, Turkey. https://doi.org/10.12681/jhvms.16062
  • Götz, F., Bannerman, T., & Schleifer, K. H. (2006). The genera staphylococcus and macrococcus. The prokaryotes, 5. doi: 10.1007/0,387,30744,3_1
  • Grecelle, C. B. Z., Mascitti, A. K., da Silva, L., Lunge, V. R., & da Costa, M. (2020). Characterization of Staphylococcus species isolated in production stages of Brazilian Colonial cheese. Revista de Patologia Tropical/Journal of Tropical Pathology, 49(1), 1,10. https://doi.org/10.5216/rpt.v49i1.60380
  • Gundogan, N., & Ataol, O. (2013). Biofilm, protease and lipase properties and antibiotic resistance profiles of staphylococci isolated from various foods. African Journal of Microbiology Research, 7(28), 3582,3588. doi:10.5897/AJMR2012.2316
  • Gundogan, N., & Avci, E. (2014). Occurrence and antibiotic resistance of E scherichia coli, S taphylococcus aureus and B acillus cereus in raw milk and dairy products in Turkey. International journal of dairy technology, 67(4), 562-569.https://doi.org/10.1111/1471-0307.12149
  • Güngören, A,, Demircioğlu, A., Saytekin, A.M. (2022). Beyaz Peynir Örneklerinden Staphylococcus aureus Suşlarının İzolasyonu, Makrolid-Linkozamid-Streptogramin B (MLSB) Direnç Fenotipleriyle, Metisilin ve Vankomisin Duyarlılıklarının Belirlenmesi. Harran Üniversitesi Veteriner Fakültesi Dergisi, 11(1), 100-106. doi:10.31196/huvfd.1070069.
  • Hayaloglu, A. A., Cakmakci, S., Brechany, E. Y., Deegan, K. C., & McSweeney, P. L. H. (2007). Microbiology, biochemistry, and volatile composition of Tulum cheese ripened in goat's skin or plastic bags. Journal of Dairy Science, 90(3), 1102,1121. https://doi.org/10.3168/jds.S0022,0302(07)71597,7
  • Heilmann, C. (2011). Adhesion mechanisms of staphylococci. Bacterial Adhesion: Chemistry, Biology and Physics, 105,123. https://doi.org/10.1007/978,94,007,0940,9_7
  • Hızlısoy, H., Onmaz, N. E., Karadal, F., Serhat, A. L., Yıldırım, Y., Gonulalan, Z., & Kılıc, H. Antibiotic Resistance Gene Profiles of Staphylococcus Aureus Isolated from Foods of Animal Origin. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 24(2). DOI: 10.9775/kvfd.2017.18772.
  • ISO 6888,1:2003: Microbiology of food and animal feeding stuffs — Horizontal method for the enumeration of coagulase,positive staphylococci — Part 1: Technique using Baird,Parker agar medium. International Organization for Standardization.
  • Kayili, E., & Sanlibaba, P. (2020). Prevalence, characterization and antibiotic resistance of Staphylococcus aureus isolated from traditional cheeses in Turkey. International Journal of Food Properties, 23(1), 1441-1451.https://doi.org/10.1080/10942912.2020.1814323.
  • Kasnowski, M. C., Mantilla, S. P. S., Oliveira, L. A. T., & Franco, R. M. (2010). Formação de biofilme na indústria de alimentos e métodos de validação de superfícies. Revista Científica Eletrônica de Medicina Veterinária, 8(15), 1-23.
  • Kim, S. J., Moon, D. C., Park, S. C., Kang, H. Y., Na, S. H., & Lim, S. K. (2019). Antimicrobial resistance and genetic characterization of coagulase, negative staphylococci from bovine mastitis milk samples in Korea. Journal of dairy science, 102(12), 11439,11448. https://doi.org/10.3168/jds.2019,17028
  • Kizanlik, P. K., & Goksoy, E. O. (2024). The prevalence, enterotoxigenic properties and antimicrobial susceptibility of Staphylococcus aureus isolated from various foods of animal origin. Veterinarski arhiv, 94(1), DOI: 10.24099/vet.arhiv.1987
  • Koca, N. (1996). Çeşitli starter kültür kombinasyonlarının İzmir teneke tulum peynirinin nitelikleri üzerine etkileri (Master's thesis,). https://tez.yok.gov.tr/UlusalTezMerkezi/tezDetay.jsp?id=asHph,04QXvH,q9nAmAXCg&no=asHph,04QXvH,q9nAmAXCg (in Turkish).
  • Kousta, M., Mataragas, M., Skandamis, P., & Drosinos, E. H. (2010). Prevalence and sources of cheese contamination with pathogens at farm and processing levels. Food control, 21(6), 805,815. https://doi.org/10.1016/j.foodcont.2009.11.015
  • Kroning, I. S., Iglesias, M. A., Sehn, C. P., Gandra, T. K. V., Mata, M. M., & da Silva, W. P. (2016). Staphylococcus aureus isolated from handmade sweets: biofilm formation, enterotoxigenicity and antimicrobial resistance. Food microbiology, 58, 105-111.https://doi.org/10.1016/j.fm.2016.04.001.
  • Kupczyński, R., Bednarski, M., Sokołowski, M., Kowalkowski, W., & Pacyga, K. (2024). Comparison of Antibiotic Use and the Frequency of Diseases Depending on the Size of Herd and the Type of Cattle Breeding. Animals, 14(13), 1889. https://doi.org/10.3390/ani14131889
  • Kürekci, C. (2016). Prevalence, antimicrobial resistance, and resistant traits of coagulase, negative staphylococci isolated from cheese samples in Turkey. Journal of dairy science, 99(4), 2675,2679. https://doi.org/10.3168/jds.2015,10725
  • Larkin, E. A., Carman, R. J., Krakauer, T., & Stiles, B. G. (2009). Staphylococcus aureus: the toxic presence of a pathogen extraordinaire. Current medicinal chemistry, 16(30), 4003,4019. https://doi.org/10.2174/092986709789352321
  • Li, R. C., & Tang, M. C. (2004). Post, antibiotic effect induced by an antibiotic combination: influence of mode, sequence and interval of exposure. Journal of Antimicrobial Chemotherapy, 54(5), 904,908. https://doi.org/10.1093/jac/dkh435
  • Mahdavi, S., & Isazadeh, A. R. (2019). Investigation of contamination rate and determination of pattern of antibiotic resistance in coagulase positive staphylococcus aureus isolated from domestic cheeses in Maragheh, Iran. Pathobiology Research, 22(2), 85,89. https://mjms.modares.ac.ir/article,30,18965,en.html
  • Medeiros Filho, M. I. M. (2019). NA, Jordano R, et al. Occurrence of staphylococcus aureus and its toxins in cheeses from the region of Andalusia, Spain. J Dairy Vet Anim Res, 8(1), 33-36.https://doi.org/10.15406/jdvar.2019.08.00239.
  • Morar, A., Ban, Cucerzan, A., Herman, V., Tîrziu, E., Sallam, K. I., Abd, Elghany, S. M., & Imre, K. (2021). Multidrug resistant coagulase- positive Staphylococcus aureus and their enterotoxins detection in traditional cheeses marketed in Banat Region, Romania. Antibiotics, 10(12), 1458. https://doi.org/10.3390/antibiotics10121458
  • Morar, A., Imre, K., Nichita, I., David, C., Stoica, F., & Sala, C. (2013). Staphylococcus spp. isolated from cheese commercialized in marketplace. https://www.cabidigitallibrary.org/doi/full/10.5555/20133335002
  • Neculai-Valeanu, A. S., Ariton, A. M., Radu, C., Porosnicu, I., Sanduleanu, C., & Amariții, G. (2024). From herd health to public health: Digital tools for combating antibiotic resistance in dairy farms. Antibiotics, 13(7), 634. https://doi.org/10.3390/antibiotics13070634
  • Normanno, G., Firinu, A., Virgilio, S., Mula, G., Dambrosio, A., Poggiu, A., ... & Celano, G. V. (2005). Coagulase, positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. International journal of food microbiology, 98(1), 73,79. https://doi.org/10.1016/j.ijfoodmicro.2004.05.008
  • Özpinar, N., & Gümüşsoy, KS. (2013). Phenotypic and genotypic determination of antibiotic resistant and biofilm forming Staphylococcus aureus isolated in Erzincan tulum cheese. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 19(3). DOI: 10.9775/kvfd.2012.8216
  • Pajohesh, R., Tajbakhsh, E., Momtaz, H., & Rahimi, E. (2022). Relationship between biofilm formation and antibiotic resistance and adherence genes in Staphylococcus aureus strains isolated from raw cow milk in Shahrekord, Iran. International Journal of Microbiology, 2022(1), 6435774. https://doi.org/10.1155/2022/6435774
  • Papadopoulos, P., Papadopoulos, T., Angelidis, A. S., Kotzamanidis, C., Zdragas, A., Papa, A., ... & Sergelidis, D. (2019). Prevalence, antimicrobial susceptibility and characterization of Staphylococcus aureus and methicillin,resistant Staphylococcus aureus isolated from dairy industries in north,central and north,eastern Greece. International journal of food microbiology, 291, 35,41. https://doi.org/10.1016/j.ijfoodmicro.2018.11.007
  • Penna, A. L. B., Gigante, M. L., & Todorov, S. D. (2021). Artisanal Brazilian cheeses—history, marketing, technological and microbiological aspects. Foods, 10(7), 1562. https://doi.org/10.3390/foods10071562
  • Pereira, G. d. N., Rosa, R. d. S., Dias, A. é A., Gonçalves, D. J. ún. S., Seribelli, A. A., Pinheiro-Hubinger, L., Eller, L. K. W., de Carvalho, T. B., & Pereira, V. C. (2022). Characterization of the virulence, agr typing and antimicrobial resistance profile of Staphylococcus aureus strains isolated from food handlers in Brazil. Brazilian Journal of Infectious Diseases: An Official Publication of the Brazilian Society of Infectious Diseases, 26(5), 102698. https://doi.org/10.1016/j.bjid.2022.102698.
  • Radoslava, S. R., Nemanja, Z., & Branko, V. (2020). Occurrence and characterization of enterotoxigenic Staphylococci isolated from soft cheeses in Serbia. Acta Veterinaria, 70(2), 238,254. https://doi.org/10.2478/acve,2020,0017
  • Ryan K.J. and Ray C.G. (2004). Sherris Medical Microbiology: An Introduction to Infectious Diseases, 4th Ed. New York: McGraw McGraw‐Hill Publisher
  • Rodrigues, M. X., Silva, N. C. C., Trevilin, J. H., Cruzado, M. M. B., Mui, T. S., Duarte, F. R. S., ... & Porto, E. (2017). Molecular characterization and antibiotic resistance of Staphylococcus spp. isolated from cheese processing plants. Journal of Dairy Science, 100(7), 5167,5175. https://doi.org/10.3168/jds.2016,12477
  • Rola, J. G., Czubkowska, A., Korpysa, Dzirba, W., & Osek, J. (2016). Occurrence of Staphylococcus aureus on farms with small scale production of raw milk cheeses in Poland. Toxins, 8(3), 62. https://doi.org/10.3390/toxins8030062
  • Rosengren, Å., Fabricius, A., Guss, B., Sylvén, S., & Lindqvist, R. (2010). Occurrence of foodborne pathogens and characterization of Staphylococcus aureus in cheese produced on farm,dairies. International journal of food microbiology, 144(2), 263,269. https://doi.org/10.1016/j.ijfoodmicro.2010.10.004
  • Samaržija, D., Damjanović, S., & Pogačić, T. (2007). Staphylococcus aureus u siru. Mljekarstvo: časopis za unaprjeđenje proizvodnje i prerade mlijeka, 57(1), 31,48. https://hrcak.srce.hr/11764
  • Spellberg, B., Guidos, R., Gilbert, D., Bradley, J., Boucher, H. W., Scheld, W. M., ... & Infectious Diseases Society of America. (2008). The epidemic of antibiotic-resistant infections: a call to action for the medical community from the Infectious Diseases Society of America. Clinical infectious diseases, 46(2), 155-164. https://doi.org/10.1086/524891
  • Savage, V. J., Chopra, I., & O'Neill, A. J. (2013). Staphylococcus aureus biofilms promote horizontal transfer of antibiotic resistance. Antimicrobial agents and chemotherapy, 57(4), 1968,1970. https://doi.org/10.1128/aac.02008,12
  • Silva, N. C., Guimaraes, F. F., de P. Manzi, M., Gómez-Sanz, E., Gómez, P., Araújo-Júnior, J. P., ... & Torres, C. (2014). Characterization of methicillin-resistant coagulase-negative staphylococci in milk from cows with mastitis in Brazil. Antonie Van Leeuwenhoek, 106, 227-233.https://doi.org/10.1007/s10482-014-0185-5.
  • Sospedra, I., Marín, R., Mañes, J., & Soriano, J. M. (2012). Rapid whole protein quantification of staphylococcal enterotoxin B by liquid chromatography. Food chemistry, 133(1), 163,166. https://doi.org/10.1016/j.foodchem.2011.12.083
  • Sylejmani, D., Hamidi, A., & Robaj, A. (2015). Occurrence of staphylococcus aureus and Coagulase positive Staph. Aureus in Artisanal cheese in Kosovo. Agriculture and Food, 3(1).
  • Şen, C., Doğan, M. A., & Yuceer, Y. (2023). Teneke Tulum Peynirlerinin Bazı Fizikokimyasal ve Duyusal Özelliklerinin Belirlenmesi. Gıda, 48(6), 1160,1171. https://doi.org/10.15237/gida.GD23048 (in Turkish).
  • Taşçıoğlu. A. (2022). Aydın ilinde çeşitli noktalarda satışa sunulan tulum ve beyaz peynirlerde staphylococcus aureus varlığının ve klasik enterotoksin genlerinin belirlenmesi (Doctoral Thesis) http://adudspace.adu.edu.tr:8080/xmlui/handle/11607/4759 (in Turkish)
  • Tilocca, B., Costanzo, N., Morittu, V. M., Spina, A. A., Soggiu, A., Britti, D., ... & Piras, C. (2020). Milk microbiota: Characterization methods and role in cheese production. Journal of Proteomics, 210, 103534. https://doi.org/10.1016/j.jprot.2019.103534
  • Tiseo, K., Huber, L., Gilbert, M., Robinson, T. P., & Van Boeckel, T. P. (2020). Global trends in antimicrobial use in food animals from 2017 to 2030. Antibiotics, 9(12), 918.https://doi.org/10.3390/antibiotics9120918.
  • Uddin, T. M., Chakraborty, A. J., Khusro, A., Zidan, B. R. M., Mitra, S., Emran, T. B., ... & Koirala, N. (2021). Antibiotic resistance in microbes: History, mechanisms, therapeutic strategies and future prospects. Journal of infection and public health, 14(12), 1750-1766.https://doi.org/10.1016/j.jiph.2021.10.020
  • Unal Turhan, E. (2019). The presence of pathogenic bacteria in traditional cheese sold in local market in Hatay province, Turkey. Applied Ecology and Environmental Research, 17(3), 7135,45. http://dx.doi.org/10.15666/aeer/1703_71357145
  • Vanderhaeghen, W., Cerpentier, T., Adriaensen, C., Vicca, J., Hermans, K., & Butaye, P. (2010). Methicillin, resistant Staphylococcus aureus (MRSA) ST398 associated with clinical and subclinical mastitis in Belgian cows. Veterinary microbiology, 144(1,2), 166,171. https://doi.org/10.1016/j.vetmic.2009.12.044
  • Williams, A. G., & Withers, S. E. (2010). Microbiological characterisation of artisanal farmhouse cheeses manufactured in Scotland. International journal of dairy technology, 63(3), 356,369. https://doi.org/10.1111/j.1471,0307.2010.00596.x
  • Yang, L., Liu, Y., Wu, H., Song, Z., Høiby, N., Molin, S., & Givskov, M. (2012). Combating biofilms. FEMS Immunology & Medical Microbiology, 65(2), 146-157.https://doi.org/10.1111/j.1574-695X.2011.00858.x
  • Yao, H., Liu, J., Jiang, X., Chen, F., Lu, X., & Zhang, J. (2021). Analysis of the clinical effect of combined drug susceptibility to guide medication for carbapenem-resistant klebsiella pneumoniae patients based on the kirby–bauer disk diffusion method. Infection and drug resistance, 79-87. https://doi.org/10.2147/IDR.S282386
  • Yerlikaya, O., & Akbulut, N. (2019). Potential use of probiotic Enterococcus faecium and Enterococcus durans strains in Izmir Tulum Cheese as adjunct culture. Journal of Food Science and Technology, 56, 2175,2185. https://doi.org/10.1007/s13197,019,03699,5
  • Yıldırım, T., Sırıken, B., & Yavuz, C. (2016). Çiğ süt ve peynirlerde koagulaz pozitif stafilokoklar. Veteriner Hekimler Derneği Dergisi, 87(2), 3-12 (in Turkish)
  • Yılmaz, Ö. (2020). Laktik Asit Bakterileri ve Hücresiz Süpernatantlarının Yara Enfeksiyonlarına Yol Açan Önemli Patojenlere Karşı Potansiyel Probiyotik Etkilerinin Araştırılması. (Doktora Tezi, Aydın Adnan Menderes Üniversitesi Sağlık Bilimleri Enstitüsü). http://adudspace.adu.edu.tr:8080/xmlui/handle/11607/3884 (in Turkish).
  • Yücel, N., & Anıl, Y. (2011). Çiğ süt ve peynir örneklerinden Staphylococcus aureus ve koagülaz negatif stafilokokların identifikasyonu ve antibiyotik duyarlılığı. Türk Hijyen ve Deneysel Biyoloji Dergisi, 68(2), 73,78. DOI ID: 10.5505/TurkHijyen.2011.58070. (in Turkish).
There are 90 citations in total.

Details

Primary Language English
Subjects Food Microbiology, Veterinary Food Hygiene and Technology
Journal Section Research Articles
Authors

Başak Gökçe Çöl 0000-0002-7627-9867

Semiha Yalçın 0000-0002-9344-0472

Burcu Çakmak Sancar 0000-0002-0737-7009

Meryem Akhan 0000-0001-8065-8635

Kübra Sağlam 0000-0002-3564-7934

Seydi Yıkmış 0000-0001-8694-0658

Publication Date March 17, 2025
Submission Date December 7, 2024
Acceptance Date March 14, 2025
Published in Issue Year 2025 Volume: 9 Issue: 1

Cite

APA Çöl, B. G., Yalçın, S., Çakmak Sancar, B., Akhan, M., et al. (2025). Prevalence, antibiotic resistance, and biofilm formation of coagulase-positive staphylococci in Izmir Tulum Cheese. International Journal of Agriculture Environment and Food Sciences, 9(1), 239-251. https://doi.org/10.31015/2025.1.26


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