Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products

ATASEVER, mustafa; bilgin, mustafa

doi:10.51354/mjen.1185346

Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products

Mustafa BİLGİN, (Atatürk Üniversitesi, Veteriner Fakültesi, Gıda Hijyeni ve Teknolojisi, Erzurum, Türkiye)

Mustafa ATASEVER (Atatürk Üniversitesi, Veteriner Fakültesi, Gıda Hijyeni ve Teknolojisi, Erzurum, Türkiye)

Manas Journal of Engineering

2 0

Yıl: 2022 Cilt: 10 Sayı: 2 Sayfa Aralığı: 151 - 158 Metin Dili: İngilizce DOI: 10.51354/mjen.1185346 İndeks Tarihi: 10-01-2023

Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products

Öz:

Milk and its products can be frequently contaminated with enterotoxigenic and methicillin-resistant S. aureus, and in such a case, it causes various diseases, especially staphylococcal food poisoning. In the present study, 100 sample materials (50 goat milk, 25 goat cream, and 25 goat cheese) were collected from 65 livestock farms in Erzurum. All samples were analyzed and tested selectively according to the EN ISO 6888-1 procedure standard. The obtained isolates were examined with the PCR in terms of nuc, Panton-Valentine Leukocidin (PVL), mecA, and enterotoxin genes. S. aureus was detected in 4 of 50 (8%) milk samples, 2 of 25 (8%) cream samples, 3 of 25 (12%) cheese samples, and 9 of the total samples (9%). While the incidence of methicillin resistance was found to be 3% by the disc diffusion method, the incidence of the mecA gene was found to be 2% by PCR. In terms of enterotoxin genes, 8% (4/50) of milk samples, 12% (3/25) of cheese samples, and 8% (2/25) of cream samples contained at least one enterotoxin gene. In total, 9% of 100 samples contained enterotoxigenic S. aureus. In conclusion, the consumption of enterotoxigenic and mecA positive S. aureus-containing raw milk, dairy products that have not been adequately heat-treated, or milk and products that are not kept in proper storage conditions pose a danger to public health.

Anahtar Kelime:

Belge Türü: Makale Makale Türü: Araştırma Makalesi Erişim Türü: Erişime Açık

[1]. Bezirtzoglou E., Maipa V., Voidarou C., Tsiotsias A., Papapetropoulou M., “Food-borne intestinal bacterial pathogens”, Microb. Ecol., 12(2), (2000), 96-104.
[2]. Wieland B., Feil C., Gloria-Maercker E., Thumm G., Lechner M., Bravo J. M., Götz F., “Genetic and biochemical analyses of the biosynthesis of the yellow carotenoid 4, 4'- diaponeurosporene of Staphylococcus aureus”, J. Bacteriol, 176(24), (1994). 7719-7726.
[3]. Wertheim, H. F., Melles, D. C., Vos, M. C., van Leeuwen W., Van Belkum A., Verbrugh H. A., Nouwen J. L., “The role of nasal carriage in Staphylococcus aureus infections”, Lancet Infect. Dis., 5(12), (2005), 751-762.
[4]. Stryjewski M.E., G.R. Corey, “Methicillin-resistant Staphylococcus aureus: an evolving pathogen”. Clin. Infect. Dis., 58, (2014), 10-19.
[5]. Xu Z., Peters B. M., Li B., Li L., Shirtliff M. E., “Staphylococcal Food Poisoning and Novel Perspectives in Food Safety”, in Prevention and Control of Food Related Diseases, vol. 1, M.H. Anthony, Eds. Croatia, İnTech, 2016, 159.
[6]. Di Giannatale E., Prencipe V., Tonelli A., Marfoglia C., Migliorati G., “Characterisation of Staphylococcus aureus strains isolated from food for human consumption”, Veterinaria Italiana, 47(2), (2011), 165-173.
[7]. Haenlein G., “Goat milk in human nutrition. Small ruminant research”, 51(2), (2004), 155-163.
[8]. Kim H.K., Falugi F., Missiakas D.M., Schneewind, O., “Peptidoglycan-linked protein A promotes T cell-dependent antibody expansion during Staphylococcus aureus infection”, Proc. Natl. Acad. Sci., 113(20), (2016), 5718-5723.
[9]. Argudín M.Á., Mendoza M.C., Rodicio M.R., “Food poisoning and Staphylococcus aureus enterotoxins. Toxins”, 2(7), (2010), 1751-1773.
[10]. Tsutsuura S., Shimamura Y., Murata M., “Temperature dependence of the production of staphylococcal enterotoxin A by Staphylococcus aureus”, Biosci. Biotechnol. Biochem., 77, (2013) 30–37.
[11]. Omoe K., Hu D. L., Ono H. K., Shimizu S., Takahashi-Omoe H., Nakane A., Imanishi K. I., “Emetic potentials of newly identified staphylococcal enterotoxin-like toxins”, Infect. Immun., 81(10), (2013), 3627-3631.
[12]. Klevens R. M., Morrison M. A., Nadle J., Petit S., Gershman K., Ray S., “Invasive methicillin-resistant Staphylococcus aureus infections in the United States”, Jama, 298(15), (2007), 1763- 1771.
[13]. Ito T., Katayama Y., Asada K., Mori N., Tsutsumimoto K., Tiensasitorn C., Hiramatsu K., “Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus”, Antimicrob. Agents Chemother., 45(5), (2001), 1323- 1336.
[14]. Archer, G.L., “Staphylococcus aureus: a well-armed pathogen” Rev. Infect. Dis., 26(5), (1998),1179-1181.
[15]. Saka, E., G. Terzi Gulel, “Detection of enterotoxin genes and methicillin resistance in Staphylococcus aureus isolated from water buffalo milk and dairy products”, J. Food Sci., 83(6), (2018), 1716-1722.
[16]. Wald R., Hess C., Urbantke V., Wittek T., Baumgartner M., “Characterization of Staphylococcus Species Isolated from Bovine Quarter Milk Samples”, Animals, 9(5), (2019), 200.
[17]. Wayne, P.A., “Performance standards for antimicrobial susceptibility testing”, Clinical Laboratory Standard Institute, 1, (2009), 19.
[18]. Oliver S.P., Jayarao B.M., Almeida R.A., “Foodborne pathogens in milk and the dairy farm environment: food safety and public health implications”, Foodbourne Pathogens & Disease, 2(2), (2005), 115-129.
[19]. Günday H., “Aydın bölgesinde ürüne işlenecek çiğ sütlerde staphylococcus aureus ve enterotoksin varlığının araştırılması,” M.S. thesis, Institute of Health Sciences, Department of Microbiology, Adnan Menderes Üniversitesi, Aydın,Türkiye, 2017.
[20]. Mørk T., Kvitle B., Mathisen T., Jørgensen H. J., “Bacteriological and molecular investigations of Staphylococcus aureus in dairy goats”, Vet. Microbiol., 141(1-2), (2010), 134-141.
[21]. Menzies, P.I., Ramanoon S.Z., “Mastitis of sheep and goats”, Vet. Clin. North Am. Food Anim., 17(2), (2001), 333-358.
[22]. Yücel N., Anıl Y., “Çiğ süt ve peynir örneklerinden Staphylococcus aureus ve koagülaz negatif stafilokokların identifikasyonu ve antibiyotik duyarlılığı”, Türk Hijyen ve Deneysel Biyoloji Dergisi, 68(2), (2011), 73-78.
[23]. Rahimi E., “Enterotoxigenicity of Staphylococcus aureus isolated from traditional and commercial dairy products marketed in Iran”, Brazilian Journal of Microbiology, 44, (2013), 393-399.
[24]. Basanisi M. G., Nobil, G., La Bella G., Russo R., Spano G., Normanno G., La Salandra G., “Molecular characterization of Staphylococcus aureus isolated from sheep and goat cheeses in southern Italy”, Small Rumin. Res., 135, (2016), 17-19.
[25]. Özpınar N., Gümüşsoy K.S., “Phenotypic and genotypic determination of antibiotic resistant and biofilm forming Staphylococcus aureus isolated in Erzincan tulum cheese”, Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 19(3), (2013), 517- 521.
[26]. Türkyılmaz S., Tekbıyık S., Oryasin E., Bozdogan B., “Molecular epidemiology and antimicrobial resistance mechanisms of methicillin resistant Staphylococcus aureus isolated from bovine milk”, Zoonoses and Public Health, 57(3), (2010),197- 203.
[27]. Can H.Y., Celik T.H., “Detection of enterotoxigenic and antimicrobial resistant S. aureus in Turkish cheeses”, Food Control, 24(1-2), (2012), 100-103.
[28]. Omoshaba E.O., Ojo O.E., Oyekunle M.A., Sonibare A. O., Adebayo A. O., “Methicillin-resistant Staphylococcus aureus (MRSA) isolated from raw milk and nasal swabs of small ruminants in Abeokuta”, Nigeria. Trop. Anim. Health Prod., 52(5), (2020), 2599-2608.
[29]. Obaidat M.M., Bani Salman A.E., Roess A.A., “High prevalence and antimicrobial resistance of mecA Staphylococcus aureus in dairy cattle, sheep, and goat bulk tank milk in Jordan”, Trop. Anim. Health Prod., 50(2), (2018), 405-412.
[30]. Jacoby G.A., Archer G.L., “New mechanisms of bacterial resistance to antimicrobial agents”, N. Engl. J. Med., 324(9), (1991), 601-612.
[31]. Oliveira D.C., Lencastre H.N.D., “Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus”, Antimicrob. Agents Chemother., 46(7), (2002), 2155- 2161.
[32]. Swenson J.M., Lonsway D., McAllister S., Thompson A., Jevitt L., Zhu W., Patel J.B., “Detection of mecA-mediated resistance using reference and commercial testing methods in a collection of Staphylococcus aureus expressing borderline oxacillin MICs”, Diagn. Microbiol. Infect. Dis., 58(1), (2007), 33-39.
[33]. Cauwelier B., Gordts B., Descheemaecker P., Van Landuyt H., “Evaluation of a disk diffusion method with cefoxitin (30 μg) for detection of methicillin-resistant Staphylococcus aureus”, Eur. J. Clin. Microbiol. Infect. Dis., 23(5), (2004), 389-392.
[34]. Tomasz A., Drugeon H.B., De Lencastre H.M., Jabes D., McDougall L., Bille, J., “New mechanism for methicillin resistance in Staphylococcus aureus: clinical isolates that lack the PBP 2a gene and contain normal penicillin-binding proteins with modified penicillin-binding capacity”, Antimicrob. Agents Chemother., 33(11), (1989), 1869-1874.
[35]. Jørgensen H.J., Mørk T., Rørvik L.M., “The occurrence of Staphylococcus aureus on a farm with small-scale production of raw milk cheese”, J. Dairy Sci., 88(11), (2005), 3810-3817.
[36]. Kashiwada T., Kikuchi K., Abe S., Kato H., Hayashi H., Morimoto T., Gemma A, “Staphylococcal enterotoxin B toxic shock syndrome induced by community- acquired methicillin- resistant Staphylococcus aureus (CA-MRSA)”, Internal Medicine, 51(21), (2012), 3085-3088.
[37]. Lyra D.G., Sousa F.G., Borges M.F., Givisiez P.E., Queiroga R.C., Souza E.L., Oliveira C.J., “Enterotoxin-encoding genes in Staphylococcus spp. from bulk goat milk. Foodborne Pathog”. Dis., 10(2), (2013), 126-130.

APA	bilgin m, ATASEVER m (2022). Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products. , 151 - 158. 10.51354/mjen.1185346
Chicago	bilgin mustafa,ATASEVER mustafa Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products. (2022): 151 - 158. 10.51354/mjen.1185346
MLA	bilgin mustafa,ATASEVER mustafa Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products. , 2022, ss.151 - 158. 10.51354/mjen.1185346
AMA	bilgin m,ATASEVER m Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products. . 2022; 151 - 158. 10.51354/mjen.1185346
Vancouver	bilgin m,ATASEVER m Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products. . 2022; 151 - 158. 10.51354/mjen.1185346
IEEE	bilgin m,ATASEVER m "Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products." , ss.151 - 158, 2022. 10.51354/mjen.1185346
ISNAD	bilgin, mustafa - ATASEVER, mustafa. "Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products". (2022), 151-158. https://doi.org/10.51354/mjen.1185346

APA	bilgin m, ATASEVER m (2022). Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products. Manas Journal of Engineering, 10(2), 151 - 158. 10.51354/mjen.1185346
Chicago	bilgin mustafa,ATASEVER mustafa Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products. Manas Journal of Engineering 10, no.2 (2022): 151 - 158. 10.51354/mjen.1185346
MLA	bilgin mustafa,ATASEVER mustafa Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products. Manas Journal of Engineering, vol.10, no.2, 2022, ss.151 - 158. 10.51354/mjen.1185346
AMA	bilgin m,ATASEVER m Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products. Manas Journal of Engineering. 2022; 10(2): 151 - 158. 10.51354/mjen.1185346
Vancouver	bilgin m,ATASEVER m Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products. Manas Journal of Engineering. 2022; 10(2): 151 - 158. 10.51354/mjen.1185346
IEEE	bilgin m,ATASEVER m "Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products." Manas Journal of Engineering, 10, ss.151 - 158, 2022. 10.51354/mjen.1185346
ISNAD	bilgin, mustafa - ATASEVER, mustafa. "Determining the enterotoxin genes and methicillin resistance in Staphylococcus Aureus isolated from goat milk and its products". Manas Journal of Engineering 10/2 (2022), 151-158. https://doi.org/10.51354/mjen.1185346