TY  - JOUR
T1  - Isolation and identification of Staphylococcus aureus obtained from cheese samples
AU  - Bozcal, Elif
PY  - 2020
DA  - July
DO  - 10.3153/FH20016
JF  - Food and Health
JO  - Food Health
PB  - Özkan ÖZDEN
WT  - DergiPark
SN  - 2602-2834
SP  - 151
EP  - 159
VL  - 6
IS  - 3
LA  - en
AB  - Milk and dairy products including cheese are one of the most significant food commodities in terms of the food industry. However, a contaminated food product could conduce a variety of food borne bacterial infections. Although Staphylococcus aureus is known as normal flora members of the humans, it`s often isolated from the community and hospital-acquired infections. Therefore, investigation of Staphylococcus aureus from cheese samples was aimed in this study. A total of nineteen (n=19) white cheese was collected from various outdoor markets in Istanbul. All cheese samples were evaluated quantitatively. Phenotypic identification tests including Gram staining, oxidase, catalase, mannitol, and DNase were performed. The presumptive Staphylococcus aureus colonies (n=47) were analyzed by the 16S rRNA PCR and sequencing. And the sequences were deposited into the National Center for Biotechnology Information. According to the nucleotide BLAST analysis, a total of 47 Staphylococaceae and Enterococcaceae members including Staphylococcus aureus (n=3), Staphylococcus carnosus (n=1), Macrococcus caseolyticus (n=1), Enterococcus faecalis (n=25), Enterococcus faecium (n=12), Enterococcus durans (n=4), and Enterococcus gallinarum (n=1) were identified. Regarding methicillin susceptibility testing, two of out of three Staphylococcus aureus were detected as methicillin-resistant.
KW  - Staphylococcus aureus
KW  - 16S rRNA
KW  - PCR
KW  - Cheese
CR  - Abdeen, E.E., Hussein, H., Hussan, Z., Abdella., W. (2016). Genotyping and virulence genes of Enterococcus faecalis Isolated from Kareish cheese and minced meat in Egypt. Research Journal of Microbiology, 11, 133-138.  https://doi.org/10.3923/jm.2016.133.138
CR  - Aguilar, C.E.G.A., Junior, O.D.R., Vidal, A.M.C.V., Ribeiro, L.F, Rossi, G.A.M. (2016). Microbial quality of industrial and retail market grated parmesan cheese in the State of São Paulo, Brazil. Food Technology, 46(12), 2257-2263. https://doi.org/10.1590/0103-8478cr20160334
CR  - Amaral, M.F.A., Silva, L.F., Casarotti, S.N., Nascimento, L.C.S., Penna, A.L.B. (2017). Enterococcus faecium and Enterococcus durans isolated from cheese: Survival in the presence of medications under simulated gastrointestinal conditions and adhesion properties. Journal of Dairy Science, 100(2), 933-949. https://doi.org/10.3168/jds.2016-11513
CR  - Anderson, A.C, Jonas, D., Huber, I., Karygianni, L.,Wölber, J., Hellwig, E., Arweiler, N., Vach, K., Wittmer, A., Al-Ahmad, A. (2016). Enterococcus faecalis from food, clinical specimens, and oral sites: prevalence of virulence factors in association with biofilm formation. Frontiers in Microbiology, 6, 1534. https://doi.org/10.3389/fmicb.2015.01534
CR  - Ataseven, Y.A. (2017). Durum ve tahmin. Süt ve süt ürünleri. Tarımsal Ekonomi ve Politika Geliştirme Enstitüsü, 305, ISBN: 978-605-2207-17-8.
CR  - Baran, A., Erdogan, A., Turgut, T., Adıgüzel, M. (2017). A review on the presence of Staphylococcus aureus in cheese. Turkish Journal of Nature and Science, (6)2, 100-105.
CR  - Bingöl, K.K, Toğay, S.Ö. (2017). Enterotoxin production potential and methicillin resistance of Staphylococcus aureus strains isolated from Urfa Cheeses. Akademik Gıda, 15(1), 29-35. https://doi.org/10.24323/akademik-gida.305772
CR  - Brown, D.F.J, Edwards, D.I, Hawkey, P.M., Morrison, D., Ridgway, G.L., Towner, K.J. (2008). Guidelines for the laboratory diagnosis and susceptibility testing of methicillin-resistant Staphylococcus aureus (MRSA). Journal Antimicrobial Chemotherapy, 56, 1000-1018.  https://doi.org/10.1093/jac/dki372
CR  - Brown, D.F.J, Yates, V.S. (1986). Methicillin susceptibility testing of Staphylococcus aureus on media containing five percent sodium chloride. European Journal of Clinical Microbiology, 5(6), 726-728. https://doi.org/10.1007/BF02013313
CR  - Bückle, A., Kranz, M., Schmidt, H., Weiss, A. (2017). Genetic diversity and population structure of food-borne Staphylococcus carnosus strains. Systematic and Applied Microbiology, 40, 34-41. https://doi.org/10.1016/j.syapm.2016.11.005
CR  - Coton, E., Desmonts, M. H., Leroy, S., Coton, M., Jamet, E., Christieans, S., Donnio, P.Y., Lebert, I., Talon, R. (2010). Biodiversity of coagulase-negative staphylococci in French cheeses, dry fermented sausages, processing environments and clinical samples. International Journal of Food Microbiology 137, 221–229. https://doi.org/10.1016/j.ijfoodmicro.2009.11.023
CR  - Cuny, C., Wieler, L.H., Witte, W. (2015). Livestock-Associated MRSA: The Impact on Humans. Antibiotics, 4, 521-543. https://doi.org/10.3390/antibiotics4040521
CR  - Donnely, C.W. (1990). Concerns of microbial pathogens in association with dairy foods. Journal of Dairy Science, 73, 1656-1661. https://doi.org/10.3168/jds.S0022-0302(90)78838-8
CR  - Ektik, N., Gökmen, M., Çibik, R. (2017). The prevalence and antibiotic resistance of methicillin-resistant Staphylococcus aureus (MRSA) in milk and dairy products in Balikesir, Turkey. Journal of the Hellenic Veterinary Medical Society, 68(4), 613-620. https://doi.org/10.12681/jhvms.16062
CR  - Food and Drug Administration Compliance Program Guidance Manual https://www.fda.gov/media/74723/download  (Accessed at 03.05.2019).
CR  - Food Safety Authority of Ireland. (2011). Staphylococcus aureus. Microbial Fact Sheet Series, 1, 1-5.
CR  - Frank, J.A, Reich, C.I, Sharma, S., Weisbaum, J.S, Wilson, B.A, Olsen, G.J. (2008). Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Applied and Environmental Microbiology, 74, 2461-2470. https://doi.org/10.1128/AEM.02272-07
CR  - Frankenberg, L., Brugna, M., Hederstedt, L. (2002). Enterococcus faecalis Heme-dependent catalase. Journal of Bacteriology, 184, 6351-6356. https://doi.org/10.1128/JB.184.22.6351-6356.2002
CR  - Gökmen, N., Gürbüz, Ü., Torlak, E., İnal, M. (2013). Identification of Staphylococcus spp. isolated in different production stages of white cheese and detection of enterotoxin. Kocatepe Veterinary Journal, 6(2), 7-11. https://doi.org/10.5578/kvj.6145
CR  - Göncüoğlu, M., Ormancı, F.S.B., Doğru, A.K. (2009). Beyaz peynir üretiminde Enterococcus faecium’un starter kültür olarak kullanılması, Ankara Üniversitesi Veteriner Fakültesi Dergisi, 56, 249-254. https://doi.org/10.1501/Vetfak_0000002290
CR  - Hanchi, H., Mottawea, W., Sebei, K., Hammami, R. (2018). The Genus Enterococcus: Between probiotic potential and safety concerns-An Update. Frontiers in Microbiology, 9, 1791. https://doi.org/10.3389/fmicb.2018.01791
CR  - Harrison, E.M., Weinert, L.A., Holden, M.T.G., Welch, J.J, Wilson, K, Morgan F.J.E., Harris S.R., Loeffler, A., Boag, A.K., Peacock, S.J., Paterson, G.K, Waller, A.S., Parkhill, J., Holmes, M.A. (2014). A shared population of epidemic methicillin-resistant Staphylococcus aureus 15 circulates in humans and companion animals. Molecular Biology, 5(3), 00985-13. https://doi.org/10.1128/mBio.00985-13
CR  - Hennekinne, J.A., De Buyser, M.L., Dragacci, S. (2012). Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiology Reviews 36, 815-836.
https://doi.org/10.1111/j.1574-6976.2011.00311.x
CR  - Herrera, F.C., Garcia-Lopez, M., Santos, J.A. (2016). Short communication: Characterization of methicillin-resistant Staphylococcus aureus isolated from raw milk fresh cheese in Colombia, Journal of Dairy Science, 99 (10), 7872-7876. https://doi.org/10.3168/jds.2016-11322
CR  - https://www.statista.com/outlook/40010400/113/cheese/turkey (Accessed at 13.02.2020).
CR  - Kadiroğlu, P., Korel, F., Ceylan, C. (2014). Quantification of Staphylococcus aureus in white cheese by the improved DNA extraction strategy combined with TaqMan and LNA probe-based qPCR. Journal of Microbiological Methods, 105, 92-97. https://doi.org/10.1016/j.mimet.2014.06.022
CR  - Kateete,D.P.,  Kimanil, C.N., Fred A Katabazi, F.A., Okeng, A., Okee, M.S.,Nanteza, A., Moses Joloba, M.L., Najjuka, F.C. (2010). Identification of Staphylococcus aureus: dNaseand mannitol salt agar improve the efficiency of the tube coagulase test. Annals of Clinical Microbiology and Antimicrobials, 9(23), 1-7. https://doi.org/10.1186/1476-0711-9-23
CR  - Kümmel, J., Stessl, B., Gonano, M., Walcher,G., Bereuter,O., Fricker, M., Grunert, T., Wagner, M., Ehling-Schulz, M.(2016).Staphylococcus aureus entrance into the dairy chain: tracking S.aureus from Dairy Cow to Cheese. Frontiers in Microbiology, 7, 1603. https://doi.org/10.3389/fmicb.2016.01603
CR  - Mazhar, S., Hill, C., McAuliffe, O. (2018). A rapid PCR-based method to discriminate Macrococcus caseolyticus and Macrococcus canis from closely-related Staphylococcus species based on the ctaC gene sequence. Journal of Microbiological Methods, 152, 36-38. https://doi.org/10.1016/j.mimet.2018.07.008
CR  - Monte, D.F.M., Júnior,W.D., Abley, M., Gebreyes, W.A., De Oliveira, C. J. B., Júnior, Melanie, Abley, W.D. L., Wondwossen, A.G., De Oliveira, C.J.B. (2018). Antimicrobial resistance and genotypic relatedness of environmental Staphylococci in semi-extensive dairy farms.Veterinary and Animal Science, 6, 103-106. https://doi.org/10.1016/j.vas.2018.07.007
CR  - Nazli, B. (1998). Researches on the ripening of turkish fermented sausage using a local starter culture combination.Turkish  Journal of Veterinary and Animal Sciences, 22, 393-397.
CR  - Nunes, R.C.S., Aquila, E.M.D., Paschoalin, W.M.F. (2015). Safety evaluation of the coagulase-negative Staphylococci microbiota of salami: superantigenic toxin production and antimicrobial resistance. BioMed Research International, 483548, 1-17. https://doi.org/10.1155/2015/483548
CR  - Özseven, A.G., Çetin, E.S., Arıdoğan, B.C., Çiftçi, E., Özseven, L. (2011). Antimicrobial Susceptibility of Enterococci Isolated from Various Clinical Specimens, Ankem Dergisi, 25(4), 256-262.  https://doi.org/10.5222/ankem.2011.256
CR  - Pollitt, E.J.G., Szkuta, P.T., Burns, N., Foster S.J. (2018). Staphylococcus aureus infection dynamics. PLoS Pathogens, 14(6), e1007112.   https://doi.org/10.1371/journal.ppat.1007112
CR  - Quast, C., Pruesse, E., Yilmaz, P., Gerken J., Schweer, T., Yarza, P., Peplies, J., Glockner, F.O. (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic acid Research, 4, 590-596. https://doi.org/10.1093/nar/gks1219
CR  - Saka, E., Gulel, G.T. (2018). detection of enterotoxin genes and methicillin-resistance in Staphylococcus aureus isolated from water buffalo milk and dairy products, Journal of Food Science, 83(6), 1716-1722. https://doi.org/10.1111/1750-3841.14172
CR  - Sanders, M.E., Akkermans, L.M.A., Haller, D., Hammerman, C., Heimbach, J.T., Hörmannsperger, G., Huys, G. (2010). Safety assessment of probiotics for human use. Gut Microbes, 1,164-185. https://doi.org/10.4161/gmic.1.3.12127
CR  - Schwendener, S. Cotting, K., Perreten, V. (2017). Novel methicillin resistance gene mecD in clinical Macrococcus caseolyticus strains from bovine and canine sources. Scientific Reports, 7, 43797. https://doi.org/10.1038/srep43797
CR  - Staphylococcal food intoxication. Division of disease control (2016). https://www.ndhealth.gov/Disease/Documents/faqs/staph_food_intoxication.pdf  (Accessed at 14.02.2019).
 
Suardana, I.W. (2014). Analysis of nucleotide sequences of the 16S rRNA gene of novel Escherichia coli Strains isolated from feces of human and Bali Cattle. Journal of Nucleic Acids, 475754, 1-7. https://doi.org/10.1155/2014/475754
CR  - Suzzi G., Caruso M., Gardini F., Lombardi A., Vannini L., Guerzoni M. E., Andrighetto, C., Lanorte, M.T. (2000). A survey of the enterococci isolated from an artisanal Italian goat’s cheese (Semicotto Caprino). Journal of Applied Microbiology, 89(2), 267–274. https://doi.org/10.1046/j.1365-2672.2000.01120.x
CR  - Temelli, S., Anar, S., Sen, C., Akyuva, P. (2006). Determination of microbiological contamination sources during Turkish white cheese production. Food Control, 17, 856-861. https://doi.org/10.1016/j.foodcont.2005.05.012
CR  - Turkish Food Codex Microbiological Criteria, Official journal (29 December 2011), General Directorate of Prime Ministry Legislation Development and Publication, 28157.
CR  - Yildirim, T., Sadati, F., Kocaman, B., Sirieken, B. (2019). Staphylococcus aureus and Staphylococcal enterotoxin detection in raw milk and cheese origin coagulase positive isolates. International Journal of Science Letters, (1), 30-41.
CR  - Younis, A., Krifucks, O., Heller, E.D., Samra, Z., Glickman, A., Saran Leitner, G. (2003). Staphylococcus aureus exosecretions and bovine mastitis. Journal of Veterinary Medicine, 50(1), 1-7. https://doi.org/10.1046/j.1439-0450.2003.00613.x
CR  - Yücel, N., Anıl, Y. (2011). Identification and antimicrobial susceptibility of Staphylococcus aureus and coagulase negative staphylococci isolated from raw milk and cheese samples. Turk Hijyen ve Deneysel Biyoloji Dergisi, 68(2), 73-78. https://doi.org/10.5505/TurkHijyen.2011.58070
UR  - https://doi.org/10.3153/FH20016
L1  - https://dergipark.org.tr/en/download/article-file/1085890
ER  -