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Isolation of Staphylococcus aureus Strains from White Cheese Samples, Determination of Methicillin and Vancomycin Susceptibility with Macrolide-Lincosamide-Streptogramin B (MLSB) Resistance Phenotypes

Year 2022, Volume: 11 Issue: 1, 66 - 72, 15.05.2022
https://doi.org/10.31196/huvfd.1070069

Abstract

Many pathogenic microorganisms (e.g., Salmonella spp., L. monocytogenes, S. aureus) can be found in traditionally produced cheeses. This situation arises from the lack of raw milk quality standards, insufficient production hygiene, and the consumption of cheese before it is ripe, and it can pose a threat to public health. S. aureus is considered the most common causative agent of food poisoning after Salmonella spp. It is well known that humans and animals are the primary reservoirs for S. aureus contamination of food. This study examined 64 samples of salted white cheese sold unpackaged and open to contamination. Coagulase-positive staphylococci were detected in 24 of the samples tested. The API 20 Staph kit system was applied to 120 isolates by selecting five specific colonies from the positive samples, and 52 of these isolates were identified as S. aureus. We performed antibiogram tests on the recovered S. aureus isolates according to Clinical and Laboratory Standards Institute (CLSI) guidelines. While none of the identified isolates was vancomycin-resistant (VRSA), we found 6 (11.5%) were methicillin-resistant (MRSA), and 46 (88.5%) were methicillin-sensitive (MSSA). While 4 (67%) of the isolated MRSA strains were resistant to erythromycin and 3 (50%) to clindamycin, 17 (37%) of the MSSA strains were resistant to erythromycin, and 7 (15.2%) to clindamycin. With or without methicillin resistance, 21 of all isolates (40.4%) showed resistance to erythromycin. In addition, 10 (19.2%) of all isolates showed both erythromycin and clindamycin resistance and 7 (13.5%) showed inducible clindamycin resistance. As a result, strains of S. aureus resistant to several antibiotics have been found in cured cheese sold unpackaged in neighborhood markets, posing a public health problem. It is necessary to pay attention to the hygiene and sanitary regulations applied to prevent this and to stop uncontrolled and unsupervised sales.

References

  • Aguilar CEG, Rossi Junior OD, Vidal AMC, Ribeiro LF, Rossi GAM, 2016: Microbial quality of industrial and retail market grated parmesan cheese in the State of São Paulo, Brazil. Cienc Rural, 46 (12), 2257-2263.
  • Anonim, 2015: Tebliğ, T.G.K. Türk Gıda Kodeksi Peynir Tebliği (No: 2015/6). Resmi gazete, (29261).
  • Basanisi MG, La Bella G, Nobili G, Franconieri I, La Salandra G, 2017: Genotyping of methicillinresistant Staphylococcus aureus (MRSA) isolated from milk and dairy products in South Italy. Food Microbiol, 62, 141–146.
  • Bannerman TL, (2003). Staphylococcus, Microcccus and other catalase-positive cocci that grow aerobically, In: Murray PR,
  • Baron EJ, Pfaller MA, Jorgenson JH, Yolken RH (Ed), Manual of Clinical Mikrobiology Volume II, 8th, 384-403, Washington, DC.
  • Can HY, Çelik TH, 2012: Detection of enterotoxigenic and antimicrobial resistant S. aureus in Turkish cheeses. Food Control, 24, 100-103.
  • CLSI, 2017: Clinical and laboratory standards institute. "Performance standards for antimicrobial susceptibility testing." CLSI supplement M100.
  • Can HY, 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, 175.
  • Cai H, Kou X, Ji H, Wang X, Wang H, Zhang Y, Shili L, Baokun L, Juan D, Qingling W, Jing Z, Hu D, 2021: Prevalence and characteristics of Staphylococcus aureus isolated from Kazak cheese in Xinjiang, China. Food Control, 123, 107759.
  • Çiçek M, Tuncer Ö, Sancak B, Şener B, 2017: Staphylococcus aureus suşlarında makrolid, linkozamid ve streptogramin b direncinin fenotipik yöntemlerle belirlenmesi ve kinupristin/dalfopristinin in vitro etkinliğinin araştırılması. Turk Mikrobiyol Cemiy Derg, 47 (2), 83-88.
  • Doulgeraki AI, Di Ciccio P, Ianieri A, Nychas GJE, 2016: Methicillin-resistant food-related Staphylococcus aureus: a review of current knowledge and biofilm formation for future studies and applications. Res Microbiol,168 (1), 1-15.
  • Dehkordi FS, Gandomi H, Basti AA, Misaghi A, Rahimi E, 2017: Phenotypic and genotypic characterization of antibiotic resistance of methicillin-resistant Staphylococcus aureus isolated from hospital food. Antimicrob Resist Infect Control, 6 (1), 1-11.
  • Erkmen O, 2010: Gıda mikrobiyolojisi Efil Yayınevi, Ankara, Türkiye.
  • Erol I, 2007: Gıda Hijyeni ve Mikrobiyolojisi. Pozitif matbaacılık, Ankara, Türkiye.
  • FDA Bacteriological Analytical Manual, Chapter 12 Staphylococcus aureus. https://www.fda.gov/food/laboratory-methods-food/bam-chapter-12-staphylococcus-aureus Son erişim tarihi: 10.01.2022.
  • Gücükoğlu A, Onur Kevenk T, Uyanik T, Çadirci Ö, Terzi G, Alişarli M, 2012: Detection of enterotoxigenic Staphylococcus aureus in raw milk and dairy products by multiplex PCR. J Food Sci, 77 (11), 620-623.
  • Hayaloglu AA, Guven M, Fox PF, 2002: Microbiological, biochemical and technological properties of Turkish White cheese ‘Beyaz Peynir’. Int Dairy J, 12, 635-648.
  • Hitchins AD, 1998: in FDA Bacteriological Analytical Manual, G.J. Jackson (Ed.), AOAC Internatıonal, Gaithersburg, MD, 1001–1013.
  • Kamber U, 2005: Geleneksel Anadolu Peynirleri. Miki Matbaacılık San ve Tic Ltd Şti, Ankara.
  • Koneman EW, Allen SD, Janda WD, Schereckenberger PC, Winn WC, Jr,1997: The Gram Positive Cocci: Part I Staphylococci and Related Organisms, In:Color Atlas and Textbook of Diagnostic Microbiology, 5th. ed, 539-576, Philadelphia.
  • Khashei R, Malekzadegan Y, Ebrahim-Saraie HS, Razavi Z, 2018: Phenotypic and genotypic characterization of macrolide, lincosamide and streptogramin B resistance among clinical isolates of staphylococci in southwest of Iran. BMC Res. Notes, 11 (1), 1-6.
  • Kayili E, Sanlibaba P, 2020: Prevalence, characterization and antibiotic resistance of Staphylococcus aureus isolated from traditional cheeses in Turkey. Int J Food Prop, 23 (1), 1441–1451.
  • Li L, Feng W, Zhang Z, Xue H, Zhao X, 2015: Macrolide-lincosamide-streptogramin resistance phenotypes and genotypes of coagulase-positive Staphylococcus aureus and coagulase-negative staphylococcal isolates from bovine mastitis. BMC Vet Res, 11 (1), 1-8.
  • Leclercq R, 2002: Mechanisms of resistance to macrolides and lincosamides: Nature of the resistance elements and their clinical implications. Arch Clin Infect Dis, 34 (4), 482-492.
  • Normanno G, Corrente M, La Salandra G, Dambrosio A, Quaglia NC, Parisi A, Greco G, Bellacicco AL, Virgilio S, Celano GV, 2007: Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animal origin product in Italy Int J Food Microbiol, 117 (2), 219-222.
  • Özel G, Aslan V, Bahar Erdem G, Çağatay M, Şencan İ, Mert A, 2011: Stafilokoklarda metisilin duyarlılığının belirlenmesinde oksasilin, sefoksitin, seftizoksim ve moksalaktam disk difüzyon yöntemlerinin karşılaştırılması. Mikrobiyol Bul, 45 (2), 258-65.
  • Özpınar N, 2011: Erzincan tulum peynirinden izole edilen Staphylococcus aureus izolatlarında antibiyotik direncinin ve biyofilm oluşturma özelliğinin fenotipik ve genotipik olarak belirlenmesi. Yüksek Lisans Tezi, Erciyes Üniversitesi Sağlık Bilimleri Enstitüsü, Kayseri.
  • Papadopoulos P, Papadopoulos T, Angelidis AS, Boukouvala E, Zdragas A, Papa A, Hadjichristodoulou C, Sergelidis D, 2018: Prevalence of Staphylococcus aureus and of methicillin-resistant S. aureus (MRSA) along the production chain of dairy products in north-western Greece. Food Microbiol, 69, 43-50.
  • Rahi A, Kazemeini H, Jafariaskar, S, Seif A, Hosseini S, Dehkordi FS, 2020: Genotypic and phenotypic-based assessment of antibiotic resistance and profile of staphylococcal cassette chromosome mec in the methicillin-resistant staphylococcus aureus recovered from raw milk. Infect Drug Resist, 13, 273-283.
  • Resende JA, Fontes CO, Ferreira‐Machado AB, Nascimento TC, Silva VL, Diniz CG, 2018: Antimicrobial‐resistance genetic markers in potentially pathogenic gram positive cocci ısolated from brazilian soft cheese. J Food Sci, 83 (2), 377-385.
  • Rodríguez-Lázaro D, Alonso-Calleja C, Oniciuc EA, Capita R, Gallego D, González-Machado C, Wagner M, Barbu V, Eiros-
  • Bouza JM, Nicolau AI and Hernández M, 2018: Characterization of biofilms formed by foodborne methicillin-resistant staphylococcus aureus. Front Microbiol, 9, 1-12.
  • Sri Prabakusuma A, Zhu J, Shi Y, Ma Q, Zhao Q, Yang Z, Xu Y, Huang A, 2022: Prevalence and antimicrobial resistance profiling of Staphylococcus aureus isolated from traditional cheese in Yunnan, China. 3 Biotech, 12 (1), 1-15.
  • Spanu V, Scarano C, Cossu F, Pala C, Spanu C, De Santis EP, 2014: Antibiotic resistance traits and molecular subtyping of Staphylococcus aureus isolated from raw sheep milk cheese. J Food Sci, 79 (10), 2066-2071.
  • Tekinşen KK, Özdemir Z, 2006: Prevalence of foodborne pathogens in Turkish Van otlu (Herb) cheese. Food Control, 17, 707-711.
  • Wang Y, Wu CM, Lu LM, Ren GWN, Cao XY, Shen JZ, 2008: Macrolide–lincosamide-resistant phenotypes and genotypes of Staphylococcus aureus isolated from bovine clinical mastitis. Vet Microbiol, 130 (1-2), 118-125.
  • Yücel N, Anıl Y, 2011: Identification and antimicrobial susceptibility of Staphylococcus aureus and coagulase negative staphylococci isolated from raw milk and cheese samples. Turk bull hyg exp biol, 68 (2), 73-78.
  • Ziyade N, Yağmur G, Elgörmüş N, Karayel F, Büyük Y, 2015: Postmortem örneklerden izole edilen Staphylococcus aureus suşlarında metisilin, vankomisin, teikoplanin ve makrolid-linkozamid-streptogramin b (Mlsb) direnci. Ankem Derg, 29 (1), 1-7.

Beyaz Peynir Örneklerinden Staphylococcus aureus Suşlarının İzolasyonu, Makrolid-Linkozamid-Streptogramin B (MLSB) Direnç Fenotipleriyle, Metisilin ve Vankomisin Duyarlılıklarının Belirlenmesi

Year 2022, Volume: 11 Issue: 1, 66 - 72, 15.05.2022
https://doi.org/10.31196/huvfd.1070069

Abstract

Geleneksel olarak halk elinde üretilen peynirlerde çok sayıda patojen mikroorganizma (örn., Salmonella spp., L. monocytogenes, S. aureus) bulunabilmektedir. Bu durum, çiğ süt kalite standardının olmaması, üretim hijyeninin yetersizliği, peynirin olgunlaşmadan tüketime sunulması gibi nedenlerden kaynaklanmakta ve halk sağlığını tehdit eden bir unsur olarak karşımıza çıkabilmektedir. S. aureus, gıda zehirlenmesi vakalarında Salmonella spp.’den sonra en yaygın görülen patojen olarak kabul edilmektedir. S. aureus’un gıdalara kontaminasyonunda en önemli rezervuarı insan ve hayvanların oluşturduğu bilinmektedir. Bu araştırmada analizi yapılmak üzere ambalajsız olarak satılan ve kontaminasyona açık 64 adet salamura beyaz peynir numunesi kullanılmıştır. Analize alınan numunelerden 24’ünde koagulaz pozitif stafilokok tespit edilmiştir. Pozitif numunelerden spesifik 5 koloni seçilerek toplamda 120 izolata API 20 Staph kit sistemi uygulanmış ve bu izolatlardan 52’si S. aureus olarak identifiye edilmiştir. Elde edilen S. aureus izolatlarına Clinical and Laboratory Standards Institute (CLSI) yönergeleri doğrultusunda antibiyogram testleri yapılmıştır. Araştırma sonucunda tanımlanan izolatların hiçbiri vankomisine dirençli (VRSA) değilken, 6’sının (%11.5) metisiline dirençli (MRSA), 46’sının ise (% 88.5) metisiline duyarlı (MSSA) olduğu tespit edilmiştir. İzole edilen MRSA suşlarından 4’ü (%67) eritromisine, 3’ü (%50) klindamisine dirençli iken, MSSA suşlarının 17’si (%37) eritromisine, 7’si (%15,2) klindamisine direnç göstermiştir. Metisilin direnci olsun ya da olmasın tüm izolatların (%40,4) 21’i Eritromisin direnci göstermiştir. Bunların dışında tüm izolatların (%19,2) 10’u hem Eritromisin hem de Klindamisin direnci göstermiş ve (%13,5) 7’sinde indüklenebilir Klindamisin direnci tespit edilmiştir. Sonuç olarak semt pazarlarında ambalajsız olarak satışa sunulan salamura peynirlerde halk sağlığı için problem oluşturan çoklu antibiyotik dirençliliği gösteren S. aureus suşları tespit edilmiştir. Bunu önlemek amacıyla uygulanan hijyen ve sanitasyon kurallarına dikkat edilmesi, kontrolsüz ve denetimsiz satışların önlenmesi gerektiği düşünülmektedir.

References

  • Aguilar CEG, Rossi Junior OD, Vidal AMC, Ribeiro LF, Rossi GAM, 2016: Microbial quality of industrial and retail market grated parmesan cheese in the State of São Paulo, Brazil. Cienc Rural, 46 (12), 2257-2263.
  • Anonim, 2015: Tebliğ, T.G.K. Türk Gıda Kodeksi Peynir Tebliği (No: 2015/6). Resmi gazete, (29261).
  • Basanisi MG, La Bella G, Nobili G, Franconieri I, La Salandra G, 2017: Genotyping of methicillinresistant Staphylococcus aureus (MRSA) isolated from milk and dairy products in South Italy. Food Microbiol, 62, 141–146.
  • Bannerman TL, (2003). Staphylococcus, Microcccus and other catalase-positive cocci that grow aerobically, In: Murray PR,
  • Baron EJ, Pfaller MA, Jorgenson JH, Yolken RH (Ed), Manual of Clinical Mikrobiology Volume II, 8th, 384-403, Washington, DC.
  • Can HY, Çelik TH, 2012: Detection of enterotoxigenic and antimicrobial resistant S. aureus in Turkish cheeses. Food Control, 24, 100-103.
  • CLSI, 2017: Clinical and laboratory standards institute. "Performance standards for antimicrobial susceptibility testing." CLSI supplement M100.
  • Can HY, 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, 175.
  • Cai H, Kou X, Ji H, Wang X, Wang H, Zhang Y, Shili L, Baokun L, Juan D, Qingling W, Jing Z, Hu D, 2021: Prevalence and characteristics of Staphylococcus aureus isolated from Kazak cheese in Xinjiang, China. Food Control, 123, 107759.
  • Çiçek M, Tuncer Ö, Sancak B, Şener B, 2017: Staphylococcus aureus suşlarında makrolid, linkozamid ve streptogramin b direncinin fenotipik yöntemlerle belirlenmesi ve kinupristin/dalfopristinin in vitro etkinliğinin araştırılması. Turk Mikrobiyol Cemiy Derg, 47 (2), 83-88.
  • Doulgeraki AI, Di Ciccio P, Ianieri A, Nychas GJE, 2016: Methicillin-resistant food-related Staphylococcus aureus: a review of current knowledge and biofilm formation for future studies and applications. Res Microbiol,168 (1), 1-15.
  • Dehkordi FS, Gandomi H, Basti AA, Misaghi A, Rahimi E, 2017: Phenotypic and genotypic characterization of antibiotic resistance of methicillin-resistant Staphylococcus aureus isolated from hospital food. Antimicrob Resist Infect Control, 6 (1), 1-11.
  • Erkmen O, 2010: Gıda mikrobiyolojisi Efil Yayınevi, Ankara, Türkiye.
  • Erol I, 2007: Gıda Hijyeni ve Mikrobiyolojisi. Pozitif matbaacılık, Ankara, Türkiye.
  • FDA Bacteriological Analytical Manual, Chapter 12 Staphylococcus aureus. https://www.fda.gov/food/laboratory-methods-food/bam-chapter-12-staphylococcus-aureus Son erişim tarihi: 10.01.2022.
  • Gücükoğlu A, Onur Kevenk T, Uyanik T, Çadirci Ö, Terzi G, Alişarli M, 2012: Detection of enterotoxigenic Staphylococcus aureus in raw milk and dairy products by multiplex PCR. J Food Sci, 77 (11), 620-623.
  • Hayaloglu AA, Guven M, Fox PF, 2002: Microbiological, biochemical and technological properties of Turkish White cheese ‘Beyaz Peynir’. Int Dairy J, 12, 635-648.
  • Hitchins AD, 1998: in FDA Bacteriological Analytical Manual, G.J. Jackson (Ed.), AOAC Internatıonal, Gaithersburg, MD, 1001–1013.
  • Kamber U, 2005: Geleneksel Anadolu Peynirleri. Miki Matbaacılık San ve Tic Ltd Şti, Ankara.
  • Koneman EW, Allen SD, Janda WD, Schereckenberger PC, Winn WC, Jr,1997: The Gram Positive Cocci: Part I Staphylococci and Related Organisms, In:Color Atlas and Textbook of Diagnostic Microbiology, 5th. ed, 539-576, Philadelphia.
  • Khashei R, Malekzadegan Y, Ebrahim-Saraie HS, Razavi Z, 2018: Phenotypic and genotypic characterization of macrolide, lincosamide and streptogramin B resistance among clinical isolates of staphylococci in southwest of Iran. BMC Res. Notes, 11 (1), 1-6.
  • Kayili E, Sanlibaba P, 2020: Prevalence, characterization and antibiotic resistance of Staphylococcus aureus isolated from traditional cheeses in Turkey. Int J Food Prop, 23 (1), 1441–1451.
  • Li L, Feng W, Zhang Z, Xue H, Zhao X, 2015: Macrolide-lincosamide-streptogramin resistance phenotypes and genotypes of coagulase-positive Staphylococcus aureus and coagulase-negative staphylococcal isolates from bovine mastitis. BMC Vet Res, 11 (1), 1-8.
  • Leclercq R, 2002: Mechanisms of resistance to macrolides and lincosamides: Nature of the resistance elements and their clinical implications. Arch Clin Infect Dis, 34 (4), 482-492.
  • Normanno G, Corrente M, La Salandra G, Dambrosio A, Quaglia NC, Parisi A, Greco G, Bellacicco AL, Virgilio S, Celano GV, 2007: Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animal origin product in Italy Int J Food Microbiol, 117 (2), 219-222.
  • Özel G, Aslan V, Bahar Erdem G, Çağatay M, Şencan İ, Mert A, 2011: Stafilokoklarda metisilin duyarlılığının belirlenmesinde oksasilin, sefoksitin, seftizoksim ve moksalaktam disk difüzyon yöntemlerinin karşılaştırılması. Mikrobiyol Bul, 45 (2), 258-65.
  • Özpınar N, 2011: Erzincan tulum peynirinden izole edilen Staphylococcus aureus izolatlarında antibiyotik direncinin ve biyofilm oluşturma özelliğinin fenotipik ve genotipik olarak belirlenmesi. Yüksek Lisans Tezi, Erciyes Üniversitesi Sağlık Bilimleri Enstitüsü, Kayseri.
  • Papadopoulos P, Papadopoulos T, Angelidis AS, Boukouvala E, Zdragas A, Papa A, Hadjichristodoulou C, Sergelidis D, 2018: Prevalence of Staphylococcus aureus and of methicillin-resistant S. aureus (MRSA) along the production chain of dairy products in north-western Greece. Food Microbiol, 69, 43-50.
  • Rahi A, Kazemeini H, Jafariaskar, S, Seif A, Hosseini S, Dehkordi FS, 2020: Genotypic and phenotypic-based assessment of antibiotic resistance and profile of staphylococcal cassette chromosome mec in the methicillin-resistant staphylococcus aureus recovered from raw milk. Infect Drug Resist, 13, 273-283.
  • Resende JA, Fontes CO, Ferreira‐Machado AB, Nascimento TC, Silva VL, Diniz CG, 2018: Antimicrobial‐resistance genetic markers in potentially pathogenic gram positive cocci ısolated from brazilian soft cheese. J Food Sci, 83 (2), 377-385.
  • Rodríguez-Lázaro D, Alonso-Calleja C, Oniciuc EA, Capita R, Gallego D, González-Machado C, Wagner M, Barbu V, Eiros-
  • Bouza JM, Nicolau AI and Hernández M, 2018: Characterization of biofilms formed by foodborne methicillin-resistant staphylococcus aureus. Front Microbiol, 9, 1-12.
  • Sri Prabakusuma A, Zhu J, Shi Y, Ma Q, Zhao Q, Yang Z, Xu Y, Huang A, 2022: Prevalence and antimicrobial resistance profiling of Staphylococcus aureus isolated from traditional cheese in Yunnan, China. 3 Biotech, 12 (1), 1-15.
  • Spanu V, Scarano C, Cossu F, Pala C, Spanu C, De Santis EP, 2014: Antibiotic resistance traits and molecular subtyping of Staphylococcus aureus isolated from raw sheep milk cheese. J Food Sci, 79 (10), 2066-2071.
  • Tekinşen KK, Özdemir Z, 2006: Prevalence of foodborne pathogens in Turkish Van otlu (Herb) cheese. Food Control, 17, 707-711.
  • Wang Y, Wu CM, Lu LM, Ren GWN, Cao XY, Shen JZ, 2008: Macrolide–lincosamide-resistant phenotypes and genotypes of Staphylococcus aureus isolated from bovine clinical mastitis. Vet Microbiol, 130 (1-2), 118-125.
  • Yücel N, Anıl Y, 2011: Identification and antimicrobial susceptibility of Staphylococcus aureus and coagulase negative staphylococci isolated from raw milk and cheese samples. Turk bull hyg exp biol, 68 (2), 73-78.
  • Ziyade N, Yağmur G, Elgörmüş N, Karayel F, Büyük Y, 2015: Postmortem örneklerden izole edilen Staphylococcus aureus suşlarında metisilin, vankomisin, teikoplanin ve makrolid-linkozamid-streptogramin b (Mlsb) direnci. Ankem Derg, 29 (1), 1-7.
There are 38 citations in total.

Details

Primary Language Turkish
Subjects Veterinary Surgery
Journal Section Research
Authors

Alper Güngören 0000-0001-7818-1372

Ayşegül Demircioğlu 0000-0002-5121-2631

Ahmet Murat Saytekin 0000-0001-7486-8054

Early Pub Date May 15, 2022
Publication Date May 15, 2022
Submission Date February 8, 2022
Acceptance Date April 29, 2022
Published in Issue Year 2022 Volume: 11 Issue: 1

Cite

APA 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), 66-72. https://doi.org/10.31196/huvfd.1070069
AMA Güngören A, Demircioğlu A, Saytekin AM. Beyaz Peynir Örneklerinden Staphylococcus aureus Suşlarının İzolasyonu, Makrolid-Linkozamid-Streptogramin B (MLSB) Direnç Fenotipleriyle, Metisilin ve Vankomisin Duyarlılıklarının Belirlenmesi. Harran Univ Vet Fak Derg. May 2022;11(1):66-72. doi:10.31196/huvfd.1070069
Chicago Güngören, Alper, Ayşegül Demircioğlu, and Ahmet Murat Saytekin. “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, no. 1 (May 2022): 66-72. https://doi.org/10.31196/huvfd.1070069.
EndNote Güngören A, Demircioğlu A, Saytekin AM (May 1, 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 66–72.
IEEE A. Güngören, A. Demircioğlu, and A. M. Saytekin, “Beyaz Peynir Örneklerinden Staphylococcus aureus Suşlarının İzolasyonu, Makrolid-Linkozamid-Streptogramin B (MLSB) Direnç Fenotipleriyle, Metisilin ve Vankomisin Duyarlılıklarının Belirlenmesi”, Harran Univ Vet Fak Derg, vol. 11, no. 1, pp. 66–72, 2022, doi: 10.31196/huvfd.1070069.
ISNAD Güngören, Alper et al. “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 (May 2022), 66-72. https://doi.org/10.31196/huvfd.1070069.
JAMA Güngören A, Demircioğlu A, Saytekin AM. Beyaz Peynir Örneklerinden Staphylococcus aureus Suşlarının İzolasyonu, Makrolid-Linkozamid-Streptogramin B (MLSB) Direnç Fenotipleriyle, Metisilin ve Vankomisin Duyarlılıklarının Belirlenmesi. Harran Univ Vet Fak Derg. 2022;11:66–72.
MLA Güngören, Alper et al. “Beyaz Peynir Örneklerinden Staphylococcus Aureus Suşlarının İzolasyonu, Makrolid-Linkozamid-Streptogramin B (MLSB) Direnç Fenotipleriyle, Metisilin Ve Vankomisin Duyarlılıklarının Belirlenmesi”. Harran Üniversitesi Veteriner Fakültesi Dergisi, vol. 11, no. 1, 2022, pp. 66-72, doi:10.31196/huvfd.1070069.
Vancouver Güngören A, Demircioğlu A, Saytekin AM. Beyaz Peynir Örneklerinden Staphylococcus aureus Suşlarının İzolasyonu, Makrolid-Linkozamid-Streptogramin B (MLSB) Direnç Fenotipleriyle, Metisilin ve Vankomisin Duyarlılıklarının Belirlenmesi. Harran Univ Vet Fak Derg. 2022;11(1):66-72.