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Çiftliklerden Alınan İnek Sütlerinde Genişlemiş Spektrumlu Beta-Laktamaz Üreten Escherichia Coli'nin Araştırılması

Year 2025, Volume: 20 Issue: 2, 57 - 63, 27.08.2025
https://doi.org/10.17094/vetsci.1646232

Abstract

Bu çalışma, sığır çiftliği süt karışımlarında genişlemiş spektrumlu beta-laktamaz (ESBL) üreten Escherichia coli'nin varlığını araştırmak amacıyla yapıldı. Burdur ili Gölhisar ilçesindeki 32 çiftlikten alınan 32 çiftlik sütü, 2 μg/ml sefotaksim veya 2 μg/ml seftazidim ilave edilmiş MacConkey agar besi yerlerine eş zamanlı olarak ekildi. Aerobik şartlarda 37°C'de 24 saat inkübasyonun ardından, kültürlerde E. coli'nin tanımlanması amacıyla laktoz pozitif kolonilere biyokimyasal/fizyolojik testler uygulandı. Daha sonra E. coli izolatında ESBL üretiminin tespiti kombine disk yöntemiyle yapıldı. ESBL sınıfını belirlemek amacıyla, izolatlarda CTX-M, SHV ve TEM genleri polimeraz zincir reaksiyonu (PZR) yöntemiyle tarandı. Süt örneklerinden selektif kültür yapıldıktan sonra 1 adet (1/32, %3,12) E. coli izole edildi. Kombine disk yöntemiyle ESBL ürettiği doğrulanan izolatın CTX-M grup 1 sınıf ESBL genini taşıdığı, TEM ve SHV sınıflarına sahip olmadığı belirlendi. Bu çalışma, bölgedeki sığır işletmelerinin çiftlik sütlerinde ESBL üreten E. coli'nin düşük düzeyde bulunabileceğini göstermiştir. Bu çalışmada bir çiftlikten elde edilen çiftlik sütü karışımında tespit edilen ESBL üreten E. coli izolatının kaynağı araştırılmamış olsa da, tüketilecek sütte bu bakterinin tespit edilmiş olması önemlidir.

Ethical Statement

Bu çalışma Mehmet Akif Ersoy Üniversitesi Hayvan Deneyleri Yerel Etik Kurulu tarafından onaylandı (Tarih: 02.10.2024; Karar numarası:1373).

Project Number

Bu araştırma bir projeden destek alınmadan gerçekleştirilmiştir.

References

  • 1. Castanheira M, Simner PJ, Bradford PA. Extended-spectrum β-lactamases: an update on their characteristics, epidemiology and detection. JAC-Antimicrob Resist. 2021;3(3):vdlab092.
  • 2. Bezabih YM, Sabiiti W, Alamneh E, et al. The global prevalence and trend of human intestinal carriage of ESBL-producing Escherichia coli in the community. J Antimicrob Chemother. 2021;76:22-29.
  • 3. Palmeira JD, Ferreira HMN. Extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in cattle production-A threat around the world. Heliyon. 2020;6:e03206.
  • 4. Rhouma M, Soufi L, Cenatus S, et al. Current insights regarding the role of farm animals in the spread of antimicrobial resistance from a one health perspective. Vet Sci. 2022;9(9):480.
  • 5. Ur Rahman S, Ali T, Ali I, et al. The growing genetic and functional diversity of extended spectrum beta‐lactamases. Bio Med Res Int. 2018;9519718.
  • 6. Bevan ER, Jones AM, Hawkey PM. Global epidemiology of CTX-M β-lactamases: Temporal and geographical shifts in genotype, J Antimicrob Chemother. 2017;72(8):2145-2155.
  • 7. Kucukbasmaci O, Ciftcioglu G, Midilli K, et al. Detection of extended spectrum Beta-Lactamase producing Enterobacteriaceae from food animals in Turkey. Revue de Médecine Vétérinaire. 2008;159:586-597.
  • 8. Pehlivanoglu F, Turutoglu H, Ozturk D, et al. Molecular characterization of ESBL-producing Escherichia coli isolated from healthy cattle and sheep. Acta Vet-Beo. 2016;66(4):520-533.
  • 9. Aslantaş Ö, Elmacıoğlu S, Yılmaz EŞ. Prevalence and characterization of ESBL- and AmpC-producing Escherichia coli from cattle. Kafkas Univ Vet Fak Derg. 2017;23:63-67.
  • 10. Yıldırım D, Pehlivanoglu F. Carriage of extended spectrum beta lactamase producing Escherichia coli in calves. F U Sağlık Bilimleri Veteriner Dergisi. 2018;32(3):155-160.
  • 11. Özpınar H, Tekiner İH, Sarıcı B, et al. Phenotypic characterization of ESBL-and AmpC-type beta lactamases in Enterobacteriaceae from chicken meat and dairy products. Ankara Üniv Vet Fak Derg. 2017;64:267-272.
  • 12. Tepeli SÖ, Zorba NND. Frequency of extended-spectrum β-lactamase (ESBL)–and AmpC β-lactamase–producing Enterobacteriaceae in a cheese production process. J Dairy Sci. 2018;101(4):2906-2914.
  • 13. Kürekci C, Osek J, Aydın M, et al. Evaluation of bulk tank raw milk and raw chicken meat samples as source of ESBL-producing Escherichia coli in Turkey: Recent insights. J Food Saf. 2019;39:e12605.
  • 14. Tepeli SÖ, Zorba M, Yalman M, et al. Microbiological and physicochemical properties of farm bulk tank milk and antimicrobial resistance of its dominant bacteria. J Food Saf. 2023;43(1):e13022.
  • 15. Turkish Ministry of Industry and Technology. Accessed September 24, 2024. www.baka.gov.tr
  • 16.Turkish Ministry of Agriculture and Forestry. Accessed September 24, 2024. www.burdur.tarımorman.gov.tr.
  • 17. Winn W, Allen S, Janda W, et al. Koneman’s color atlas and textbook of diagnostic microbiology. 6th ed. Philadelphia: Lippincott Williams and Wilkins; 2006.
  • 18. CLSI. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. 7th ed. CLSI supplement VET01S. Clinical and Laboratory Standards Institute; 2024.
  • 19. Heffernan HM, Woodhouse RE, Pope CE, et al. Prevalence and types of extended-spectrum betalactamases among urinary Escherichia coli and Klebsiella spp. in New Zealand. Int J Antimicrob Agents. 2009;34:544-549.
  • 20. Tenover FC, Rasheed JK. Detection of antimicrobial resistance genes and mutations associated with antimicrobial resistance in microorganisms. In: Persing DH, Tenover FC, Versalovic J, Tang Y-W, Unger ER, Relman DA, White TF, eds. Molecular Microbiology: Diagnostic Principles and Practice. Washington DC: ASM Publishing; 2004:391-406.
  • 21. Arpin C, Dubois V, Coulange L, et al. Extended spectrum beta-lactamase-producing Enterobacteriaceae in community and private health care centers. Antimicrob Agents Chemother. 2003;47:3506-3514.
  • 22. Saladin M, Cao VTB, Lambert T, et al. Diversity of CTX-M ß-lactamases and their promoter regions from Enterobacteriaceae isolated in three Parisian hospitals. FEMS Microbiol Lett. 2002;209:161-168.
  • 23. Jeong SH, Bae IK, Know SB, et al. Dissemination of transferable CTX-M-type extended-spectrum Beta-lactamase-producing E. coli in Korea. J Appl Microbiol. 2005;98(4):921-927.
  • 24. CLSI. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals. 7th ed. CLSI supplement VET01S. Clinical and Laboratory Standards Institute, 2024.
  • 25. CLSI. Performance Standards for Antimicrobial Susceptibility Testing. 34th ed. CLSI supplement M100. Clinical and Laboratory Standards Institute, 2024.
  • 26. Geser N, Stephan R, Hachler H. Occurrence and characteristics of extended-spectrum beta-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Vet Res. 2012;8:21.
  • 27. Vásquez L, Ramírez NF, Akineden Ö, et al. Presence of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in bulk-tank milk of bovine dairy farms in Antioquia, Colombia. Rev Colomb Cienc Pecu. 2017;30:85-100.
  • 28. Devi LS, Broor S, Rautela RS, et al. Increasing prevalence of Escherichia coli andKlebsiella pneumoniae producing CTX-M-type extended-spectrum beta-lactamase, carbapenemase, and NDM-1 in patients from a rural community with community acquired infections: A 3-year study. Int J Appl Basic Med Res. 2020;10(3):156-163.
  • 29. Helldal L, Karami N, Floren K, et al. Shift of CTX‐M genotypes has determined the increased prevalence of extended‐spectrum β‐lactamase‐producing Escherichia coli in south‐western Sweden. Clin Microbiol Infect. 2013;19(2):E87-E90.
  • 30. Park N, In Hur J, Lee S, et al. Prevalence of CTX-M types among ESBL-producing pathogenic Escherichia coli isolates from foodborne diarrheal patients in Gyeonggi-do, South Korea. Food Sci Biotechnol. 2024;33:2825-2833.
  • 31. Mandujano-Hernández A, Martínez-Vázquez AV, Paz-González AD, et al. The global rise of ESBL-producing Escherichia coli in the livestock sector: A five-year overview. Animals (Basel). 2024;14(17):2490.
  • 32. Wang J, Stephan R, Power K, et al. Nucleotide sequences of 16 transmissible plasmids identified in nine multidrug-resistant Escherichia coli isolates expressing an ESBL phenotype isolated from food-producing animals and healthy humans. J Antimicrob Chemother. 2014;69(10):2658-2668.
  • 33. Rozwandowicz M, Brouwer MSM, Fischer J, et al. Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. J Antimicrob Chemother. 2018;73(5):1121-1137.
  • 34. Tseng CH, Liu CW, Liu PY. Extended-spectrum β-lactamases (ESBL) producing bacteria in animals. Antibiotics (Basel). 2023;12(4):661.
  • 35. Carattoli A. Animal reservoirs for extended spectrum β-lactamase producers. Clin Microbiol Infect. 2018;14:117-123.

Investigation of Extended-Spectrum Beta-Lactamase Producing Escherichia Coli in Milk on Dairy Cattle Farm

Year 2025, Volume: 20 Issue: 2, 57 - 63, 27.08.2025
https://doi.org/10.17094/vetsci.1646232

Abstract

The present study was conducted to investigate the presence of extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli (E. coli) in cattle farm milk mixtures. Thirty two farm milks from 32 farms in Gölhisar district of Burdur city (Türkiye) were concurrently cultured on MacConkey agar plates supplemented with either 2 μg/mL cefotaxime or 2 μg/mL ceftazidime. After incubation at 37°C for 24 h under aerobic conditions, biochemical/physiological tests were applied to the lactose positive colonies for identification of E. coli in the cultures. Subsequently, determination of ESBL production in E. coli isolate was done by the combined disk method. In order to determine the ESBL class, the isolates were screened for CTX-M, SHV and TEM genes by polymerase chain reaction (PCR). After the selective culture of the milk samples, one (1/32, 3.12%) E. coli was isolated. The isolate confirmed as an ESBL procedure by the combined disc method harbored the CTX-M group 1 ESBL gene, but tested negative for TEM and SHV genes. This study showed that ESBL-producing E. coli could be found at low level in farm milks of the cattle farms in the region. Although the source of the ESBL-producing E. coli isolated from the farm milk mixture was not identified in this study, it is important that this bacterium was detected in the milk to be consumed.

Ethical Statement

This study was approved by the Mehmet Akif Ersoy University Animal Experiments Local Ethics Committee (Date: 02.10.2024; decision number:1373).

Project Number

Bu araştırma bir projeden destek alınmadan gerçekleştirilmiştir.

References

  • 1. Castanheira M, Simner PJ, Bradford PA. Extended-spectrum β-lactamases: an update on their characteristics, epidemiology and detection. JAC-Antimicrob Resist. 2021;3(3):vdlab092.
  • 2. Bezabih YM, Sabiiti W, Alamneh E, et al. The global prevalence and trend of human intestinal carriage of ESBL-producing Escherichia coli in the community. J Antimicrob Chemother. 2021;76:22-29.
  • 3. Palmeira JD, Ferreira HMN. Extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in cattle production-A threat around the world. Heliyon. 2020;6:e03206.
  • 4. Rhouma M, Soufi L, Cenatus S, et al. Current insights regarding the role of farm animals in the spread of antimicrobial resistance from a one health perspective. Vet Sci. 2022;9(9):480.
  • 5. Ur Rahman S, Ali T, Ali I, et al. The growing genetic and functional diversity of extended spectrum beta‐lactamases. Bio Med Res Int. 2018;9519718.
  • 6. Bevan ER, Jones AM, Hawkey PM. Global epidemiology of CTX-M β-lactamases: Temporal and geographical shifts in genotype, J Antimicrob Chemother. 2017;72(8):2145-2155.
  • 7. Kucukbasmaci O, Ciftcioglu G, Midilli K, et al. Detection of extended spectrum Beta-Lactamase producing Enterobacteriaceae from food animals in Turkey. Revue de Médecine Vétérinaire. 2008;159:586-597.
  • 8. Pehlivanoglu F, Turutoglu H, Ozturk D, et al. Molecular characterization of ESBL-producing Escherichia coli isolated from healthy cattle and sheep. Acta Vet-Beo. 2016;66(4):520-533.
  • 9. Aslantaş Ö, Elmacıoğlu S, Yılmaz EŞ. Prevalence and characterization of ESBL- and AmpC-producing Escherichia coli from cattle. Kafkas Univ Vet Fak Derg. 2017;23:63-67.
  • 10. Yıldırım D, Pehlivanoglu F. Carriage of extended spectrum beta lactamase producing Escherichia coli in calves. F U Sağlık Bilimleri Veteriner Dergisi. 2018;32(3):155-160.
  • 11. Özpınar H, Tekiner İH, Sarıcı B, et al. Phenotypic characterization of ESBL-and AmpC-type beta lactamases in Enterobacteriaceae from chicken meat and dairy products. Ankara Üniv Vet Fak Derg. 2017;64:267-272.
  • 12. Tepeli SÖ, Zorba NND. Frequency of extended-spectrum β-lactamase (ESBL)–and AmpC β-lactamase–producing Enterobacteriaceae in a cheese production process. J Dairy Sci. 2018;101(4):2906-2914.
  • 13. Kürekci C, Osek J, Aydın M, et al. Evaluation of bulk tank raw milk and raw chicken meat samples as source of ESBL-producing Escherichia coli in Turkey: Recent insights. J Food Saf. 2019;39:e12605.
  • 14. Tepeli SÖ, Zorba M, Yalman M, et al. Microbiological and physicochemical properties of farm bulk tank milk and antimicrobial resistance of its dominant bacteria. J Food Saf. 2023;43(1):e13022.
  • 15. Turkish Ministry of Industry and Technology. Accessed September 24, 2024. www.baka.gov.tr
  • 16.Turkish Ministry of Agriculture and Forestry. Accessed September 24, 2024. www.burdur.tarımorman.gov.tr.
  • 17. Winn W, Allen S, Janda W, et al. Koneman’s color atlas and textbook of diagnostic microbiology. 6th ed. Philadelphia: Lippincott Williams and Wilkins; 2006.
  • 18. CLSI. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. 7th ed. CLSI supplement VET01S. Clinical and Laboratory Standards Institute; 2024.
  • 19. Heffernan HM, Woodhouse RE, Pope CE, et al. Prevalence and types of extended-spectrum betalactamases among urinary Escherichia coli and Klebsiella spp. in New Zealand. Int J Antimicrob Agents. 2009;34:544-549.
  • 20. Tenover FC, Rasheed JK. Detection of antimicrobial resistance genes and mutations associated with antimicrobial resistance in microorganisms. In: Persing DH, Tenover FC, Versalovic J, Tang Y-W, Unger ER, Relman DA, White TF, eds. Molecular Microbiology: Diagnostic Principles and Practice. Washington DC: ASM Publishing; 2004:391-406.
  • 21. Arpin C, Dubois V, Coulange L, et al. Extended spectrum beta-lactamase-producing Enterobacteriaceae in community and private health care centers. Antimicrob Agents Chemother. 2003;47:3506-3514.
  • 22. Saladin M, Cao VTB, Lambert T, et al. Diversity of CTX-M ß-lactamases and their promoter regions from Enterobacteriaceae isolated in three Parisian hospitals. FEMS Microbiol Lett. 2002;209:161-168.
  • 23. Jeong SH, Bae IK, Know SB, et al. Dissemination of transferable CTX-M-type extended-spectrum Beta-lactamase-producing E. coli in Korea. J Appl Microbiol. 2005;98(4):921-927.
  • 24. CLSI. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals. 7th ed. CLSI supplement VET01S. Clinical and Laboratory Standards Institute, 2024.
  • 25. CLSI. Performance Standards for Antimicrobial Susceptibility Testing. 34th ed. CLSI supplement M100. Clinical and Laboratory Standards Institute, 2024.
  • 26. Geser N, Stephan R, Hachler H. Occurrence and characteristics of extended-spectrum beta-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Vet Res. 2012;8:21.
  • 27. Vásquez L, Ramírez NF, Akineden Ö, et al. Presence of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in bulk-tank milk of bovine dairy farms in Antioquia, Colombia. Rev Colomb Cienc Pecu. 2017;30:85-100.
  • 28. Devi LS, Broor S, Rautela RS, et al. Increasing prevalence of Escherichia coli andKlebsiella pneumoniae producing CTX-M-type extended-spectrum beta-lactamase, carbapenemase, and NDM-1 in patients from a rural community with community acquired infections: A 3-year study. Int J Appl Basic Med Res. 2020;10(3):156-163.
  • 29. Helldal L, Karami N, Floren K, et al. Shift of CTX‐M genotypes has determined the increased prevalence of extended‐spectrum β‐lactamase‐producing Escherichia coli in south‐western Sweden. Clin Microbiol Infect. 2013;19(2):E87-E90.
  • 30. Park N, In Hur J, Lee S, et al. Prevalence of CTX-M types among ESBL-producing pathogenic Escherichia coli isolates from foodborne diarrheal patients in Gyeonggi-do, South Korea. Food Sci Biotechnol. 2024;33:2825-2833.
  • 31. Mandujano-Hernández A, Martínez-Vázquez AV, Paz-González AD, et al. The global rise of ESBL-producing Escherichia coli in the livestock sector: A five-year overview. Animals (Basel). 2024;14(17):2490.
  • 32. Wang J, Stephan R, Power K, et al. Nucleotide sequences of 16 transmissible plasmids identified in nine multidrug-resistant Escherichia coli isolates expressing an ESBL phenotype isolated from food-producing animals and healthy humans. J Antimicrob Chemother. 2014;69(10):2658-2668.
  • 33. Rozwandowicz M, Brouwer MSM, Fischer J, et al. Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. J Antimicrob Chemother. 2018;73(5):1121-1137.
  • 34. Tseng CH, Liu CW, Liu PY. Extended-spectrum β-lactamases (ESBL) producing bacteria in animals. Antibiotics (Basel). 2023;12(4):661.
  • 35. Carattoli A. Animal reservoirs for extended spectrum β-lactamase producers. Clin Microbiol Infect. 2018;14:117-123.
There are 35 citations in total.

Details

Primary Language English
Subjects Veterinary Food Hygiene and Technology, Veterinary Microbiology
Journal Section Research Articles
Authors

Sümeyye Kübra Gücüöz This is me 0009-0006-9854-4525

Faruk Pehlivanoğlu 0000-0001-9358-8007

Project Number Bu araştırma bir projeden destek alınmadan gerçekleştirilmiştir.
Publication Date August 27, 2025
Submission Date February 24, 2025
Acceptance Date May 26, 2025
Published in Issue Year 2025 Volume: 20 Issue: 2

Cite

APA Gücüöz, S. K., & Pehlivanoğlu, F. (2025). Investigation of Extended-Spectrum Beta-Lactamase Producing Escherichia Coli in Milk on Dairy Cattle Farm. Veterinary Sciences and Practices, 20(2), 57-63. https://doi.org/10.17094/vetsci.1646232
AMA Gücüöz SK, Pehlivanoğlu F. Investigation of Extended-Spectrum Beta-Lactamase Producing Escherichia Coli in Milk on Dairy Cattle Farm. Veterinary Sciences and Practices. August 2025;20(2):57-63. doi:10.17094/vetsci.1646232
Chicago Gücüöz, Sümeyye Kübra, and Faruk Pehlivanoğlu. “Investigation of Extended-Spectrum Beta-Lactamase Producing Escherichia Coli in Milk on Dairy Cattle Farm”. Veterinary Sciences and Practices 20, no. 2 (August 2025): 57-63. https://doi.org/10.17094/vetsci.1646232.
EndNote Gücüöz SK, Pehlivanoğlu F (August 1, 2025) Investigation of Extended-Spectrum Beta-Lactamase Producing Escherichia Coli in Milk on Dairy Cattle Farm. Veterinary Sciences and Practices 20 2 57–63.
IEEE S. K. Gücüöz and F. Pehlivanoğlu, “Investigation of Extended-Spectrum Beta-Lactamase Producing Escherichia Coli in Milk on Dairy Cattle Farm”, Veterinary Sciences and Practices, vol. 20, no. 2, pp. 57–63, 2025, doi: 10.17094/vetsci.1646232.
ISNAD Gücüöz, Sümeyye Kübra - Pehlivanoğlu, Faruk. “Investigation of Extended-Spectrum Beta-Lactamase Producing Escherichia Coli in Milk on Dairy Cattle Farm”. Veterinary Sciences and Practices 20/2 (August2025), 57-63. https://doi.org/10.17094/vetsci.1646232.
JAMA Gücüöz SK, Pehlivanoğlu F. Investigation of Extended-Spectrum Beta-Lactamase Producing Escherichia Coli in Milk on Dairy Cattle Farm. Veterinary Sciences and Practices. 2025;20:57–63.
MLA Gücüöz, Sümeyye Kübra and Faruk Pehlivanoğlu. “Investigation of Extended-Spectrum Beta-Lactamase Producing Escherichia Coli in Milk on Dairy Cattle Farm”. Veterinary Sciences and Practices, vol. 20, no. 2, 2025, pp. 57-63, doi:10.17094/vetsci.1646232.
Vancouver Gücüöz SK, Pehlivanoğlu F. Investigation of Extended-Spectrum Beta-Lactamase Producing Escherichia Coli in Milk on Dairy Cattle Farm. Veterinary Sciences and Practices. 2025;20(2):57-63.

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