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PRESENCE OF THE POTENTIAL PATHOGENS AND MULTIPLE ANTIBIOTIC RESISTANCE IN MILK FROM HEALTHY ANIMALS: EVALUATION OF STREPTOCOCCUS SPP. STRAINS

Year 2023, Volume: 48 Issue: 5, 952 - 962, 15.10.2023
https://doi.org/10.15237/gida.GD23065

Abstract

The variety of microorganisms contained in raw milk and their resistance profile potentially pose a danger to human health and the food industry. This study was aimed to investigate pathogen content of milk samples obtained from healthy animals and the prevalence of Streptococcus, a common contaminant of milk, and antibiotic resistance profiles. In total, 358 isolates, including Staphylococcus spp., Streptococcus spp., Lactococcus spp, Escherichia coli, Klebsiella oxytoca, Enterococcus faecalis and Macrococcus caseolyticus, were obtained from 249 milk samples. The prevalence of streptococci was found 24.58%. Streptococcal isolates were found most resistant to the aminoglycoside class, followed by quinolone, tetracycline, macrolide, beta lactam, nitrofuran and phenicol resistance respectively. This situation has shown that the consumption of raw milk can be a potential risk for foodborne infection. Hence, it was thought that consumers should avoid unpasteurized milk and dairy products, monitor raw milk more in terms of antibiotic resistance, and take the necessary precautions.

Project Number

-

References

  • Ahmed, I. M. (2021). Detection of CTX-M gene in extended spectrum β-lactamases producing Enterobacteriaceae isolated from bovine milk. Iraqi Journal of Veterinary Sciences, 35(2), 397-402. Doi: 10.33899/ijvs.2020.126909.1412
  • Andersson, D. I., Balaban, N. Q., Baquero, F. (2020). Antibiotic resistance: turning evolutionary principles into clinical reality. FEMS Microbiol Review, 44(2), 171-188. Doi: 10.1093/femsre/fuaa001
  • Başar, C. S., Heperkan, Z. D. (2021). Sütün mikrobiyotası ve bozulmasına yol açan önemli bakteriler. Gıda, 46(3), 660-668. Doi: 10.15237/gida.GD21034
  • Berendonk, T. U., Manaia, C. M., Merlin, C., Fatta-Kassinos, D., Cytryn, E., Walsh, F., ... & Martinez, J. L. (2015). Tackling antibiotic resistance: the environmental framework. Nature reviews microbiology, 13(5), 310-317.
  • Brosius, J., Palmer, M.L., Kennedy, P.J., Noller, H.F. (1978). Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proceedings of the National Academy of Sciences 75, 4801–4805. Doi: 10.1073/pnas.75.10.4801
  • Cervinkova, D., Vlkova, H., Borodacova, I., Makovcova, J., Babak, V., Lorencova, A., Jaglic, Z. (2013). Prevalence of mastitis pathogens in milk from clinically healthy cows. Veterinarni Medicina, 58(11), 567-575.
  • Cheng, W. N., Han, S. G. (2020). Bovine mastitis: Risk factors, therapeutic strategies, and alternative treatments-A review. Asian-Australasian Journal of Animal Sciences, 33(11), 1699. Doi: 10.5713/ajas.20.0156
  • Chiesa, L. M., DeCastelli, L., Nobile, M., Martucci, F., Mosconi, G., Fontana, M., Panseri, S. (2020). Analysis of antibiotic residues in raw bovine milk and their impact toward food safety and on milk starter cultures in cheese-making process. Lwt, 131, 109783. Doi: 10.1016/j.lwt.2020.109783
  • CLSI (2019). Performance standards for antimicrobial susceptibility testing. 29th ed. CLSI supplement M100. Wayne, PA ABD.
  • de Jong A, Simjee S, El Garch F ve ark. (2018). Antimicrobial susceptibility of enterococci recovered from healthy cattle, pigs and chickens in nine EU countries (EASSA Study) to critically important antibiotics. Veterinary Microbiology, 216, 168-175. Doi: 10.1016/j.vetmic.2018.02.010
  • Companyó, R., Granados, M., Guiteras, J. ve Prat, M. D. (2009). Antibiotics in food: Legislation and validation of analytical methodologies. Analytical and Bioanalytical Chemistry, 395(4), 877–891. doi:10.1007/s00216-009-2969-4
  • Delibaş, Y., Türkyılmaz, S. (2018). Detection of Some Bacteriocin Genes in Enterococcus faecium Isolates Obtained from Mastitic Bovine Milk Samples. Van Veterinary Journal, 29(1).
  • Emam, A., El-Diasty, M., Abdelkhalek, A. (2021). Prevalence of Staphyloсoссus aureus and Streptococcus agalaсtiae isolated from Raw Milk in Dakahlia Governorate, Egypt. Zagazig Veterinary Journal, 49(1), 67-77. Doi: 10.21608/ZVJZ.2021.64186.1131
  • Fusco, V., Chieffi, D., Fanelli, F., Logrieco, A. F., Cho, G. S., Kabisch, J., Franz, C. M. (2020). Microbial quality and safety of milk and milk products in the 21st century. Comprehensive Reviews in Food Science and Food Safety, 19(4), 2013-2049. Doi: 10.1111/1541-4337.12568
  • Gueimonde, M.; Sánchez, B.; G. de los Reyes-Gavilán, C.; Margolles, A. Antibiotic resistance in probiotic bacteria. Front Microbiol, 2013, 4, 202. https://doi.org/10.3389/fmicb.2013.00202
  • Guneri, C. O., Kızılyıldırım, S. (2022). Tüketime sunulan çiğ sütlerde Escherichia coli O157: H7 araştırılması. Süleyman Demirel Üniversitesi Sağlık Bilimleri Dergisi, 13(3), 441-447. Doi: 10.22312/sdusbed.1202809
  • Guzmán-Luna, P., Nag, R., Martínez, I., Mauricio-Iglesias, M., Hospido, A., & Cummins, E. (2022). Quantifying current and future raw milk losses due to bovine mastitis on European dairy farms under climate change scenarios. Science of the Total Environment, 833. Doi: 155149. 10.1016/j.scitotenv.2022.155149
  • İrkin, R., Batu, Z. ve Özbek, K. (2019). Hayvansal besinlerdeki antibiyotik kalıntılarının insan sağlığına etkileri. International Agean Symposium on Innovative Interdisciplinary Scientific Researches Proceedings Book.
  • Kabelitz, T., Aubry, E., van Vorst, K., Amon, T., & Fulde, M. (2021). The role of Streptococcus spp. in bovine mastitis. Microorganisms, 9(7), 1497. Doi: 10.3390/microorganisms9071497
  • Keyvan, E. (2019). Çiğ süt örneklerinden izole edilen Staphylococcus aureus izolatlarında antibiyotik direnç özelliklerinin tespiti. Veteriner Hekimler Derneği Dergisi. 90(1): 9-14.
  • Kou, X., Cai, H., Huang, S., Ni, Y., Luo, B., Qian, H., Wang, X. (2021). Prevalence and characteristics of Staphylococcus aureus isolated from retail raw milk in Northern Xinjiang, China. Frontiers in Microbiology, 12, 705947. Doi: 10.3389/fmicb.2021.705947
  • Küçükbüğrü, N., Acaröz, U. (2020). Gıdalarda antibiyotik kalıntıları ve halk sağlığına etkileri. Veteriner Farmakoloji ve Toksikoloji Derneği Bülteni, 11(3), 161-167. Doi:10.38137/vetfarmatoksbulten.822713 Lucey, J. A. (2015). Raw milk consumption: risks and benefits. Nutrition Today, 50(4), 189. doi: 10.1097/NT.0000000000000108
  • Magagula, S., Petzer, I. M., Famuyide, I. M., & Karzis, J. (2023). Biofilm expression and antimicrobial resistance patterns of Streptococcus uberis isolated from milk samples of dairy cows in South Africa. Journal of Dairy Research, 90(1), 42-46. Doi: 10.1017/S0022029923000158.
  • Miclean, M., Cadar, O., Levei, E. A., Roman, R., Ozunu, A., & Levei, L. (2019). Metal (Pb, Cu, Cd, and Zn) transfer along food chain and health risk assessment through raw milk consumption from free-range cows. International Journal of Environmental Research and Public Health, 16(21), 4064. Doi: 10.3390/ijerph16214064
  • Nhung, N. T., Cuong, N. V., Thwaites, G., and Carrique-Mas, J. (2016). Antimicrobial usage and antimicrobial resistance in animal production in southeast asia: a review. Antibiotics 5:37. doi: 10.3390/antibiotics5040037
  • Pérez, V. K. C., da Costa, G. M., Guimaraes, A. S., Heinemann, M. B., Lage, A. P., & Dorneles, E. M. S. (2020). Relationship between virulence factors and antimicrobial resistance in Staphylococcus aureus from bovine mastitis. Journal of Global Antimicrobial Resistance, 22, 792-802. Doi: 10.1016/j.jgar.2020.06.010
  • Read, A. F., Woods, R. J. (2014). Antibiotic resistance management. Evolution, Medicine, and Public Health, 2014(1), 147. Doi:10.1093/emph/eou024
  • Saed, H. A. E. M. R., Ibrahim, H. M. M. (2020). Antimicrobial profile of multidrug-resistant Streptococcus spp. isolated from dairy cows with clinical mastitis. Journal of Advanced Veterinary and Animal Research, 7(2), 186. Doi: 10.5455/javar.2020.g409
  • Sezener, M. G., Fındık, A., Ergüden, V. E., Akgöz, S., Gülhan, T., Çiftci, A. (2019). The Determination of Antibiotic Resistances and Some Virulence Genes of Staphylococcus aureus Isolated from Bovine Mastitis. JAES, 2019, 4.2: 182-187. Doi: 10.35229/jaes.571977
  • Sharun, K., Dhama, K., Tiwari, R., Gugjoo, M. B., Iqbal Yatoo, M.; Patel, S. K., Chaicumpa, W. (2021). Advances in therapeutic and managemental approaches of bovine mastitis: a comprehensive review. Veterinary Quarterly 41(1), 107-136. Doi: 10.1080/01652176.2021.1882713
  • Sipahi, N., Karakaya, E., Ikiz, S. (2019). Phenotypic and genotypic investigation of the heavy metal resistance in Escherichia coli isolates recovered from cattle stool samples. Turkish Journal of Veterinary & Animal Sciences, 43(5), 684-691. Doi: 10.3906/vet-1903-82
  • Sipahi, N., Mutlu, C., Akkan, T. (2013). Giresun İlinde tüketime sunulan bazı balıklardan izole edilen Enterobacteriaceae üyelerinin antibiyotik ve ağır metal dirençlilik düzeyleri. Gıda, 38(6), 343-349. Doi: 10.5505/gida.2013.55264
  • Skočková, A., Bogdanovıčová, K., Koláčková, I., Karpíšková, R. (2015). Antimicrobial-resistant and extended-spectrum β-Lactamase–producing Escherichia coli in raw cow's milk. Journal of Food Protection, 78(1), 72-77. Doi: 10.4315/0362-028X.JFP-14-250
  • Sørensen, U. B. S., Klaas, I. C., Boes, J., & Farre, M. (2019). The distribution of clones of Streptococcus agalactiae (group B streptococci) among herdspersons and dairy cows demonstrates lack of host specificity for some lineages. Veterinary Microbiology, 235, 71-79. Doi: 10.1016/j.vetmic.2019.06.008
  • Sorge, U. S., Huber-Schlenstedt, R., Schierling, K. (2021). 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, 104(5), 5998-6012. Doi: 10.3168/jds.2020-19896
  • Tian, X. Y., Zheng, N., Han, R. W., Ho, H., Wang, J., Wang, Y. T., Yu, Z. N. (2019). Antimicrobial resistance and virulence genes of Streptococcus isolated from dairy cows with mastitis in China. Microbial Pathogenesis, 131, 33-39.
  • Zalewska, M., Błażejewska, A., Czapko, A., & Popowska, M. (2021). Antibiotics and antibiotic resistance genes in animal manure–consequences of its application in agriculture. Frontiers in Microbiology, 12, 640. Doi: 10.3389/fmicb.2021.610656
  • Zhao, Y., Shao, W., Wang, F., Ma, J. (2022). Chen from mastitis milk samples in China. Journal of Veterinary Research 66, 581-590. Doi: 10.2478/jvetres-2022-0069

SAĞLIKLI HAYVANLARDAN ALINAN SÜT ÖRNEKLERİNDE POTANSİYEL PATOJENLER VE ÇOKLU ANTİBİYOTİK DİRENÇLİLİĞİ: STREPTOCOCCUS SPP. SUŞLARININ DEĞERLENDİRİLMESİ

Year 2023, Volume: 48 Issue: 5, 952 - 962, 15.10.2023
https://doi.org/10.15237/gida.GD23065

Abstract

Çiğ sütün içerdiği mikroorganizma çeşitliliği ve bunların direnç profili potansiyel olarak insan sağlığı ve gıda endüstrisi için bir tehlike arz etmektedir. Bu çalışmada sağlıklı hayvanlardan elde edilen süt örneklerinin patojen ihtivası yönünden incelenmesi, sütün yaygın kontaminantı Streptococcus spp. prevalansının ve antibiyotik direnç profillerinin araştırılması amaçlanmıştır. 249 süt örneğinden Staphylococcus spp., Streptococcus spp., Lactococcus spp., Escherichia coli, Klebsiella oxytoca, Enterecoccus faecalis ve Macrococcus caseolyticus olmak üzere 358 izolat elde edilmiştir. Streptokok prevalansı %24.58 olarak tespit edilmiştir. Streptokok izolatlarının en fazla aminoglikozid sınıfına dirençli olduğu, ardından sırasıyla kinolon, tetrasiklin, makrolid, beta laktam, nitrofuran ve fenikole karşı direnç gösterdiği tespit edilmiştir. Bu durum çiğ süt tüketiminin gıda kaynaklı enfeksiyon için potansiyel bir risk olabileceğini göstermiştir. Bu nedenle tüketicilerin pastörize edilmemiş süt ve süt ürünlerinden kaçınması, çiğ sütlerin antibiyotik direnci yönünden daha fazla izlenmesi ve gerekli önlemlerin alınması gerektiği düşünülmüştür.

Supporting Institution

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Project Number

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Thanks

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References

  • Ahmed, I. M. (2021). Detection of CTX-M gene in extended spectrum β-lactamases producing Enterobacteriaceae isolated from bovine milk. Iraqi Journal of Veterinary Sciences, 35(2), 397-402. Doi: 10.33899/ijvs.2020.126909.1412
  • Andersson, D. I., Balaban, N. Q., Baquero, F. (2020). Antibiotic resistance: turning evolutionary principles into clinical reality. FEMS Microbiol Review, 44(2), 171-188. Doi: 10.1093/femsre/fuaa001
  • Başar, C. S., Heperkan, Z. D. (2021). Sütün mikrobiyotası ve bozulmasına yol açan önemli bakteriler. Gıda, 46(3), 660-668. Doi: 10.15237/gida.GD21034
  • Berendonk, T. U., Manaia, C. M., Merlin, C., Fatta-Kassinos, D., Cytryn, E., Walsh, F., ... & Martinez, J. L. (2015). Tackling antibiotic resistance: the environmental framework. Nature reviews microbiology, 13(5), 310-317.
  • Brosius, J., Palmer, M.L., Kennedy, P.J., Noller, H.F. (1978). Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proceedings of the National Academy of Sciences 75, 4801–4805. Doi: 10.1073/pnas.75.10.4801
  • Cervinkova, D., Vlkova, H., Borodacova, I., Makovcova, J., Babak, V., Lorencova, A., Jaglic, Z. (2013). Prevalence of mastitis pathogens in milk from clinically healthy cows. Veterinarni Medicina, 58(11), 567-575.
  • Cheng, W. N., Han, S. G. (2020). Bovine mastitis: Risk factors, therapeutic strategies, and alternative treatments-A review. Asian-Australasian Journal of Animal Sciences, 33(11), 1699. Doi: 10.5713/ajas.20.0156
  • Chiesa, L. M., DeCastelli, L., Nobile, M., Martucci, F., Mosconi, G., Fontana, M., Panseri, S. (2020). Analysis of antibiotic residues in raw bovine milk and their impact toward food safety and on milk starter cultures in cheese-making process. Lwt, 131, 109783. Doi: 10.1016/j.lwt.2020.109783
  • CLSI (2019). Performance standards for antimicrobial susceptibility testing. 29th ed. CLSI supplement M100. Wayne, PA ABD.
  • de Jong A, Simjee S, El Garch F ve ark. (2018). Antimicrobial susceptibility of enterococci recovered from healthy cattle, pigs and chickens in nine EU countries (EASSA Study) to critically important antibiotics. Veterinary Microbiology, 216, 168-175. Doi: 10.1016/j.vetmic.2018.02.010
  • Companyó, R., Granados, M., Guiteras, J. ve Prat, M. D. (2009). Antibiotics in food: Legislation and validation of analytical methodologies. Analytical and Bioanalytical Chemistry, 395(4), 877–891. doi:10.1007/s00216-009-2969-4
  • Delibaş, Y., Türkyılmaz, S. (2018). Detection of Some Bacteriocin Genes in Enterococcus faecium Isolates Obtained from Mastitic Bovine Milk Samples. Van Veterinary Journal, 29(1).
  • Emam, A., El-Diasty, M., Abdelkhalek, A. (2021). Prevalence of Staphyloсoссus aureus and Streptococcus agalaсtiae isolated from Raw Milk in Dakahlia Governorate, Egypt. Zagazig Veterinary Journal, 49(1), 67-77. Doi: 10.21608/ZVJZ.2021.64186.1131
  • Fusco, V., Chieffi, D., Fanelli, F., Logrieco, A. F., Cho, G. S., Kabisch, J., Franz, C. M. (2020). Microbial quality and safety of milk and milk products in the 21st century. Comprehensive Reviews in Food Science and Food Safety, 19(4), 2013-2049. Doi: 10.1111/1541-4337.12568
  • Gueimonde, M.; Sánchez, B.; G. de los Reyes-Gavilán, C.; Margolles, A. Antibiotic resistance in probiotic bacteria. Front Microbiol, 2013, 4, 202. https://doi.org/10.3389/fmicb.2013.00202
  • Guneri, C. O., Kızılyıldırım, S. (2022). Tüketime sunulan çiğ sütlerde Escherichia coli O157: H7 araştırılması. Süleyman Demirel Üniversitesi Sağlık Bilimleri Dergisi, 13(3), 441-447. Doi: 10.22312/sdusbed.1202809
  • Guzmán-Luna, P., Nag, R., Martínez, I., Mauricio-Iglesias, M., Hospido, A., & Cummins, E. (2022). Quantifying current and future raw milk losses due to bovine mastitis on European dairy farms under climate change scenarios. Science of the Total Environment, 833. Doi: 155149. 10.1016/j.scitotenv.2022.155149
  • İrkin, R., Batu, Z. ve Özbek, K. (2019). Hayvansal besinlerdeki antibiyotik kalıntılarının insan sağlığına etkileri. International Agean Symposium on Innovative Interdisciplinary Scientific Researches Proceedings Book.
  • Kabelitz, T., Aubry, E., van Vorst, K., Amon, T., & Fulde, M. (2021). The role of Streptococcus spp. in bovine mastitis. Microorganisms, 9(7), 1497. Doi: 10.3390/microorganisms9071497
  • Keyvan, E. (2019). Çiğ süt örneklerinden izole edilen Staphylococcus aureus izolatlarında antibiyotik direnç özelliklerinin tespiti. Veteriner Hekimler Derneği Dergisi. 90(1): 9-14.
  • Kou, X., Cai, H., Huang, S., Ni, Y., Luo, B., Qian, H., Wang, X. (2021). Prevalence and characteristics of Staphylococcus aureus isolated from retail raw milk in Northern Xinjiang, China. Frontiers in Microbiology, 12, 705947. Doi: 10.3389/fmicb.2021.705947
  • Küçükbüğrü, N., Acaröz, U. (2020). Gıdalarda antibiyotik kalıntıları ve halk sağlığına etkileri. Veteriner Farmakoloji ve Toksikoloji Derneği Bülteni, 11(3), 161-167. Doi:10.38137/vetfarmatoksbulten.822713 Lucey, J. A. (2015). Raw milk consumption: risks and benefits. Nutrition Today, 50(4), 189. doi: 10.1097/NT.0000000000000108
  • Magagula, S., Petzer, I. M., Famuyide, I. M., & Karzis, J. (2023). Biofilm expression and antimicrobial resistance patterns of Streptococcus uberis isolated from milk samples of dairy cows in South Africa. Journal of Dairy Research, 90(1), 42-46. Doi: 10.1017/S0022029923000158.
  • Miclean, M., Cadar, O., Levei, E. A., Roman, R., Ozunu, A., & Levei, L. (2019). Metal (Pb, Cu, Cd, and Zn) transfer along food chain and health risk assessment through raw milk consumption from free-range cows. International Journal of Environmental Research and Public Health, 16(21), 4064. Doi: 10.3390/ijerph16214064
  • Nhung, N. T., Cuong, N. V., Thwaites, G., and Carrique-Mas, J. (2016). Antimicrobial usage and antimicrobial resistance in animal production in southeast asia: a review. Antibiotics 5:37. doi: 10.3390/antibiotics5040037
  • Pérez, V. K. C., da Costa, G. M., Guimaraes, A. S., Heinemann, M. B., Lage, A. P., & Dorneles, E. M. S. (2020). Relationship between virulence factors and antimicrobial resistance in Staphylococcus aureus from bovine mastitis. Journal of Global Antimicrobial Resistance, 22, 792-802. Doi: 10.1016/j.jgar.2020.06.010
  • Read, A. F., Woods, R. J. (2014). Antibiotic resistance management. Evolution, Medicine, and Public Health, 2014(1), 147. Doi:10.1093/emph/eou024
  • Saed, H. A. E. M. R., Ibrahim, H. M. M. (2020). Antimicrobial profile of multidrug-resistant Streptococcus spp. isolated from dairy cows with clinical mastitis. Journal of Advanced Veterinary and Animal Research, 7(2), 186. Doi: 10.5455/javar.2020.g409
  • Sezener, M. G., Fındık, A., Ergüden, V. E., Akgöz, S., Gülhan, T., Çiftci, A. (2019). The Determination of Antibiotic Resistances and Some Virulence Genes of Staphylococcus aureus Isolated from Bovine Mastitis. JAES, 2019, 4.2: 182-187. Doi: 10.35229/jaes.571977
  • Sharun, K., Dhama, K., Tiwari, R., Gugjoo, M. B., Iqbal Yatoo, M.; Patel, S. K., Chaicumpa, W. (2021). Advances in therapeutic and managemental approaches of bovine mastitis: a comprehensive review. Veterinary Quarterly 41(1), 107-136. Doi: 10.1080/01652176.2021.1882713
  • Sipahi, N., Karakaya, E., Ikiz, S. (2019). Phenotypic and genotypic investigation of the heavy metal resistance in Escherichia coli isolates recovered from cattle stool samples. Turkish Journal of Veterinary & Animal Sciences, 43(5), 684-691. Doi: 10.3906/vet-1903-82
  • Sipahi, N., Mutlu, C., Akkan, T. (2013). Giresun İlinde tüketime sunulan bazı balıklardan izole edilen Enterobacteriaceae üyelerinin antibiyotik ve ağır metal dirençlilik düzeyleri. Gıda, 38(6), 343-349. Doi: 10.5505/gida.2013.55264
  • Skočková, A., Bogdanovıčová, K., Koláčková, I., Karpíšková, R. (2015). Antimicrobial-resistant and extended-spectrum β-Lactamase–producing Escherichia coli in raw cow's milk. Journal of Food Protection, 78(1), 72-77. Doi: 10.4315/0362-028X.JFP-14-250
  • Sørensen, U. B. S., Klaas, I. C., Boes, J., & Farre, M. (2019). The distribution of clones of Streptococcus agalactiae (group B streptococci) among herdspersons and dairy cows demonstrates lack of host specificity for some lineages. Veterinary Microbiology, 235, 71-79. Doi: 10.1016/j.vetmic.2019.06.008
  • Sorge, U. S., Huber-Schlenstedt, R., Schierling, K. (2021). 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, 104(5), 5998-6012. Doi: 10.3168/jds.2020-19896
  • Tian, X. Y., Zheng, N., Han, R. W., Ho, H., Wang, J., Wang, Y. T., Yu, Z. N. (2019). Antimicrobial resistance and virulence genes of Streptococcus isolated from dairy cows with mastitis in China. Microbial Pathogenesis, 131, 33-39.
  • Zalewska, M., Błażejewska, A., Czapko, A., & Popowska, M. (2021). Antibiotics and antibiotic resistance genes in animal manure–consequences of its application in agriculture. Frontiers in Microbiology, 12, 640. Doi: 10.3389/fmicb.2021.610656
  • Zhao, Y., Shao, W., Wang, F., Ma, J. (2022). Chen from mastitis milk samples in China. Journal of Veterinary Research 66, 581-590. Doi: 10.2478/jvetres-2022-0069
There are 38 citations in total.

Details

Primary Language Turkish
Subjects Food Engineering
Journal Section Articles
Authors

Nisa Sipahi 0000-0001-8915-3545

Cansu Çelik Doğan 0000-0002-9508-7473

Project Number -
Early Pub Date September 1, 2023
Publication Date October 15, 2023
Published in Issue Year 2023 Volume: 48 Issue: 5

Cite

APA Sipahi, N., & Çelik Doğan, C. (2023). SAĞLIKLI HAYVANLARDAN ALINAN SÜT ÖRNEKLERİNDE POTANSİYEL PATOJENLER VE ÇOKLU ANTİBİYOTİK DİRENÇLİLİĞİ: STREPTOCOCCUS SPP. SUŞLARININ DEĞERLENDİRİLMESİ. Gıda, 48(5), 952-962. https://doi.org/10.15237/gida.GD23065
AMA Sipahi N, Çelik Doğan C. SAĞLIKLI HAYVANLARDAN ALINAN SÜT ÖRNEKLERİNDE POTANSİYEL PATOJENLER VE ÇOKLU ANTİBİYOTİK DİRENÇLİLİĞİ: STREPTOCOCCUS SPP. SUŞLARININ DEĞERLENDİRİLMESİ. The Journal of Food. October 2023;48(5):952-962. doi:10.15237/gida.GD23065
Chicago Sipahi, Nisa, and Cansu Çelik Doğan. “SAĞLIKLI HAYVANLARDAN ALINAN SÜT ÖRNEKLERİNDE POTANSİYEL PATOJENLER VE ÇOKLU ANTİBİYOTİK DİRENÇLİLİĞİ: STREPTOCOCCUS SPP. SUŞLARININ DEĞERLENDİRİLMESİ”. Gıda 48, no. 5 (October 2023): 952-62. https://doi.org/10.15237/gida.GD23065.
EndNote Sipahi N, Çelik Doğan C (October 1, 2023) SAĞLIKLI HAYVANLARDAN ALINAN SÜT ÖRNEKLERİNDE POTANSİYEL PATOJENLER VE ÇOKLU ANTİBİYOTİK DİRENÇLİLİĞİ: STREPTOCOCCUS SPP. SUŞLARININ DEĞERLENDİRİLMESİ. Gıda 48 5 952–962.
IEEE N. Sipahi and C. Çelik Doğan, “SAĞLIKLI HAYVANLARDAN ALINAN SÜT ÖRNEKLERİNDE POTANSİYEL PATOJENLER VE ÇOKLU ANTİBİYOTİK DİRENÇLİLİĞİ: STREPTOCOCCUS SPP. SUŞLARININ DEĞERLENDİRİLMESİ”, The Journal of Food, vol. 48, no. 5, pp. 952–962, 2023, doi: 10.15237/gida.GD23065.
ISNAD Sipahi, Nisa - Çelik Doğan, Cansu. “SAĞLIKLI HAYVANLARDAN ALINAN SÜT ÖRNEKLERİNDE POTANSİYEL PATOJENLER VE ÇOKLU ANTİBİYOTİK DİRENÇLİLİĞİ: STREPTOCOCCUS SPP. SUŞLARININ DEĞERLENDİRİLMESİ”. Gıda 48/5 (October 2023), 952-962. https://doi.org/10.15237/gida.GD23065.
JAMA Sipahi N, Çelik Doğan C. SAĞLIKLI HAYVANLARDAN ALINAN SÜT ÖRNEKLERİNDE POTANSİYEL PATOJENLER VE ÇOKLU ANTİBİYOTİK DİRENÇLİLİĞİ: STREPTOCOCCUS SPP. SUŞLARININ DEĞERLENDİRİLMESİ. The Journal of Food. 2023;48:952–962.
MLA Sipahi, Nisa and Cansu Çelik Doğan. “SAĞLIKLI HAYVANLARDAN ALINAN SÜT ÖRNEKLERİNDE POTANSİYEL PATOJENLER VE ÇOKLU ANTİBİYOTİK DİRENÇLİLİĞİ: STREPTOCOCCUS SPP. SUŞLARININ DEĞERLENDİRİLMESİ”. Gıda, vol. 48, no. 5, 2023, pp. 952-6, doi:10.15237/gida.GD23065.
Vancouver Sipahi N, Çelik Doğan C. SAĞLIKLI HAYVANLARDAN ALINAN SÜT ÖRNEKLERİNDE POTANSİYEL PATOJENLER VE ÇOKLU ANTİBİYOTİK DİRENÇLİLİĞİ: STREPTOCOCCUS SPP. SUŞLARININ DEĞERLENDİRİLMESİ. The Journal of Food. 2023;48(5):952-6.

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