Presence and antimicrobial resistance of ESBL Escherichia coli from fecal samples of dairy cattle in northern Ecuador

Main Article Content

Pamela Carolina Calvopiña Montenegro
Diana Sofía de Janon González
José Luis Medina Santana
Javier Vargas-Estrella
Lenin Ron-Garrido
Freddy Proaño-Pérez
Christian Vinueza-Burgos

Abstract

Escherichia coli causes colibacillosis in farm animals that act as reservoirs for pathogenic strains. Antimicrobial resistance of E. coli producing Extended Spectrum Beta-lactamases [ESBL] is a serious public health problem that can be attributed to factors related to food consumption and contact with domestic animals. This study aimed to determine the presence and patterns of antimicrobial resistance of ESBL E. coli isolated from fecal samples from dairy cattle in the Pichincha province. A total of 182 bovine feces samples were analyzed, 112 samples from cattle slaughtered at the official slaughterhouse in Quito-Pichincha province, and 70 samples from the collection of the Foodborne Diseases and Antimicrobial Resistance Research Unit [UNIETAR]. The isolation of ESBL E. coli, biochemical identification, and resistance tests using the main antibiotics were carried out at UNIETAR. It was possible to identify 93 positive samples for ESBL E. coli (51%), phenotypic analysis revealed that antibiotics such as amoxicillin plus clavulanic acid, cefepime, ceftazidime, ciprofloxacin, amikacin, tetracycline, presented resistance higher than 80%. Furthermore, low resistance to nitrofurantoin, cefoxitin, and ertapenem was observed, while no isolate was resistant to tigecycline. One hundred percent of the isolates presented multi-resistance phenotypes, with the most frequent pattern being composed of 7 families of antibiotics. In conclusion, these results suggest that E. coli from dairy cattle origin could be an important reservoir of ESBL genes.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

Article Details

How to Cite
Calvopiña Montenegro, P. C., de Janon González, D. S., Medina Santana, J. L., Vargas-Estrella, J., Ron-Garrido, L., Proaño-Pérez, F., & Vinueza-Burgos, C. (2024). Presence and antimicrobial resistance of ESBL Escherichia coli from fecal samples of dairy cattle in northern Ecuador. Siembra, 11(2), e6542. https://doi.org/10.29166/siembra.v11i2.6542
Section
Original article
Author Biographies

Diana Sofía de Janon González, Universidad Central del Ecuador, Facultad de Medicina Veterinaria y Zootecnia, UNIETAR. Jerónimo Leyton y Gato Sobral. 170521. Quito, Pichincha, Ecuador

https://orcid.org/0000-0003-4771-5663

José Luis Medina Santana, Universidad Central del Ecuador, Facultad de Medicina Veterinaria y Zootecnia, UNIETAR. Jerónimo Leyton y Gato Sobral. 170521. Quito, Pichincha, Ecuador

https://orcid.org/0000-0003-4410-0524

Javier Vargas-Estrella, Universidad Central del Ecuador, Facultad de Medicina Veterinaria y Zootecnia. Jerónimo Leyton y Gato Sobral. 170521. Quito, Pichincha, Ecuador

https://orcid.org/0000-0002-0016-0886

Lenin Ron-Garrido, Universidad Central del Ecuador, Facultad de Medicina Veterinaria y Zootecnia. Jerónimo Leyton y Gato Sobral. 170521. Quito, Pichincha, Ecuador

https://orcid.org/0000-0001-9021-4376

Freddy Proaño-Pérez, Universidad Central del Ecuador, Facultad de Medicina Veterinaria y Zootecnia. Jerónimo Leyton y Gato Sobral. 170521. Quito, Pichincha, Ecuador

https://orcid.org/0000-0002-3392-327X

Christian Vinueza-Burgos, Universidad Central del Ecuador, Facultad de Medicina Veterinaria y Zootecnia, UNIETAR. Jerónimo Leyton y Gato Sobral. 170521. Quito, Pichincha, Ecuador

https://orcid.org/0000-0002-4893-502X

References

Akova, M. (2016). Epidemiology of antimicrobial resistance in bloodstream infections. Virulence, 7(3), 252-266. https://doi.org/10.1080/21505594.2016.1159366

Alonso, C. A., Zarazaga, M., Ben Sallem, R., Jouini, A., Ben Slama, K., y Torres, C. (2017). Antibiotic resistance in Escherichia coli in husbandry animals: the African perspective. Letters in Applied Microbiology, 64(5), 318–334. https://doi.org/10.1111/lam.12724

Amancha, G., Celis, Y., Irazabal, J., Falconi, M., Villacis, K., Thekkur, P., Nair, D., Perez, F., y Verdonck, K. (2023). High levels of antimicrobial resistance in Escherichia coli and Salmonella from poultry in Ecuador. Revista Panamericana de Salud Publica, 47, e15. https://doi.org/10.26633/RPSP.2023.15

Bélanger, L., Garenaux, A., Harel, J., Boulianne, M., Nadeau, E., y Dozois, C. M. (2011). Escherichia coli from animal reservoirs as a potential source of human extraintestinal pathogenic E. coli. FEMS Immunology & Medical Microbiology, 62(1), 1-10. https://doi.org/10.1111/j.1574-695X.2011.00797.x

Benavides, J. A., Salgado-Caxito, M., Opazo-Capurro, A., González Muñoz, P., Piñeiro, A., Otto Medina, M., Rivas, L., Munita, J., y Millán, J. (2021). ESBL-producing Escherichia coli carrying CTX-M genes circulating among livestock, dogs, and wild mammals in small-scale farms of central Chile. Antibiotics, 10(5), 510. https://doi.org/10.3390/antibiotics10050510

Castanheira, M., Simner, P. J., y Bradford, P. A. (2021). Extended-spectrum β-lactamases: An update on their characteristics, epidemiology and detection. JAC-Antimicrobial Resistance, 3(3), dlab092. https://doi.org/10.1093/jacamr/dlab092

Cebeci, T. (2022). Prevalence, characterization, and PFGE profiles of multidrug-resistant, extended-spectrum β-lactamase-producing Escherichia coli strains in animal derived foods from public markets in eastern Turkey. Journal of the Hellenic Veterinary Medical Society, 73(3), 4633-4644. https://doi.org/10.12681/jhvms.29251

Chong, Y., Shimoda, S., y Shimono, N. (2018). Current epidemiology, genetic evolution and clinical impact of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae. Infection, Genetics and Evolution, 61, 185-188. https://doi.org/10.1016/j.meegid.2018.04.005

Clinical and Laboratory Standards Institute [CLSI]. (2023). M100-Performance Standards for Antimicrobial Susceptibility Testing (33a ed.). CLSI. https://clsi.org/standards/products/microbiology/documents/m100/

Cota-Rubio, E., Hurtado, L., Pérez-Morales, E., y Alcantara, L. (2014). Resistencia a antibióticos de cepas bacterianas aisladas de animales destinados al consumo humano: Revisión sistemática. Revista Iberoamericana de Ciencias, 1(1), 75-85. http://reibci.org/publicados/2014/mayo/4569156.pdf

Dantas Palmeira, J., y Ferreira, H. M. N. (2020). Extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in cattle production – a threat around the world. Heliyon, 6(1), e03206. https://doi.org/10.1016/j.heliyon.2020.e03206

Doi, Y., Iovleva, A., y Bonomo, R. A. (2017). The ecology of extended-spectrum β-lactamases (ESBLs) in the developed world. Journal of Travel Medicine, 24(1), S44-S51. https://doi.org/10.1093/jtm/taw102

Dong, L., Meng, L., Liu, H., Wu, H., Schroyen, M., Zheng, N., y Wang, J. (2022). Effect of cephalosporin treatment on the microbiota and antibiotic resistance genes in feces of dairy cows with clinical mastitis. Antibiotics, 11(1), 117. https://doi.org/10.3390/antibiotics11010117

Dorado-García, A., Mevius, D. J., Jacobs, J. J. H., Van Geijlswijk, I. M., Mouton, J. W., Wagenaar, J. A., y Heederik, D. J. (2016). Quantitative assessment of antimicrobial resistance in livestock during the course of a nationwide antimicrobial use reduction in the Netherlands. Journal of Antimicrobial Chemotherapy, 71(12), 3607-3619. https://doi.org/10.1093/jac/dkw308

Dorado-García, A., Smid, J. H., van Pelt, W., Bonten, M. J. M., Fluit, A. C., van den Bunt, G., Wagenaar, J. A., Hordijk, J., Dierikx, C. M., Veldman, K. T., de Koeijer, A., Dohmen, W., Schmitt, H., Liakopoulos, A., Pacholewicz, E., Lam, T. J. G. M., Velthuis, A. G., Heuvelink, A., Gonggrijp, M. A., y Heederik, D. J. J. (2018). Molecular relatedness of ESBL/AmpC-producing Escherichia coli from humans, animals, food and the environment: A pooled analysis. Journal of Antimicrobial Chemotherapy, 73(2), 339-347. https://doi.org/10.1093/jac/dkx397

Egervärn, M., Börjesson, S., Byfors, S., Finn, M., Kaipe, C., Englund, S., y Lindblad, M. (2014). Escherichia coli with extended-spectrum beta-lactamases or transferable AmpC beta-lactamases and Salmonella on meat imported into Sweden. International Journal of Food Microbiology, 171, 8-14. https://doi.org/10.1016/j.ijfoodmicro.2013.11.005

European Commission. (2005). Ban on antibiotics as growth promoters in animal feed enters into effect. https://ec.europa.eu/commission/presscorner/detail/en/IP_05_1687

European Food Safety Authority [EFSA], y European Centre for Disease Prevention and Control [ECDC]. (2023). The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2020/2021. EFSA Journal, 21(3), 7867. https://doi.org/10.2903/j.efsa.2023.7867

Genovese, C., La Fauci, V., D’Amato, S., Squeri, A., Anzalone, C., Costa, G. B., Fedele, F., y Squeri, R. (2020). Molecular epidemiology of antimicrobial resistant microorganisms in the 21th century: A review of the literature. Acta Biomedica, 91(2), 256-273. https://doi.org/10.23750/abm.v91i2.9176

Hesp, A., Veldman, K., van der Goot, J., Mevius, D., y van Schaik, G. (2019). Monitoring antimicrobial resistance trends in commensal escherichia coli from livestock, the Netherlands, 1998 to 2016. Eurosurveillance, 24(25), 1800438. https://doi.org/10.2807/1560-7917.ES.2019.24.25.1800438

Instituto Nacional de Investigación en Salud Pública [INSPI]. (2018). Reporte de datos de resistencia a los antimicrobianos en Ecuador 2014-2018. Ministerio de Salud Pública. https://www.salud.gob.ec/wp-content/uploads/2019/08/gaceta_ram2018.pdf

Jácome Mora, J. C. (2022). Prevalencia de agentes bacterianos resistentes a antibióticos en mastitis bovina de ganaderías lecheras del cantón Antonio Ante. Universidad Técnica del Norte. http://repositorio.utn.edu.ec/handle/123456789/11957

Jalil, A., Gul, S., Bhatti, M. F., Siddiqui, M. F., y Adnan, F. (2023). High occurrence of multidrug-resistant Escherichia coli strains in bovine fecal samples from healthy cows serves as rich reservoir for AMR transmission. Antibiotics, 12(1), 37. https://doi.org/10.3390/antibiotics12010037

Kaesbohrer, A., Bakran-Lebl, K., Irrgang, A., Fischer, J., Kämpf, P., Schiffmann, A., Werckenthin, C., Busch, M., Kreienbrock, L., y Hille, K. (2019). Diversity in prevalence and characteristics of ESBL/pAmpC producing E. coli in food in Germany. Veterinary Microbiology, 233, 52-60. https://doi.org/10.1016/j.vetmic.2019.03.025

Lee, S., Teng, L., DiLorenzo, N., Weppelmann, T. A., y Jeong, K. C. (2020). Prevalence and molecular characteristics of extended-spectrum and AmpC β-Lactamase producing Escherichia coli in grazing beef cattle. Frontiers in Microbiology, 10, 3076. https://doi.org/10.3389/fmicb.2019.03076

Liu, Z., Wang, K., Zhang, Y., Xia, L., Zhao, L., Guo, C., Liu, X., Qin, L., y Hao, Z. (2022). High prevalence and diversity characteristics of bla NDM, mcr, and bla ESBLs harboring multidrug-resistant Escherichia coli from chicken, pig, and cattle in China. Frontiers in Cellular and Infection Microbiology, 11, 755545. https://doi.org/10.3389/fcimb.2021.755545

Martínez, E. P., Golding, S. E., van Rosmalen, J., Vinueza-Burgos, C., Verbon, A., y van Schaik, G. (2023). Antibiotic prescription patterns and non-clinical factors influencing antibiotic use by Ecuadorian veterinarians working on cattle and poultry farms: A cross-sectional study. Preventive Veterinary Medicine, 213, 105858. https://doi.org/10.1016/j.prevetmed.2023.105858

Martínez-Vázquez, A. V., Vázquez-Villanueva, J., Leyva-Zapata, L. M., Barrios-García, H., Rivera, G., y Bocanegra-García, V. (2021). Multidrug resistance of Escherichia coli strains isolated from bovine feces and carcasses in Northeast Mexico. Frontiers in Veterinary Science, 8, 643802. https://doi.org/10.3389/fvets.2021.643802

McVey, D. S., Kennedy, M., Chengappa, M. M., y Wilkes, R. P. (eds.). (2022). Veterinary Microbiology (4a ed.). Wiley. https://doi.org/10.1002/9781119650836

Mueller, M., y Tainter, C. R. (2023). Escherichia coli Infection. StatPearls. https://www.ncbi.nlm.nih.gov/books/NBK564298/

Oliver, S. P., y Murinda, S. E. (2012). Antimicrobial resistance of mastitis pathogens. Veterinary Clinics of North America: Food Animal Practice, 28(2), 165-185. https://doi.org/10.1016/j.cvfa.2012.03.005

Öney, M., Karadag, M. A., y Kaya, D. (2023). Efficacy of an internal teat sealant alone or in combination with an intramammary antibiotic during the dry period treatment in dairy cows. Medycyna Weterynaryjna, 79(2), 72-76. https://doi.org/10.21521/mw.6735

Organización Mundial de Sanidad Animal [OMSA]. (2021). Lista de agentes antimicrobianos importantes para la medicina veterinaria. OMSA. https://www.woah.org/app/uploads/2021/06/e-oie-lista-antimicrobianos-junio2021.pdf

Organización Panamericana de La Salud [OPS]. (2021). ¿Por qué la región de las Américas avanza hacia la prohibición y restricción del uso de colistina en producción animal?. OPS. https://www.paho.org/es/noticias/4-10-2021-por-que-region-americas-avanza-hacia-prohibicion-restriccion-uso-colistina

Ortega-Paredes, D., de Janon, S., Villavicencio, F., Ruales, K. J., De La Torre, K., Villacís, J. E., Wagenaar, J. A., Matheu, J., Bravo-Vallejo, C., Fernández-Moreira, E., y Vinueza-Burgos, C. (2020). Broiler farms and carcasses are an important reservoir of multi-drug resistant Escherichia coli in Ecuador. Frontiers in Veterinary Science, 7, 547843. https://doi.org/10.3389/fvets.2020.547843

Palma, E., Tilocca, B., y Roncada, P. (2020). Antimicrobial resistance in veterinary medicine: An overview. International Journal of Molecular Sciences, 21(6), 1914. https://doi.org/10.3390/ijms21061914

Tabaran, A., Soulageon, V., Chirila, F., Reget, O. L., Mihaiu, M., Borzan, M., y Dan, S. D. (2022). Pathogenic E. coli from cattle as a reservoir of resistance genes to various groups of antibiotics. Antibiotics, 11(3), 404. https://doi.org/10.3390/ANTIBIOTICS11030404

Tutija, J. F., Ramos, C. A. N., Lemos, R. A. A., Santos, A. A. L., Reckziegel, G. H., Freitas, M. G., y Leal, C. R. B. (2022). Molecular and phenotypic characterization of Escherichia coli from calves in an important meat-producing region in Brazil. Journal of Infection in Developing Countries, 16(6), 1030-1036. https://doi.org/10.3855/jidc.13377

Walsh, T. R. (2018). A one-health approach to antimicrobial resistance. Nature Microbiology, 3(8), 854-855. https://doi.org/10.1038/s41564-018-0208-5

Winn, W., Allen, S., Janda, W., Koneman, E., Procop, G., Schreckenberger, P., y Woods, G. (2013). Koneman Diagnóstico microbiólogico Texto y Atlas en color (6a ed.). Editorial Médica Panamericana.

World Health Organization [WHO]. (2021a). Global Antimicrobial Resistance and Use Surveillance System (GLASS) Report. WHO. https://apps.who.int/iris/bitstream/handle/10665/341666/9789240027336-eng.pdf

World Health Organization [WHO]. (2021b). WHO integrated global surveillance on ESBL-producing E. coli using a “One Health” approach: Implementation and opportunities. WHO. https://www.who.int/publications/i/item/9789240021402

World Health Organization [WHO]. (2021c). Antimicrobial resistance. https://www.who.int/es/news-room/fact-sheets/detail/antimicrobial-resistance

Yang, S. C., Lin, C.-H., Aljuffali, I. A., y Fang, J.-Y. (2017). Current pathogenic Escherichia coli foodborne outbreak cases and therapy development. Archives of Microbiology, 3, 811-825. https://doi.org/10.1007/s00203-017-1393-y

Zhang, F., y Cheng, W. (2022). The mechanism of bacterial resistance and potential bacteriostatic strategies. Antibiotics, 11(9), 1215. https://doi.org/10.3390/antibiotics11091215

Most read articles by the same author(s)