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Identification of Enterococcus spp. and Lactococcus spp. Strains Isolated from Bovine Mastitis by MALDI-TOF MS and Evaluation of Antimicrobial Resistance Profiles

Yıl 2024, Cilt: 43 Sayı: 1, 8 - 14, 02.09.2024
https://doi.org/10.30782/jrvm.1327978

Öz

Mastitis is an important problem affecting animal health, welfare, and economy. Bacterial agents play a dominant role in the disease. The role of enterococcal and lactococcal species among environmental bacterial agents in mastitis has been underestimated due to inadequate identification. The aim of this study was to isolate and identify Enterococcus spp. and Lactococcus spp. from mastitic bovine milk and to evaluate the agents phenotypically in terms of antimicrobial resistance. A total of 108 milk samples from cattle with suspected mastitis were analyzed for enterococci and lactococci by standard microbiological techniques and matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS). By standard microbiological methods, 38 (35%) Enterococcus spp. and 13 (12%) Lactococcus spp. were isolated and identified from 51 milk samples. In species-level identification with MALDI-TOF MS, six different enterococci and three different lactococci were identified within acceptable score ranges. In antibiogram tests performed with the standard Kirby-Bauer method using 10 antimicrobials, 26% of the Enterococcus spp. and 46% of the Lactococcus spp. were resistant to at least 50% of the antimicrobials tested. In Enterococcus spp., the highest resistance rates were observed for enrofloxacin (79%) and ampicillin + cloxacillin (71%), while the best sensitivity (100%) was obtained for penicillin and ampicillin. In Lactococcus spp., the highest resistance rate was observed for enrofloxacin (85%) and amoxicillin + clavulanic acid (70%) and the best sensitivity (100%) was obtained for penicillin, ampicillin, and gentamicin.
As a result, it was concluded that the diversity and high rate of antimicrobial resistance of enterococcal and lactococcal species in mastitis isolates poses a serious potential threat to animal and public health.

Kaynakça

  • 1. Bradley AJ. Bovine mastitis: An Evolving Disease. The veterinary journal. 2002;164(2):116-128.
  • 2. Sorge US, Huber-Schlenstedt R, Schierling K. In vitro antimicrobial resistance profiles of Streptococcus uberis, Lactococcus spp., and Enterococcus spp. from quarter milk samples of cows between 2015 and 2019 in Southern Germany. Journal of Dairy Science. 2021;104(5):5998-6012.
  • 3. Devriese LA, Hommez J, Laevens H, Pot B, Vandamme P, Haesebrouck F. Identification of aesculin-hydrolyzing streptococci, lactococci, aerococci and enterococci from subclinical intramammary infections in dairy cows. Veterinary Microbiology. 1999;70(1-2):87- 94.
  • 4. Rodrigues MX, Lima SF, Higgins CH, Canniatti-Brazaca SG, Bicalho RC. The Lactococcus genus as a potential emerging mastitis pathogen group: A report on an outbreak investigation. Journal of Dairy Science. 2016;99(12):9864-9874.
  • 5. Ahmadi A, Khezri A, Nørstebø H, Ahmad R. A culture-, amplification-independent, and rapid method for identification of pathogens and antibiotic resistance profile in bovine mastitis milk. Frontiers in Microbiology. 2022; 13:1104701.
  • 6. Nonnemann B, Lyhs U, Svennesen L, Kristensen KA, Klaas IC, Pedersen K. Bovine mastitis bacteria resolved by MALDI-TOF mass spectrometry. Journal of Dairy Science. 2019;102(3):2515-2524.
  • 7. Ashraf A, Imran M. Diagnosis of bovine mastitis: from laboratory to farm. Tropical animal health and production. 2018;50:1193-1202.
  • 8. Jahan NA, Godden SM, Royster E, Schoenfuss TC, Gebhart C, Timmerman J, Fink RC. Evaluation of the matrix-assisted laser desorption ionization time of flight mass spectrometry (MALDI-TOF MS) system in the detection of mastitis pathogens from bovine milk samples. Journal of Microbiological Methods. 2021;182:106168.
  • 9. Tenhagen BA, Köster G, Wallmann J, Heuwieser W. Prevalence of Mastitis pathogens and Their Resistance Against Antimicrobial Agents in Dairy Cows in Brandenburg, Germany. Journal of Dairy Science. 2006;89(7):2542-2551.
  • 10. Duse A, Persson-Waller K, Pedersen K. Microbial Aetiology, Antibiotic Susceptibility and Pathogen-Specific Risk Factors for Udder Pathogens from Clinical Mastitis in Dairy Cows. Animals. 2021;11(7):2113.
  • 11. Devirgiliis C, Zinno P, Perozzi G. Update on antibiotic resistance in foodborne Lactobacillus and Lactococcus species. Frontiers in microbiology. 2013;4:301.
  • 12. Xie X, Pan Z, Yu Y, et al. Prevalence, Virulence, and Antibiotics Gene Profiles in Lactococcus garvieae Isolated from Cows with Clinical Mastitis in China. Microorganisms. 2023;11(2):379.
  • 13. García-Solache M, Rice LB. The Enterococcus: a model of adaptability to its environment. Clinical microbiology reviews. 2019;32(2):00058-18.
  • 14. Middleton JR, Fox LK, Pighetti G, Petersson-Wolfe C, eds. Laboratory handbook on Bovine Mastitis. National Mastitis Council;USA:2017.
  • 15. Ndeokwelu D, Olawale O, Alabi B, Oluwatosin O, Osho P. Probiotic Profiling of Selected Yogurt Drinks in Benin City, Edo-State, Nigeria. Clinica Immunology and Research. 2022;6(1):1-9.
  • 16. Mercanoğlu-Taban B., Numanoğlu-Çevik Y. The efficiency of MALDI-TOF MS method in detecting Staphylococcus aureus isolated from raw milk and artisanal dairy foods. CyTA-Journal of Food, 2021;19(1):739- 750.
  • 17. CLSI. Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard— Twelfth Edition. CLSI document M02-A12. Wayne, PA: Clinical and Laboratory Standards Institute;2015.
  • 18. CLSI. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals (6th ed. CLSI standard VET01S), Clinical and Laboratory Standards Institute;2023.
  • 19. CLSI. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals (4th ed. CLSI standard VET08), Clinical and Laboratory Standards Institute;2018.
  • 20. European Committee on Antimicrobial Susceptibility Testing. European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters. EUCAST Clinical Breakpoint Tables, Version 13.1;2023.
  • 21. Klaas IC, Zadoks RN. An update on environmental mastitis: Challenging perceptions. Transbound Emercing Diseases. 2018;65(1):166-185.
  • 22. Rowe SM, Godden SM, Royster E, Timmerman J, Boyle M. Postcalving udder health and productivity in cows approaching dry-off with intramammary infections caused by non-aureus Staphylococcus, Aerococcus, Enterococcus, Lactococcus, and Streptococcus species. Journal of Dairy Science. 2021;104(5):6061-6079.
  • 23. Tel OY, Keskin O, Zonturlu AK, Kaya NBA. Şanlıurfa yöresinde subklinik mastitislerin görülme oranı, aerobik bakteri izolasyonu ve duyarlı antibiyotiklerin belirlenmesi. Fırat Ünivetsitesi Sağlık Bilimleri Veteteriner Dergisi. 2009;23(2):101-106.
  • 24. Kenar B, Aksoy A, Köse Z. The new mastitis agents emerged in cattle in Turkey and an investigation of their antimicrobial susceptibility. Kocatepe Veterinary Journal. 2019;12(4):400-406.
  • 25. Kuyucuoğlu Y. Antibiotic resistances of enterococci isolated from bovine subclinical mastitis. Eurasian Journal of Veterinary Sciences. 2011;27(4):231-234.
  • 26. de Oliveira RP, Aragão BB, de Melo RPB, et al. Bovine mastitis in northeastern Brazil: Occurrence of emergent bacteria and their phenotypic and genotypic profile of antimicrobial resistance. Comparative Immunology, Microbiology and Infectious Diseases. 2022;85:101802.
  • 27. Bi Y, Wang YJ, Qin Y, et al. Prevalence of bovine mastitis pathogens in bulk tank milk in China. Plos one. 2016;11(5):0155621.
  • 28. Juliano LCB, Gouvêa FLR, Latosinski GS, et al. Species diversity and antimicrobial resistance patterns of Enterococcus spp. isolated from mastitis cases, milking machine and the environment of dairy cows. Letters in Applied Microbiology. 2022;75(4):924-932.
  • 29. Ahmed W, Neubauer H, Tomaso H, et al. Characterization of enterococci-and ESBL-producing Escherichia coli isolated from milk of bovides with mastitis in Egypt. Pathogens. 2021;10(2):97.
  • 30. Różańska H, Lewtak-Piłat A, Kubajka M, Weiner M. Occurrence of enterococci in mastitic cow’s milk and their antimicrobial resistance. Journal of veterinary research. 2019;63(1):93.
  • 31. Gao X, Fan C, Zhang Z, et al. Enterococcal isolates from bovine subclinical and clinical mastitis: Antimicrobial resistance and integron-gene cassette distribution. Microbial pathogenesis. 2019;129:82-87.
  • 32. Pascu C, Herman V, Iancu, I, Costinar L. Etiology of mastitis and antimicrobial resistance in dairy cattle farms in the western part of Romania. Antibiotics. 2022;11(1):57.
  • 33. Erbas G, Parin U, Türkyılmaz S, Uçan N, Öztürk M, Kaya O. Distribution of antibiotic resistance genes in Enterococcus spp. isolated from mastitis bovine milk. Acta Veterinaria-Beograd. 2016;66(3):336-346.
  • 34. Kim HJ, Youn HY, Kang HJ, et al. Prevalence and virulence characteristics of Enterococcus faecalis and Enterococcus faecium in bovine mastitis milk compared to bovine normal raw milk in South Korea. Animals. 2022;12(11):1407.
  • 35. Lin Y, Han J, Barkema HW, et al. Comparative genomic analyses of Lactococcus garvieae isolated from bovine mastitis in China. Microbiology Spectrum. 2023;11(3):02995-22.
  • 36. Blaiotta G, Pepe O, Mauriello G, et al. 16S–23S rDNA intergenic spacer region polymorphism of Lactococcus garvieae, Lactococcus raffinolactis and Lactococcus lactis as revealed by PCR and nucleotide sequence analysis. Systematic and Applied Microbiology. 2002;25(4):520-527.
  • 37. Werner B, Moroni P, Gioia G, et al. Genotypic and phenotypic identification of environmental streptococci and association of Lactococcus lactis ssp. lactis with intramammary infections among different dairy farms. Journal of dairy science. 2014;97(11):6964-6969.
  • 38. Hollenbeck BL, Rice LB. Intrinsic and acquired resistance mechanisms in enterococcus. Virulence, 2012;3(5):421-569.
  • 39. de Moraes GN, Guimarães FDF, Fornazari F, et al. Antimicrobial susceptibility profile of Enterococcus species isolated from cows with clinical mastitis and from bulk milk tanks in Brazil. African Journal of Microbiology Research, 2023;17(2):29-34.
  • 40. Plumed-Ferrer C, Barberio A, Franklin-Guild R, et al. Antimicrobial susceptibilities and random amplified polymorphic DNA-PCR fingerprint characterization of Lactococcus lactis ssp. lactis and Lactococcus garvieae isolated from bovine intramammary infections. Journal of Dairy Science, 2015;98(9):6216-6225.
  • 41. Velazquez-Meza ME, Galarde-López M, Carrillo- Quiróz B, Alpuche-Aranda CM. Antimicrobial resistance: One Health approach. Veterinary World, 2022;15(3):743-749.
  • 42. Kılıç E, Yenilmez F. Türkiye ve AB ülkelerinde antibiyotik kullanımı ve Dış ticaret dengesi üzerine bir değerlendirme. Halk Sağlığı Dergisi. 2019;4(1):45-54.
Yıl 2024, Cilt: 43 Sayı: 1, 8 - 14, 02.09.2024
https://doi.org/10.30782/jrvm.1327978

Öz

Kaynakça

  • 1. Bradley AJ. Bovine mastitis: An Evolving Disease. The veterinary journal. 2002;164(2):116-128.
  • 2. Sorge US, Huber-Schlenstedt R, Schierling K. In vitro antimicrobial resistance profiles of Streptococcus uberis, Lactococcus spp., and Enterococcus spp. from quarter milk samples of cows between 2015 and 2019 in Southern Germany. Journal of Dairy Science. 2021;104(5):5998-6012.
  • 3. Devriese LA, Hommez J, Laevens H, Pot B, Vandamme P, Haesebrouck F. Identification of aesculin-hydrolyzing streptococci, lactococci, aerococci and enterococci from subclinical intramammary infections in dairy cows. Veterinary Microbiology. 1999;70(1-2):87- 94.
  • 4. Rodrigues MX, Lima SF, Higgins CH, Canniatti-Brazaca SG, Bicalho RC. The Lactococcus genus as a potential emerging mastitis pathogen group: A report on an outbreak investigation. Journal of Dairy Science. 2016;99(12):9864-9874.
  • 5. Ahmadi A, Khezri A, Nørstebø H, Ahmad R. A culture-, amplification-independent, and rapid method for identification of pathogens and antibiotic resistance profile in bovine mastitis milk. Frontiers in Microbiology. 2022; 13:1104701.
  • 6. Nonnemann B, Lyhs U, Svennesen L, Kristensen KA, Klaas IC, Pedersen K. Bovine mastitis bacteria resolved by MALDI-TOF mass spectrometry. Journal of Dairy Science. 2019;102(3):2515-2524.
  • 7. Ashraf A, Imran M. Diagnosis of bovine mastitis: from laboratory to farm. Tropical animal health and production. 2018;50:1193-1202.
  • 8. Jahan NA, Godden SM, Royster E, Schoenfuss TC, Gebhart C, Timmerman J, Fink RC. Evaluation of the matrix-assisted laser desorption ionization time of flight mass spectrometry (MALDI-TOF MS) system in the detection of mastitis pathogens from bovine milk samples. Journal of Microbiological Methods. 2021;182:106168.
  • 9. Tenhagen BA, Köster G, Wallmann J, Heuwieser W. Prevalence of Mastitis pathogens and Their Resistance Against Antimicrobial Agents in Dairy Cows in Brandenburg, Germany. Journal of Dairy Science. 2006;89(7):2542-2551.
  • 10. Duse A, Persson-Waller K, Pedersen K. Microbial Aetiology, Antibiotic Susceptibility and Pathogen-Specific Risk Factors for Udder Pathogens from Clinical Mastitis in Dairy Cows. Animals. 2021;11(7):2113.
  • 11. Devirgiliis C, Zinno P, Perozzi G. Update on antibiotic resistance in foodborne Lactobacillus and Lactococcus species. Frontiers in microbiology. 2013;4:301.
  • 12. Xie X, Pan Z, Yu Y, et al. Prevalence, Virulence, and Antibiotics Gene Profiles in Lactococcus garvieae Isolated from Cows with Clinical Mastitis in China. Microorganisms. 2023;11(2):379.
  • 13. García-Solache M, Rice LB. The Enterococcus: a model of adaptability to its environment. Clinical microbiology reviews. 2019;32(2):00058-18.
  • 14. Middleton JR, Fox LK, Pighetti G, Petersson-Wolfe C, eds. Laboratory handbook on Bovine Mastitis. National Mastitis Council;USA:2017.
  • 15. Ndeokwelu D, Olawale O, Alabi B, Oluwatosin O, Osho P. Probiotic Profiling of Selected Yogurt Drinks in Benin City, Edo-State, Nigeria. Clinica Immunology and Research. 2022;6(1):1-9.
  • 16. Mercanoğlu-Taban B., Numanoğlu-Çevik Y. The efficiency of MALDI-TOF MS method in detecting Staphylococcus aureus isolated from raw milk and artisanal dairy foods. CyTA-Journal of Food, 2021;19(1):739- 750.
  • 17. CLSI. Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard— Twelfth Edition. CLSI document M02-A12. Wayne, PA: Clinical and Laboratory Standards Institute;2015.
  • 18. CLSI. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals (6th ed. CLSI standard VET01S), Clinical and Laboratory Standards Institute;2023.
  • 19. CLSI. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals (4th ed. CLSI standard VET08), Clinical and Laboratory Standards Institute;2018.
  • 20. European Committee on Antimicrobial Susceptibility Testing. European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters. EUCAST Clinical Breakpoint Tables, Version 13.1;2023.
  • 21. Klaas IC, Zadoks RN. An update on environmental mastitis: Challenging perceptions. Transbound Emercing Diseases. 2018;65(1):166-185.
  • 22. Rowe SM, Godden SM, Royster E, Timmerman J, Boyle M. Postcalving udder health and productivity in cows approaching dry-off with intramammary infections caused by non-aureus Staphylococcus, Aerococcus, Enterococcus, Lactococcus, and Streptococcus species. Journal of Dairy Science. 2021;104(5):6061-6079.
  • 23. Tel OY, Keskin O, Zonturlu AK, Kaya NBA. Şanlıurfa yöresinde subklinik mastitislerin görülme oranı, aerobik bakteri izolasyonu ve duyarlı antibiyotiklerin belirlenmesi. Fırat Ünivetsitesi Sağlık Bilimleri Veteteriner Dergisi. 2009;23(2):101-106.
  • 24. Kenar B, Aksoy A, Köse Z. The new mastitis agents emerged in cattle in Turkey and an investigation of their antimicrobial susceptibility. Kocatepe Veterinary Journal. 2019;12(4):400-406.
  • 25. Kuyucuoğlu Y. Antibiotic resistances of enterococci isolated from bovine subclinical mastitis. Eurasian Journal of Veterinary Sciences. 2011;27(4):231-234.
  • 26. de Oliveira RP, Aragão BB, de Melo RPB, et al. Bovine mastitis in northeastern Brazil: Occurrence of emergent bacteria and their phenotypic and genotypic profile of antimicrobial resistance. Comparative Immunology, Microbiology and Infectious Diseases. 2022;85:101802.
  • 27. Bi Y, Wang YJ, Qin Y, et al. Prevalence of bovine mastitis pathogens in bulk tank milk in China. Plos one. 2016;11(5):0155621.
  • 28. Juliano LCB, Gouvêa FLR, Latosinski GS, et al. Species diversity and antimicrobial resistance patterns of Enterococcus spp. isolated from mastitis cases, milking machine and the environment of dairy cows. Letters in Applied Microbiology. 2022;75(4):924-932.
  • 29. Ahmed W, Neubauer H, Tomaso H, et al. Characterization of enterococci-and ESBL-producing Escherichia coli isolated from milk of bovides with mastitis in Egypt. Pathogens. 2021;10(2):97.
  • 30. Różańska H, Lewtak-Piłat A, Kubajka M, Weiner M. Occurrence of enterococci in mastitic cow’s milk and their antimicrobial resistance. Journal of veterinary research. 2019;63(1):93.
  • 31. Gao X, Fan C, Zhang Z, et al. Enterococcal isolates from bovine subclinical and clinical mastitis: Antimicrobial resistance and integron-gene cassette distribution. Microbial pathogenesis. 2019;129:82-87.
  • 32. Pascu C, Herman V, Iancu, I, Costinar L. Etiology of mastitis and antimicrobial resistance in dairy cattle farms in the western part of Romania. Antibiotics. 2022;11(1):57.
  • 33. Erbas G, Parin U, Türkyılmaz S, Uçan N, Öztürk M, Kaya O. Distribution of antibiotic resistance genes in Enterococcus spp. isolated from mastitis bovine milk. Acta Veterinaria-Beograd. 2016;66(3):336-346.
  • 34. Kim HJ, Youn HY, Kang HJ, et al. Prevalence and virulence characteristics of Enterococcus faecalis and Enterococcus faecium in bovine mastitis milk compared to bovine normal raw milk in South Korea. Animals. 2022;12(11):1407.
  • 35. Lin Y, Han J, Barkema HW, et al. Comparative genomic analyses of Lactococcus garvieae isolated from bovine mastitis in China. Microbiology Spectrum. 2023;11(3):02995-22.
  • 36. Blaiotta G, Pepe O, Mauriello G, et al. 16S–23S rDNA intergenic spacer region polymorphism of Lactococcus garvieae, Lactococcus raffinolactis and Lactococcus lactis as revealed by PCR and nucleotide sequence analysis. Systematic and Applied Microbiology. 2002;25(4):520-527.
  • 37. Werner B, Moroni P, Gioia G, et al. Genotypic and phenotypic identification of environmental streptococci and association of Lactococcus lactis ssp. lactis with intramammary infections among different dairy farms. Journal of dairy science. 2014;97(11):6964-6969.
  • 38. Hollenbeck BL, Rice LB. Intrinsic and acquired resistance mechanisms in enterococcus. Virulence, 2012;3(5):421-569.
  • 39. de Moraes GN, Guimarães FDF, Fornazari F, et al. Antimicrobial susceptibility profile of Enterococcus species isolated from cows with clinical mastitis and from bulk milk tanks in Brazil. African Journal of Microbiology Research, 2023;17(2):29-34.
  • 40. Plumed-Ferrer C, Barberio A, Franklin-Guild R, et al. Antimicrobial susceptibilities and random amplified polymorphic DNA-PCR fingerprint characterization of Lactococcus lactis ssp. lactis and Lactococcus garvieae isolated from bovine intramammary infections. Journal of Dairy Science, 2015;98(9):6216-6225.
  • 41. Velazquez-Meza ME, Galarde-López M, Carrillo- Quiróz B, Alpuche-Aranda CM. Antimicrobial resistance: One Health approach. Veterinary World, 2022;15(3):743-749.
  • 42. Kılıç E, Yenilmez F. Türkiye ve AB ülkelerinde antibiyotik kullanımı ve Dış ticaret dengesi üzerine bir değerlendirme. Halk Sağlığı Dergisi. 2019;4(1):45-54.
Toplam 42 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Veteriner Bilimleri (Diğer)
Bölüm Research Articles
Yazarlar

Songül Ötkün 0000-0003-2736-953X

Ayda Nur Oğuz 0000-0002-0771-8029

Ferhat Yıldırım 0009-0006-9399-8245

Yaşar Tel 0000-0001-7848-3899

Yayımlanma Tarihi 2 Eylül 2024
Kabul Tarihi 16 Nisan 2024
Yayımlandığı Sayı Yıl 2024 Cilt: 43 Sayı: 1

Kaynak Göster

APA Ötkün, S., Oğuz, A. N., Yıldırım, F., Tel, Y. (2024). Identification of Enterococcus spp. and Lactococcus spp. Strains Isolated from Bovine Mastitis by MALDI-TOF MS and Evaluation of Antimicrobial Resistance Profiles. Journal of Research in Veterinary Medicine, 43(1), 8-14. https://doi.org/10.30782/jrvm.1327978
AMA Ötkün S, Oğuz AN, Yıldırım F, Tel Y. Identification of Enterococcus spp. and Lactococcus spp. Strains Isolated from Bovine Mastitis by MALDI-TOF MS and Evaluation of Antimicrobial Resistance Profiles. J Res Vet Med. Eylül 2024;43(1):8-14. doi:10.30782/jrvm.1327978
Chicago Ötkün, Songül, Ayda Nur Oğuz, Ferhat Yıldırım, ve Yaşar Tel. “Identification of Enterococcus Spp. And Lactococcus Spp. Strains Isolated from Bovine Mastitis by MALDI-TOF MS and Evaluation of Antimicrobial Resistance Profiles”. Journal of Research in Veterinary Medicine 43, sy. 1 (Eylül 2024): 8-14. https://doi.org/10.30782/jrvm.1327978.
EndNote Ötkün S, Oğuz AN, Yıldırım F, Tel Y (01 Eylül 2024) Identification of Enterococcus spp. and Lactococcus spp. Strains Isolated from Bovine Mastitis by MALDI-TOF MS and Evaluation of Antimicrobial Resistance Profiles. Journal of Research in Veterinary Medicine 43 1 8–14.
IEEE S. Ötkün, A. N. Oğuz, F. Yıldırım, ve Y. Tel, “Identification of Enterococcus spp. and Lactococcus spp. Strains Isolated from Bovine Mastitis by MALDI-TOF MS and Evaluation of Antimicrobial Resistance Profiles”, J Res Vet Med, c. 43, sy. 1, ss. 8–14, 2024, doi: 10.30782/jrvm.1327978.
ISNAD Ötkün, Songül vd. “Identification of Enterococcus Spp. And Lactococcus Spp. Strains Isolated from Bovine Mastitis by MALDI-TOF MS and Evaluation of Antimicrobial Resistance Profiles”. Journal of Research in Veterinary Medicine 43/1 (Eylül 2024), 8-14. https://doi.org/10.30782/jrvm.1327978.
JAMA Ötkün S, Oğuz AN, Yıldırım F, Tel Y. Identification of Enterococcus spp. and Lactococcus spp. Strains Isolated from Bovine Mastitis by MALDI-TOF MS and Evaluation of Antimicrobial Resistance Profiles. J Res Vet Med. 2024;43:8–14.
MLA Ötkün, Songül vd. “Identification of Enterococcus Spp. And Lactococcus Spp. Strains Isolated from Bovine Mastitis by MALDI-TOF MS and Evaluation of Antimicrobial Resistance Profiles”. Journal of Research in Veterinary Medicine, c. 43, sy. 1, 2024, ss. 8-14, doi:10.30782/jrvm.1327978.
Vancouver Ötkün S, Oğuz AN, Yıldırım F, Tel Y. Identification of Enterococcus spp. and Lactococcus spp. Strains Isolated from Bovine Mastitis by MALDI-TOF MS and Evaluation of Antimicrobial Resistance Profiles. J Res Vet Med. 2024;43(1):8-14.