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Investigation on Antimicrobial Resistance Levels of Escherichia coli Strains Isolated from Bovine Fecal Samples and Comparison with Guidelines of the Clinical Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST)

Year 2023, Volume: 16 Issue: 3, 334 - 341, 30.09.2023
https://doi.org/10.30607/kvj.1302078

Abstract

This study was carried out to investigate the antibiotic resistance levels of Escherichia coli isolates of bovine origin and to compare the results with CLSI and EUCAST guideline values. For this purpose, 97 E. coli strains isolated from fecal samples of cattle in 12 different farms were tested against 32 antibiotics by using the disk diffusion method. The zone diameters of 13 antibiotics examined within the scope of the study were compared according to the CLSI and EUCAST 2020 guidelines, and their consistency levels were evaluated statistically. The highest resistance rates in E. coli isolates were determined against tetracycline (68%), streptomycin (63.9%), ampicillin (58.8%), and doxycycline (50.5%) antibiotics. On the other hand, the isolates were found to be highly susceptible to amikacin and cephalosporin group antibiotics. When CLSI and EUCAST guidelines were compared, it was found that there were statistically significant differences between the resistance rates of nitrofurantoin, gentamicin, and amikacin. Only 10 (10.3%) of the isolates were detected to be susceptible to all the antibiotics tested, whereas 17.5% were resistant to 10 or more antibiotics. The results of this study showed that E. coli isolates of bovine origin were highly resistant against antibiotics used in the field for a long period, especially the number of isolates with multiple antibiotic resistance was striking. It was concluded that due to substantial inconsistencies between the CLSI and EUCAST guidelines for some antibiotics such as amikacin, nitrofurantoin, and gentamicin, there is an urgent need to execute necessary updates in both guidelines.

References

  • Aasmäe B, Häkkinen L, Kaart T, Kalmus, P. Antimicrobial resistance of Escherichia coli and Enterococcus spp. isolated from Estonian cattle and swine from 2010 to 2015. Acta Vet Scand. 2019; 61(1):5.
  • Acik, MN, Yurdakul NE, Cakici L, Onat N, Dogan O, Cetinkaya B. traT and CNF2 genes of Escherichia coli isolated from milk of healthy cows and sheep. Res Vet Sci. 2004; 77(1):17-21.
  • Bengtsson-Palme J, Kristiansson E, Larsson, DJ. Environmental factors influencing the development and spread of antibiotic resistance. FEMS Microbiol Rev. 2018;.42(1):fux053.
  • Blake DP, Hillman K, Fenlon DR, Low JC. Transfer of antibiotic resistance between commensal and pathogenic members of the Enterobacteriaceae under ileal conditions. J Appl Microbiol. 2003;. 95(3):428-436.
  • Boireau C, Morignat É, Cazeau G, Jarrige N, Jouy É, Haenni M, Madec, JY, Leblond A, Gay É. Antimicrobial resistance trends in Escherichia coli isolated from diseased food‐producing animals in France: A 14‐year period time‐series study. Zoonoses Public Health. 2018; 65(1):e86-e94.
  • Boyen F, Vangroenweghe F, Butaye P, De Graef E, Castryck F, Heylen P, Vanrobaeys M, Haesebrouck F. Disk prediffusion is a reliable method for testing colistin susceptibility in porcine E. coli strains. Vet Microbiol (2010). 144(3-4):359-362.
  • Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing. 30th ed. CLSI supplement M100. 2020.
  • Dheilly A, Le Devendec L, Mourand G, Bouder A, Jouy E, Kempf I. Resistance gene transfer during treatments for experimental avian colibacillosis. Antimicrob Agents Chemother. 2012; 56(1), 189-196.
  • Kassim A, Omuse G, Premji Z, Revathi G. Comparison of clinical laboratory standards institute and European committee on antimicrobial susceptibility testing guidelines for the interpretation of antibiotic susceptibility at a university teaching hospital in Nairobi, Kenya: a cross-sectional study. Ann Clin Microbiol Antimicrob. 2016; 15(1): 21.
  • Lim SK, Lim KG, Lee HS, Jung SC, Kang MI, Nam HM. Prevalence and molecular characterization of fluoroquinolone-resistant Escherichia coli isolated from diarrheic cattle in Korea. J Vet Med Sci. 2010; 72(5):611-614.
  • Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu LF, Gu D, Ren H, Chen X, Lv L, He D, Zhou H, Liang Z, Liu JH, Shen J. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: A microbiological and molecular biological study. Lancet Infect Dis. 2016; 16(2):161-168.
  • Mammeri H, Van De Loo M, Poirel L, Martinez-Martinez L, Nordmann P. Emergence of plasmid-mediated quinolone resistance in Escherichia coli in Europe. Antimicrob Agents Chemother. 2005; 49(1):71-76.
  • Moniri R, Dastehgoli K. Fluoroquinolone-resistant Escherichia coli isolated from healthy broilers with previous exposure to fluoroquinolones: Is there a link? Microb Ecol Health Dis. 2005; 17(2):69-74.
  • Odonkor ST, Ampofo JK. Escherichia coli as an indicator of bacteriological quality of water: an overview. Microbiol Res. 2013; 4(1):e2-e2.
  • Prestinaci F, Pezzotti P, Pantosti A. Antimicrobial resistance: A global multifaceted phenomenon. Pathog Glob Health. 2015; 109:309-318.
  • Sánchez-Bautista A, Coy J, García-Shimizu P, Rodríguez JC. From CLSI to EUCAST guidelines in the interpretation of antimicrobial susceptibility: What is the effect in our setting? Enferm Infecc Microbiol Clin (English ed.) 2018; 36(4):229-232.
  • Shin SW, Shin MK, Jung M, Belaynehe KM, Yoo HS. Prevalence of antimicrobial resistance and transfer of tetracycline resistance genes in Escherichia coli isolates from beef cattle. Appl Environ Microbiol. 2015; 81(16):5560-5566.
  • Stromberg ZR, Van Goor A, Redweik GA., Wymore Brand MJ, Wannemuehler MJ, Mellata M. Pathogenic and non-pathogenic Escherichia coli colonization and host inflammatory response in a defined microbiota mouse model. Dis Model Mech. 2018;11(11):dmm035063.
  • Tadesse DA, Zhao S, Tong E, Ayers S, Singh A, Bartholomew MJ, McDermott PF. Antimicrobial drug resistance in Escherichia coli from humans and food animals, United States, 1950-2002. Emerging infectious diseases. 2012; 18(5), 741-749.
  • Tchesnokova V, Radey M, Chattopadhyay S, Larson L, Weaver JL, Kisiela D, Sokurenko EV. Pandemic fluoroquinolone resistant Escherichia coli clone ST1193 emerged via simultaneous homologous recombinations in 11 gene loci. Proc Natl Acad Sci. 2019; 116(29):14740-14748.
  • The European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters. Version 10.0, 2020.
  • Van den Bogaard AE, Stobberingh EE. Epidemiology of resistance to antibiotics: Links between animals and humans. Inter J Antimicrob Agents. 2000; 14(4):327-335.
  • Vidovic N, Vidovic S. Antimicrobial resistance and food animals: Influence of livestock environment on the emergence and dissemination of antimicrobial resistance. Antibiotics 2020; 9(2):52.
  • White DG, Hudson C, Maurer JJ, Ayers S, Zhao S, Lee MD, Bolton L, Foley T, Sherwood J. Characterization of chloramphenicol and florfenicol resistance in Escherichia coli associated with bovine diarrhea. Journal of clinical microbiology. 2000; 38(12), 4593–4598.
  • World Health Organization (WHO) 2014. Antimicrobial resistance: global report on surveillance.https://apps.who.int/iris/bitstream/handle/10665/112642/9789241564748 eng.pdf.
  • Yassin AK, Gong J, Kelly P, Lu G, Guardabassi L, Wei L, Han X, Qiu H, Price S, Cheng D, Wang C. Antimicrobial resistance in clinical Escherichia coli isolates from poultry and livestock, China. PLoS One. 2017; 21;12(9):e0185326.

Sığır Dışkı Örneklerinden İzole Edilen Escherichia coli Suşlarının Antimikrobiyal Direnç Düzeylerinin Araştırılması ve Klinik Laboratuvar Standartları Enstitüsü (CLSI) ve Avrupa Antimikrobiyal Duyarlılık Testi Komitesi (EUCAST) Kılavuzlarıyla Karşılaştırılması

Year 2023, Volume: 16 Issue: 3, 334 - 341, 30.09.2023
https://doi.org/10.30607/kvj.1302078

Abstract

Bu çalışma, sığır orijinli Escherichia coli izolatlarının antibiyotik direnç düzeylerinin araştırılması ve sonuçların CLSI ve EUCAST kılavuz değerleri ile karşılaştırılması amacıyla yapılmıştır. Bu amaçla 12 farklı işletmedeki sığırların dışkı örneklerinden izole edilen 97 E. coli suşu, disk difüzyon yöntemi kullanılarak 32 antibiyotiğe karşı test edilmiştir. Çalışma kapsamında incelenen 13 antibiyotiğin zon çapları CLSI ve EUCAST 2020 kılavuzlarına göre karşılaştırıldı ve tutarlılık düzeyleri istatistiksel olarak değerlendirildi. E. coli izolatlarında en yüksek direnç oranları tetrasiklin (%68), streptomisin (%63,9), ampisilin (%58,8) ve doksisiklin (%50,5) antibiyotiklerine karşı saptanmıştır. Öte yandan, izolatların amikasin ve sefalosporin grubu antibiyotiklere karşı yüksek duyarlı olduğu saptanmıştır. CLSI ve EUCAST kılavuzları karşılaştırıldığında nitrofurantoin, gentamisin ve amikasin direnç oranları arasında istatistiksel olarak anlamlı farklar olduğu görüldü. İzolatların sadece 10'unun (%10,3) test edilen tüm antibiyotiklere duyarlı olduğu, %17,5'inin ise 10 ve daha fazla antibiyotiğe dirençli olduğu saptandı. Bu çalışmanın sonuçları sığır orijinli E. coli izolatlarının uzun süredir sahada kullanılan antibiyotiklere karşı oldukça dirençli olduğunu göstermiştir, özellikle çoklu antibiyotik direncine sahip izolatların sayısı dikkat çekicidir. Amikasin, nitrofurantoin ve gentamisin gibi bazı antibiyotikler için CLSI ve EUCAST kılavuzları arasındaki önemli tutarsızlıklar nedeniyle, her iki kılavuzda da gerekli güncellemelerin acilen yapılması gerektiği sonucuna varılmıştır.

References

  • Aasmäe B, Häkkinen L, Kaart T, Kalmus, P. Antimicrobial resistance of Escherichia coli and Enterococcus spp. isolated from Estonian cattle and swine from 2010 to 2015. Acta Vet Scand. 2019; 61(1):5.
  • Acik, MN, Yurdakul NE, Cakici L, Onat N, Dogan O, Cetinkaya B. traT and CNF2 genes of Escherichia coli isolated from milk of healthy cows and sheep. Res Vet Sci. 2004; 77(1):17-21.
  • Bengtsson-Palme J, Kristiansson E, Larsson, DJ. Environmental factors influencing the development and spread of antibiotic resistance. FEMS Microbiol Rev. 2018;.42(1):fux053.
  • Blake DP, Hillman K, Fenlon DR, Low JC. Transfer of antibiotic resistance between commensal and pathogenic members of the Enterobacteriaceae under ileal conditions. J Appl Microbiol. 2003;. 95(3):428-436.
  • Boireau C, Morignat É, Cazeau G, Jarrige N, Jouy É, Haenni M, Madec, JY, Leblond A, Gay É. Antimicrobial resistance trends in Escherichia coli isolated from diseased food‐producing animals in France: A 14‐year period time‐series study. Zoonoses Public Health. 2018; 65(1):e86-e94.
  • Boyen F, Vangroenweghe F, Butaye P, De Graef E, Castryck F, Heylen P, Vanrobaeys M, Haesebrouck F. Disk prediffusion is a reliable method for testing colistin susceptibility in porcine E. coli strains. Vet Microbiol (2010). 144(3-4):359-362.
  • Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing. 30th ed. CLSI supplement M100. 2020.
  • Dheilly A, Le Devendec L, Mourand G, Bouder A, Jouy E, Kempf I. Resistance gene transfer during treatments for experimental avian colibacillosis. Antimicrob Agents Chemother. 2012; 56(1), 189-196.
  • Kassim A, Omuse G, Premji Z, Revathi G. Comparison of clinical laboratory standards institute and European committee on antimicrobial susceptibility testing guidelines for the interpretation of antibiotic susceptibility at a university teaching hospital in Nairobi, Kenya: a cross-sectional study. Ann Clin Microbiol Antimicrob. 2016; 15(1): 21.
  • Lim SK, Lim KG, Lee HS, Jung SC, Kang MI, Nam HM. Prevalence and molecular characterization of fluoroquinolone-resistant Escherichia coli isolated from diarrheic cattle in Korea. J Vet Med Sci. 2010; 72(5):611-614.
  • Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu LF, Gu D, Ren H, Chen X, Lv L, He D, Zhou H, Liang Z, Liu JH, Shen J. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: A microbiological and molecular biological study. Lancet Infect Dis. 2016; 16(2):161-168.
  • Mammeri H, Van De Loo M, Poirel L, Martinez-Martinez L, Nordmann P. Emergence of plasmid-mediated quinolone resistance in Escherichia coli in Europe. Antimicrob Agents Chemother. 2005; 49(1):71-76.
  • Moniri R, Dastehgoli K. Fluoroquinolone-resistant Escherichia coli isolated from healthy broilers with previous exposure to fluoroquinolones: Is there a link? Microb Ecol Health Dis. 2005; 17(2):69-74.
  • Odonkor ST, Ampofo JK. Escherichia coli as an indicator of bacteriological quality of water: an overview. Microbiol Res. 2013; 4(1):e2-e2.
  • Prestinaci F, Pezzotti P, Pantosti A. Antimicrobial resistance: A global multifaceted phenomenon. Pathog Glob Health. 2015; 109:309-318.
  • Sánchez-Bautista A, Coy J, García-Shimizu P, Rodríguez JC. From CLSI to EUCAST guidelines in the interpretation of antimicrobial susceptibility: What is the effect in our setting? Enferm Infecc Microbiol Clin (English ed.) 2018; 36(4):229-232.
  • Shin SW, Shin MK, Jung M, Belaynehe KM, Yoo HS. Prevalence of antimicrobial resistance and transfer of tetracycline resistance genes in Escherichia coli isolates from beef cattle. Appl Environ Microbiol. 2015; 81(16):5560-5566.
  • Stromberg ZR, Van Goor A, Redweik GA., Wymore Brand MJ, Wannemuehler MJ, Mellata M. Pathogenic and non-pathogenic Escherichia coli colonization and host inflammatory response in a defined microbiota mouse model. Dis Model Mech. 2018;11(11):dmm035063.
  • Tadesse DA, Zhao S, Tong E, Ayers S, Singh A, Bartholomew MJ, McDermott PF. Antimicrobial drug resistance in Escherichia coli from humans and food animals, United States, 1950-2002. Emerging infectious diseases. 2012; 18(5), 741-749.
  • Tchesnokova V, Radey M, Chattopadhyay S, Larson L, Weaver JL, Kisiela D, Sokurenko EV. Pandemic fluoroquinolone resistant Escherichia coli clone ST1193 emerged via simultaneous homologous recombinations in 11 gene loci. Proc Natl Acad Sci. 2019; 116(29):14740-14748.
  • The European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters. Version 10.0, 2020.
  • Van den Bogaard AE, Stobberingh EE. Epidemiology of resistance to antibiotics: Links between animals and humans. Inter J Antimicrob Agents. 2000; 14(4):327-335.
  • Vidovic N, Vidovic S. Antimicrobial resistance and food animals: Influence of livestock environment on the emergence and dissemination of antimicrobial resistance. Antibiotics 2020; 9(2):52.
  • White DG, Hudson C, Maurer JJ, Ayers S, Zhao S, Lee MD, Bolton L, Foley T, Sherwood J. Characterization of chloramphenicol and florfenicol resistance in Escherichia coli associated with bovine diarrhea. Journal of clinical microbiology. 2000; 38(12), 4593–4598.
  • World Health Organization (WHO) 2014. Antimicrobial resistance: global report on surveillance.https://apps.who.int/iris/bitstream/handle/10665/112642/9789241564748 eng.pdf.
  • Yassin AK, Gong J, Kelly P, Lu G, Guardabassi L, Wei L, Han X, Qiu H, Price S, Cheng D, Wang C. Antimicrobial resistance in clinical Escherichia coli isolates from poultry and livestock, China. PLoS One. 2017; 21;12(9):e0185326.
There are 26 citations in total.

Details

Primary Language English
Subjects Veterinary Sciences
Journal Section RESEARCH ARTICLE
Authors

Recep Kalın 0000-0002-9173-9550

Burcu Karagülle 0000-0002-6628-4515

Mehmet Nuri Açık 0000-0002-1908-5898

Murat Karahan 0000-0002-7024-1649

Yasin Öztürk This is me 0000-0002-9612-0677

Burhan Çetinkaya 0000-0001-6347-1684

Publication Date September 30, 2023
Acceptance Date September 4, 2023
Published in Issue Year 2023 Volume: 16 Issue: 3

Cite

APA Kalın, R., Karagülle, B., Açık, M. N., Karahan, M., et al. (2023). Investigation on Antimicrobial Resistance Levels of Escherichia coli Strains Isolated from Bovine Fecal Samples and Comparison with Guidelines of the Clinical Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST). Kocatepe Veterinary Journal, 16(3), 334-341. https://doi.org/10.30607/kvj.1302078
AMA Kalın R, Karagülle B, Açık MN, Karahan M, Öztürk Y, Çetinkaya B. Investigation on Antimicrobial Resistance Levels of Escherichia coli Strains Isolated from Bovine Fecal Samples and Comparison with Guidelines of the Clinical Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST). kvj. September 2023;16(3):334-341. doi:10.30607/kvj.1302078
Chicago Kalın, Recep, Burcu Karagülle, Mehmet Nuri Açık, Murat Karahan, Yasin Öztürk, and Burhan Çetinkaya. “Investigation on Antimicrobial Resistance Levels of Escherichia Coli Strains Isolated from Bovine Fecal Samples and Comparison With Guidelines of the Clinical Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST)”. Kocatepe Veterinary Journal 16, no. 3 (September 2023): 334-41. https://doi.org/10.30607/kvj.1302078.
EndNote Kalın R, Karagülle B, Açık MN, Karahan M, Öztürk Y, Çetinkaya B (September 1, 2023) Investigation on Antimicrobial Resistance Levels of Escherichia coli Strains Isolated from Bovine Fecal Samples and Comparison with Guidelines of the Clinical Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST). Kocatepe Veterinary Journal 16 3 334–341.
IEEE R. Kalın, B. Karagülle, M. N. Açık, M. Karahan, Y. Öztürk, and B. Çetinkaya, “Investigation on Antimicrobial Resistance Levels of Escherichia coli Strains Isolated from Bovine Fecal Samples and Comparison with Guidelines of the Clinical Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST)”, kvj, vol. 16, no. 3, pp. 334–341, 2023, doi: 10.30607/kvj.1302078.
ISNAD Kalın, Recep et al. “Investigation on Antimicrobial Resistance Levels of Escherichia Coli Strains Isolated from Bovine Fecal Samples and Comparison With Guidelines of the Clinical Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST)”. Kocatepe Veterinary Journal 16/3 (September 2023), 334-341. https://doi.org/10.30607/kvj.1302078.
JAMA Kalın R, Karagülle B, Açık MN, Karahan M, Öztürk Y, Çetinkaya B. Investigation on Antimicrobial Resistance Levels of Escherichia coli Strains Isolated from Bovine Fecal Samples and Comparison with Guidelines of the Clinical Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST). kvj. 2023;16:334–341.
MLA Kalın, Recep et al. “Investigation on Antimicrobial Resistance Levels of Escherichia Coli Strains Isolated from Bovine Fecal Samples and Comparison With Guidelines of the Clinical Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST)”. Kocatepe Veterinary Journal, vol. 16, no. 3, 2023, pp. 334-41, doi:10.30607/kvj.1302078.
Vancouver Kalın R, Karagülle B, Açık MN, Karahan M, Öztürk Y, Çetinkaya B. Investigation on Antimicrobial Resistance Levels of Escherichia coli Strains Isolated from Bovine Fecal Samples and Comparison with Guidelines of the Clinical Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST). kvj. 2023;16(3):334-41.

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