Keçilerde Staphylococcus aureus’un Bakteriyolojik ve Moleküler Olarak Araştırılması

Öz

Bu çalışmada, 2010 yılının yaz aylarında Aydın ilinde yetiştirilen 50 laktasyondaki Hair (Anadolu Kara) keçisi ve 50 laktasyondaki Saanen keçisinden süt, deri, vajinal mukoza ve nazal mukozadan toplam 400 örnek toplanmıştır. Örnekler, Adnan Menderes Üniversitesi Veteriner Fakültesi Mikrobiyoloji Anabilim Dalı laboratuvarına taşınmıştır. Toplanan 400 örneğin 48’inden (%12) Staphylococcus aureus izole edilmiştir. Polimeraz zincir reaksiyonu (PCR) analizi sonucunda, bu izolatların 13’ünde (%27) 278-bp fragmentinde sek stafilokokal enterotoksin geninin bulunduğu tespit edilmiştir. Tespit edilen enterotoksin genlerinin 10’u (%66,7) süt izolatlarında, 2’si (%22) nazal izolatlarda ve 1’i (%11,1) deri izolatında belirlenmiştir. Irklara göre dağılım incelendiğinde; Hair keçilerinin süt izolatlarında 8 (%42,1), Saanen keçilerinin süt izolatlarında 2 (%25), Hair keçilerinin deri izolatında 1 (%5,2) ve Hair keçilerinin nazal izolatlarında 2 (%10,5) gen saptanmıştır. Hair keçilerinde S. aureus’un daha yüksek oranda görülmesi, bu ırkın daha çok ekstansif yetiştiriciliğe tabi tutulması ve çevresel etkenlere daha fazla maruz kalmasıyla ilişkili olabilir. Bu bulgular, Hair keçisi sürülerinde yönetim, besleme ve hijyen uygulamalarının önemini vurgulamaktadır. Ayrıca, stafilokokal enterotoksin genlerinin moleküler yöntemlerle hızlı ve yüksek duyarlılıkla tespit edilebildiği gösterilmiştir.

Anahtar Kelimeler

• Enterotoksin
• Keçi
• PCR
• Staphylococcus aureus
• Süt

Bacteriological and Molecular Characterization of Staphylococcus aureus Isolates from Hair and Saanen Goats

Öz

In this study, a total of 400 samples were collected from the milk, skin, vaginal mucosa, and nasal mucosa of 50 lactating Hair goats and 50 lactating Saanen goats raised in the Aydın province during the summer of 2010. The samples were transported to the laboratory of the Department of Microbiology, Faculty of Veterinary Medicine, Adnan Menderes University. Staphylococcus aureus was isolated from 48 samples (12%). Polymerase chain reaction (PCR) analysis revealed that 13 (27%) of these isolates harbored the sek staphylococcal enterotoxin gene (278-bp fragment). Among the detected enterotoxin genes, 10 (66.7%) were obtained from milk isolates, 2 (22%) from nasal isolates, and 1 (11.1%) from a skin isolate. Distribution by breed showed that 8 (42.1%) of the genes were detected in milk isolates of Hair goats, 2 (25%) in milk isolates of Saanen goats, 1 (5.2%) in a skin isolate of a Hair goat, and 2 (10.5%) in nasal isolates of Hair goats. The higher prevalence of S. aureus in Hair goats may be associated with their extensive breeding practices and increased environmental exposure to the pathogen. These findings emphasize the importance of management, nutrition, and hygiene practices in Hair goat flocks. Furthermore, molecular methods provided rapid and highly sensitive detection of staphylococcal enterotoxin genes.

Anahtar Kelimeler

• Goat
• Enterotoxin
• Milk
• PCR
• Staphylococcus aureus

Kaynakça

1. Angelidis, A.S., Komodromos, D., Giannakou, R., Arsenos, G.,Gelasakis, A.I., Kyritsi, M.,… & Sergelidis, D. (2020). Isolation and characterization of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) from milk of dairy goats under low-input farm management in Greece. Veterinary Microbiology, 247, 108749.https://doi.org/10.1016/j.vetmic.2020.108749
2. Angelidis, A.S., Komodromos, D., Giannakou, R., Arsenos, G.,Gelasakis, A.I., Kyritsi, M.,… & Sergelidis, D. (2020). Isolation and characterization of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) from milk of dairy goats under low-input farm management in Greece. Veterinary Microbiology, 247, 108749.https://doi.org/10.1016/j.vetmic.2020.108749
3. Berger, T.F.H., Brasca, M., Buchner, M., Bütikofer, U., Castiglioni,., Cremonesi, P., … & Schwendimann, L. (2025). Critical factors affecting the prevalence of Staphylococcus aureus and staphylococcal enterotoxins in raw milk cheese in the Alpine region of Austria, Italy, and Switzerland. Foods, 14(13), 2176. https://doi.org/10.3390/foods14132176
4. Berger, T.F.H., Brasca, M., Buchner, M., Bütikofer, U., Castiglioni,., Cremonesi, P., … & Schwendimann, L. (2025). Critical factors affecting the prevalence of Staphylococcus aureus and staphylococcal enterotoxins in raw milk cheese in the Alpine region of Austria, Italy, and Switzerland. Foods, 14(13), 2176. https://doi.org/10.3390/foods14132176
5. Bergonier, D., Sobral, D., & Martins, K. (2003). Staphylococcus infections in small ruminants. Veterinary Research, 34(5), 521–537. https://doi.org/10.1051/vetres:2003030 Bianchi, D.M., Gallina, S., Bellio, A., Chiesa, F., Civera, T.,Decastelli, L., & Carraro, E. (2014). Enterotoxin gene profiles ofStaphylococcus aureus isolated from milk and dairy productsin Italy. Letters in Applied Microbiology, 58(2), 190–196.https://doi.org/10.1111/lam.12182
6. Bergonier, D., Sobral, D., & Martins, K. (2003). Staphylococcus infections in small ruminants. Veterinary Research, 34(5), 521–537. https://doi.org/10.1051/vetres:2003030 Bianchi, D.M., Gallina, S., Bellio, A., Chiesa, F., Civera, T.,Decastelli, L., & Carraro, E. (2014). Enterotoxin gene profiles ofStaphylococcus aureus isolated from milk and dairy productsin Italy. Letters in Applied Microbiology, 58(2), 190–196.https://doi.org/10.1111/lam.12182
7. Cieza, M.Y.R., Vélez, C.C., Ramírez, D.A., Delgado, J.L., Carranza,P.L., & Salinas, J.A. (2024). Staphylococcal enterotoxins:Description and importance. Pathogens, 13(5), 391.https://doi.org/10.3390/pathogens13080676
8. Cieza, M.Y.R., Vélez, C.C., Ramírez, D.A., Delgado, J.L., Carranza,P.L., & Salinas, J.A. (2024). Staphylococcal enterotoxins:Description and importance. Pathogens, 13(5), 391.https://doi.org/10.3390/pathogens13080676

9. Fusco, V., Quero, G.M., Morea, M., Blaiotta, G., & Visconti, A.(2011). Rapid and reliable identification of Staphylococcus aureus harbouring the enterotoxin gene cluster (egc)and quantitative detection in raw milk by real-time PCR.International Journal of Food Microbiology, 144(3), 528–537. https://doi.org/10.1016/j.ijfoodmicro.2010.11.016
10. Fusco, V., Quero, G.M., Morea, M., Blaiotta, G., & Visconti, A.(2011). Rapid and reliable identification of Staphylococcus aureus harbouring the enterotoxin gene cluster (egc)and quantitative detection in raw milk by real-time PCR.International Journal of Food Microbiology, 144(3), 528–537. https://doi.org/10.1016/j.ijfoodmicro.2010.11.016
11. Kayili, E., & Sanlibaba, P. (2020). Prevalence, characterizationand antibiotic resistance of Staphylococcus aureus isolated from traditional cheeses in Turkey. InternationalJournal of Food Properties, 23(1), 1441–1451. https://doi.org/10.1080/10942912.2020.1814323
12. Kayili, E., & Sanlibaba, P. (2020). Prevalence, characterizationand antibiotic resistance of Staphylococcus aureus isolated from traditional cheeses in Turkey. InternationalJournal of Food Properties, 23(1), 1441–1451. https://doi.org/10.1080/10942912.2020.1814323
13. Kırkan, Ş., Erbaş, G., Savaşan, S., Uçan, N., Gürpınar, S., & Özavcı, V.(2014). Detection of antimicrobial resistance in Staphylococcusaureus isolated from Saanen goats with subclinical mastitis. AnimalHealth, Production and Hygiene, 3(1), 284–287.
14. Kırkan, Ş., Erbaş, G., Savaşan, S., Uçan, N., Gürpınar, S., & Özavcı, V.(2014). Detection of antimicrobial resistance in Staphylococcusaureus isolated from Saanen goats with subclinical mastitis. AnimalHealth, Production and Hygiene, 3(1), 284–287.
15. Koneman, E.W., Allen, S.D., Janda, W.M., Schreckenberger, P.C., &Winn, W.C. (1997). Gram-positive cocci: Staphylococci and relatedorganisms. In Color Atlas and Textbook of Diagnostic Microbiology(5th ed.). New York, NY: Lippincott.
16. Koneman, E.W., Allen, S.D., Janda, W.M., Schreckenberger, P.C., &Winn, W.C. (1997). Gram-positive cocci: Staphylococci and relatedorganisms. In Color Atlas and Textbook of Diagnostic Microbiology(5th ed.). New York, NY: Lippincott.
17. Kürekci, C. (2016). Short communication: Prevalence, antimicrobial resistance, and resistant traits of coagulase-negative staphylococciisolated from cheese samples in Turkey. Journal of Dairy Science, 99(4), 2675–2679. https://doi.org/10.3168/jds.2015-10725
18. Kürekci, C. (2016). Short communication: Prevalence, antimicrobial resistance, and resistant traits of coagulase-negative staphylococciisolated from cheese samples in Turkey. Journal of Dairy Science, 99(4), 2675–2679. https://doi.org/10.3168/jds.2015-10725
19. Letertre, C., Perelle, S., Dilasser, F., & Fach, P. (2003). Detection andgenotyping by real-time PCR of the staphylococcal enterotoxingenes sea to sej. Molecular and Cellular Probes, 17(4), 139–147. https://doi.org/10.1016/S0890-8508(03)00045-8
20. Letertre, C., Perelle, S., Dilasser, F., & Fach, P. (2003). Detection andgenotyping by real-time PCR of the staphylococcal enterotoxingenes sea to sej. Molecular and Cellular Probes, 17(4), 139–147. https://doi.org/10.1016/S0890-8508(03)00045-8
21. Merz, A., Stephan, R., & Johler, S. (2016). Staphylococcus aureusisolates from goat and sheep milk seem to be closely relatedand differ from isolates detected from bovine milk. Frontiers inMicrobiology, 7, 319. https://doi.org/10.3389/fmicb.2016.00319
22. Merz, A., Stephan, R., & Johler, S. (2016). Staphylococcus aureusisolates from goat and sheep milk seem to be closely relatedand differ from isolates detected from bovine milk. Frontiers inMicrobiology, 7, 319. https://doi.org/10.3389/fmicb.2016.00319
23. Mørk, T., Kvitle, B., Mathisen, T., & Jørgensen, H.J. (2010).Bacteriological and molecular investigations of Staphylococcus aureus in dairy goats. Veterinary Microbiology, 141(1–2), 134–141. https://doi.org/10.1016/j.vetmic.2009.08.019
24. Mørk, T., Kvitle, B., Mathisen, T., & Jørgensen, H.J. (2010).Bacteriological and molecular investigations of Staphylococcus aureus in dairy goats. Veterinary Microbiology, 141(1–2), 134–141. https://doi.org/10.1016/j.vetmic.2009.08.019
25. Murray, P.R., Baron, E.J., Jorgensen, J.H., Pfaller, M.A., & Yolken,R.H. (Eds.). (2003). Manual of Clinical Microbiology (8th ed.).Washington, DC: ASM Press.
26. Murray, P.R., Baron, E.J., Jorgensen, J.H., Pfaller, M.A., & Yolken,R.H. (Eds.). (2003). Manual of Clinical Microbiology (8th ed.).Washington, DC: ASM Press.
27. Özavcı, V., & Kırkan, Ş. (2012). Methicillin resistance in Staphylococcus aureus and infections. Etlik Veteriner Mikrobiyoloji Dergisi, 23(1), 70–76. Pehlivan, E. (2017). The role of environmental factors in the productivityof Hair goats in Aegean pastures. Ege Üniversitesi Ziraat FakültesiDergisi, 54(2), 153–160.
28. Özavcı, V., & Kırkan, Ş. (2012). Methicillin resistance in Staphylococcus aureus and infections. Etlik Veteriner Mikrobiyoloji Dergisi, 23(1), 70–76. Pehlivan, E. (2017). The role of environmental factors in the productivityof Hair goats in Aegean pastures. Ege Üniversitesi Ziraat FakültesiDergisi, 54(2), 153–160.
29. Pexara, A., Solomakos, N., Sergelidis, D., Angelidis, A.S., &Govaris, A. (2016). Occurrence and antibiotic resistance ofenterotoxigenic Staphylococcus aureus in raw ovine and caprine milk in Greece. Dairy Science & Technology, 96(3), 345–357.https://://doi.org/10.1007/s13594-015-0272-z
30. Pexara, A., Solomakos, N., Sergelidis, D., Angelidis, A.S., &Govaris, A. (2016). Occurrence and antibiotic resistance ofenterotoxigenic Staphylococcus aureus in raw ovine and caprine milk in Greece. Dairy Science & Technology, 96(3), 345–357.https://://doi.org/10.1007/s13594-015-0272-z
31. Pinchuk, I.V., Beswick, E.J., & Reyes, V.E. (2010).Staphylococcal enterotoxins. Toxins, 2(8), 2177–2197. https://doi.org/10.3390/toxins2082177
32. Pinchuk, I.V., Beswick, E.J., & Reyes, V.E. (2010).Staphylococcal enterotoxins. Toxins, 2(8), 2177–2197. https://doi.org/10.3390/toxins2082177
33. Qian, W., Shen, L., Li, X., Wang, T., Liu, M., Wang, W., Fu, Y., & Zeng,Q. (2019). Epidemiological characteristics of Staphylococcus aureusin raw goat milk in Shaanxi Province, China. Antibiotics, 8(3), 141. https://doi.org/10.3390/antibiotics8030141
34. Qian, W., Shen, L., Li, X., Wang, T., Liu, M., Wang, W., Fu, Y., & Zeng,Q. (2019). Epidemiological characteristics of Staphylococcus aureusin raw goat milk in Shaanxi Province, China. Antibiotics, 8(3), 141. https://doi.org/10.3390/antibiotics8030141
35. Savaşan, S., Kırkan, Ş., Erbaş, G., Parın, U., & Çiftci, A. (2017).Determination of virulence factors of Staphylococci isolated frombovine mastitis. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 23(6), 947–952. https://doi.org/10.9775/kvfd.2017.18015
36. Savaşan, S., Kırkan, Ş., Erbaş, G., Parın, U., & Çiftci, A. (2017).Determination of virulence factors of Staphylococci isolated frombovine mastitis. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 23(6), 947–952. https://doi.org/10.9775/kvfd.2017.18015
37. Sekkin, S., Kum, C., Kırkan, Ş., Güleş, Ö., & Akar, F. (2010). The efficacyof a cefoperazone–danofloxacin combination in the treatment ofsubclinical mastitis in dairy cows caused by Staphylococcus aureus. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 16(1), 97–104.https://doi.org/10.9775/kvfd.2009.501
38. Sekkin, S., Kum, C., Kırkan, Ş., Güleş, Ö., & Akar, F. (2010). The efficacyof a cefoperazone–danofloxacin combination in the treatment ofsubclinical mastitis in dairy cows caused by Staphylococcus aureus. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 16(1), 97–104.https://doi.org/10.9775/kvfd.2009.501
39. Titouche, Y., Akkou, M., Campaña-Burguet, A., González-Azcona, C.,Djaoui, Y., Mechoub, D., … & Hennekinne, J.A. (2024). Phenotypic and genotypic characterization of Staphylococcus aureus isolated from nasal samples of healthy dairy goats in Algeria. Pathogens, 13(5), 408. https://doi.org/10.3390/pathogens13050408
40. Titouche, Y., Akkou, M., Campaña-Burguet, A., González-Azcona, C.,Djaoui, Y., Mechoub, D., … & Hennekinne, J.A. (2024). Phenotypic and genotypic characterization of Staphylococcus aureus isolated from nasal samples of healthy dairy goats in Algeria. Pathogens, 13(5), 408. https://doi.org/10.3390/pathogens13050408