Presence of extended-spectrum beta-lactamase–producing Escherichia coli in fecal content of cattle from two slaughterhouses in Lima, Peru, 2023–2024
DOI:
https://doi.org/10.20453/stv.v13i2.6867Abstract
The indiscriminate use of antimicrobials has led enterobacteria such as Escherichia coli to develop a variety of resistance mechanisms such as the production of extended-spectrum beta-lactamases (ESBL). Beta-lactam antimicrobials including penicillins, monobactams, and cephalosporins are among the most widely used in both animals and humans; Therefore, the presence of ESBL-producing E. coli (ESBL-EC) has the ability to hydrolyze these antimicrobials, leading to resistance against this class of agents, which represents a potencial threat to human and animal health. This study aimed to determine the presence of ESBL-EC in fecal samples from cattle at two slaughterhouses in Lima, Peru. A total of 260 fecal samples from cattle were collected at two slaughterhouses: S1 (n=134) and S2 (n=126). Antibiotic discs of cefotaxime (CTX) 30 µg, aztreonam (ATM) 30 µg, ceftazidime (CAZ) 30 µg, cefpodoxime (CPD) 10 µg and ceftriaxone (CRO) were used as screening method. While, antimicrobials cefotaxime - clavulanic acid (CTX-CLA) (30/10 µg) and ceftazidime - clavulanic acid (CAZ-CLA) (30/10 µg) were used in combined disc method for ESBL-EC phenotypic confirmation. The interpretation results follow the guidelines of the Clinical and Laboratory Standards Institute (CLSI). Finally, was determined that 23.5% (61/260) of fecal sample presented ESBL-EC. Our results demonstrate that cattle intended for human consumption are carriers of ESBL-EC representing a potential public health risk.
Keywords: ESBL-EC, antimicrobial resistance, cattle
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References
Allocati, N., Masulli, M., Alexeyev, M. y Di Ilio, C. (2013). Escherichia coli in Europe: an overview. International Journal of Environmental Research and Public Health, 10(12), 6235-6254. https://doi.org/10.3390/ijerph10126235
Alós, J. (2015). Resistencia bacteriana a los antibióticos: una crisis global. Enfermedades infecciosas y Microbiología Clínica, 33(10), 692-699. https://doi.org/10.1016/j.eimc.2014.10.004
Ambler R. P. (1980). The structure of beta-lactamases. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 289(1036), 321–331. https://doi.org/10.1098/rstb.1980.0049
Aworh, M., Ekeng, E., Nilsson, P., Egyir, B., Owusu-Nyantakyi, C. y Hendriksen, R. (2022). Extended-spectrum ß-lactamase-producing Escherichia coli among humans, beef cattle, and abattoir environments in Nigeria. Frontiers in Cellular and Infection Microbiology, 12, 869314. https://doi.org/10.3389/fcimb.2022.869314
Aworh, M., Lawal, O., Egyir, B. y Hendriksen, R. (2025). In silico genomic insights into bacteriophages infecting ESBL-producing Escherichia coli from human, animal, and environmental sources. BMC Microbiology, 25, 200. https://doi.org/10.1186/s12866-025-03913-9
Barlow, R., McMillan, K., Mellor, G., Duffy, L., Jordan, D., Abraham, R., O’dea, M., Sahibzada, S. y Abraham S. (2022). Phenotypic and genotypic assessment of antimicrobial resistance in Escherichia coli from australian cattle populations at slaughter. Journal of Food Protection, 85(4), 563-570. https://doi.org/10.4315/JFP-21-430
Bazalar-Gonzales, J., Silvestre-Espejo, T., Rodríguez, C., Carhuaricra, D., Ignacion, Y., Luna, L., Rosadio, R. y Maturrano, L. (2024). Genomic insights into ESBL-producing Escherichia coli isolated from no -human primates in the peruvian Amazon. Frontiers in Veterinary Science, 10, 1340428. https://doi.org/10.3389/fvets.2023.1340428
Benavides, J., Godreuil, S., Opazo-Capurro, A., Mahamat, O., Falcon, N., Oravcova, K. y Streicker, D. (2022). Long-term maintenance of multidrog-resistant Escherichia coli carried by vampire bats and shared with livestock in Peru. Science of the Total Environment, 810, 152045. https://doi.org/10.1016/j.scitotenv.2021.152045
Bradford, P. (2001). Extended-spectrum ß-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clinical Microbiology Reviews, 14(4), 933-951. https://doi.org/10.1128/CMR.14.4.933-951.2001
Briñas, L., Moreno, M., Teshager, T., Sáenz, Y., Porrero, M., Domínguez, L. y Torres, C. (2005). Monitoring and characterization of extended-spectrum β-lactamases in Escherichia coli strains from healthy and sick animals in Spain in 2003. Antimicrobial Agents and Chemotherapy, 49(3), 1262-1264. https://doi.org/10.1128/AAC.49.3.1262-1264.2005
Bush, K. y Jacoby, G. (2010). Updated functional classification of β-lactamases. Antimicrobial Agents and Chemotheraphy, 54(3), 969-676. https://doi.org/10.1128/AAC.01009-09
Carhuallanqui, A., Villafana, L., Gonzalez-Veliz, R., Cobo-Díaz, J., Álvarez-Ordoñez, A. y Ramos-Delgado, D. (2025). Colistin-resistant Escherichia coli isolated from houseflies and feces of cattle and pigs at a slaughterhouse in Lima, Peru. Antibiotics, 14(8), 818. https://doi.org/10.3390/antibiotics14080818
Ceino, F., Koga, I. y Peña, N. (2019). Detección fenotípica y genotípica de Escherichia coli productoras de β-lactamasas espectro extendido aisladas de aves de abasto en Perú. Biotempo, 16(2), 181-186. https://doi.org/10.31381/biotempo.v16i2.2528
Chávez, K., Condolo, L., Vinueza, P. y Tiama, N. (2025). Patrones de resistencia a los antibióticos en bacterias aisladas de mastitis subclínicas. Revista de Investigaciones Veterinarias del Perú, 36(1), e30199. https://doi.org/10.15381/rivep.v36i1.30199
Clinical and Laboratory Standards Institute [CLSI] (2024). M100 Performance Standards for Antimicrobial Susceptibility Testing (34.a ed.).
Cortez, V. y Shiva, C. (2019). Detección de enterobacterias productoras de β-lactamasas de espectro extendido (BLEE) aisladas en carne molida de supermercados de un distrito de Lima, Perú. Salud y Tecnología Veterinaria, 7(1), 1-7. https://doi.org/10.20453/stv.v7i1.3561
Cortez-Sandoval, V., González, R. y Ramos, D. (2022). Detección de enterobacterias productoras de β-lactamasas de espectro extendido (BLEE) aisladas en carne de pollo de mercados de abasto de un distrito de Lima, Perú. Revista de Investigaciones Veterinarias del Perú. 33(3), e22899. https://doi.org/10.15381/rivep.v33i3.22899
Dahms, C., Hübner, N., Kossow, A., Mellmann, A., Dittmann, K. y Kramer, A. (2015). Occurrence of ESBL-producing Escherichia coli in livestock and farm workers in Mecklenburg-Western Pomerania, Germany. PloS ONE, 10(11), e0143326. https://doi.org/10.1371/journal.pone.0143326
Dever, L. y Dermody, T. (1991). Mechanisms of bacterial resistance to antibiotics. Archives of Internal Medicine, 151(5), 886-895. https://doi.org/10.1001/archinte.1991.00400050040010
Egbule, O. y Yusuf, I. (2019). Multiple antibiotic resistances in Escherichia coli isolated from cattle and poultry faeces in Abraka, South-South Nigeria. Pertanika Journal of Tropical Agricultural Science, 42(2), 585-594. http://pertanika2.upm.edu.my/resources/files/Pertanika%20PAPERS/JTAS%20Vol.%2042%20(2)%20May.%202019/13%20JTAS-1598-2018.pdf
Estrada-Calles, D. M., Rodríguez-Gamboa, M. F., y Velázquez-Álvarez, E. A. (2022). Resistencia a antibióticos betalactámicos: situación actual y nuevas estrategias. RD-ICUAP, 8(22), 13–27. https://doi.org/10.32399/icuap.rdic.2448-5829.2022.22.682
Ewers, C., Bethe, A., Semmler, T., Guenther, S. y Wieler, L. (2012). Extended-spectrum β-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clinical Microbiology and Infection, 18(7), 646-655. https://doi.org/10.1111/j.1469-0691.2012.03850.x
Gajdács, M., Urbán, E., Stájer, A. y Baráth, Z. (2021). Antimicrobial resistance in the context of the sustainable development goals: a brief review. European Journal of Investigation in Health, Psychology and Education, 11(1), 71-82. https://doi.org/10.3390/ejihpe11010006
García-Alarcón, Z., Alderete-Gutiérrez, J., Ramírez-Trejo, C., Leal-Rodríguez, J., Olave-Leyva, J. y Martínez-Juárez, V. (2025). Resistencia a antimicrobianos en bovinos leche y bovinos carne y su posible impacto en la salud pública a nivel mundial. Boletín de Ciencias Agropecuarias del ICAP, 11(21), 21-29. https://doi.org/10.29057/icap.v11i21.13111
Geser, N., Stephan, R. y Hächler, H. (2012). Occurrence and characteristics of extended-spectrum β-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Veterinary Research, 8(1), 21. https://doi.org/ 10.1186/1746-6148-8-21
Geser, N., Stephan, R., Kuhnert, P., Zbinden, R., Kaeppeli, U., Cernela, N. y Haechler, H. (2011). Fecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae in swine and cattle at slaughter in Switzerland. Journal of Food Protection, 74(3), 446-449. https://doi.org/10.4315/0362-028X.JFP-10-372
Ghafourian, S., Sadeghifard, N., Soheili, S. y Sekawi, Z. (2015). Extended spectrum beta-lactamases: definition, classification and epidemiology. Current Issues in Molecular Biology, 17, 11-22. https://doi.org/10.21775/cimb.017.011
Huamán, M., Salvador-Luján, G., Morales, L., Alba, J., Velasquez, L., Pacheco, J. y Pons, M. (2024). Resistance to cephalosporins and quinolones in Escherichia coli isolated from irrigation water from the Rímac river in east Lima, Peru. Revista Peruana de Medicina Experimental y Salud Pública, 41(2), 114-120. https://doi.org/10.17843/rpmesp.2024.412.13246
Huamán-Chacón, L. y Gonzales-Escalante, E. (2019). Escherichia coli productor de betalactamasas de espectro extendido en pollos para consumo humano. Revista Peruana de Medicina Experimental y Salud Pública, 36(2), 361-362. http://www.scielo.org.pe/scielo.php?script=sci_arttext&pid=S1726-46342019000200029
Khalifeh, O. M. y Obaidat, M. (2022). Urinary tract virulence genes in extended-spectrum beta-lactamase E. coli from dairy cows, beef cattle, and small ruminants. Acta Tropica, 234, 106611. https://doi.org/10.1016/j.actatropica.2022.106611
Larson, A., Hartinger, S., Riveros, M., Salmon-Mulanovich, G., Hattendorf, J., Verastegui, H. y Mäusezahl, D. (2019). Antibiotic-Resistant Escherichia coli in drinking water samples from rural andean households in Cajamarca, Peru. The American Journal if Tropical Medicine and Hygiene, 100(6), 1363-1368. https://doi.org/10.4269/ajtmh.18-0776
Lezameta, L., Gonzales-Escalante, E., Tamariz, J. (2010). Comparación de cuatro métodos fenotípicos para la detección de beta-lactamasas de espectro extendido. Revista Peruana de Medicina Experimental y Salud Pública, 27(3), 345-351. http://www.scielo.org.pe/scielo.php?script=sci_arttext&pid=S1726-46342010000300006
Ma, F., Xu, S., Tang, Z., Li, Z. y Zhang, L. (2021). Use of antimicrobials in food animals and impact of transmission of antimicrobial resistance on humans. Biosafety and Health, 3(1), 32-38. https://doi.org/10.1016/j.bsheal.2020.09.004
Newell, D., Koopmans, M., Verhoef, L., Duizer, E., Aidara-Kane, A., Sprong, H., Opsteegh, M., Langelaar, M., Threfall, J., Scheutz, F., Van der Giessen, J. y Kruse H. (2010). Food-borne diseases - the challenges of 20 years ago still persist while new ones continue to emerge. International Journal of Food Microbiology, 139(supl. 1), S3-S15. https://doi.org/10.1016/j.ijfoodmicro.2010.01.021
Pires, A., Pereira, G., Fangueiro, D., Bexiga, R. y Oliveira, M. (2024). When the solution becomes the problem: a review on antimicrobial resistance in dairy cattle. Future Microbiology, 19(10), 903-929. https://doi.org/10.2217/fmb-2023-0232
Quiñones, D. (2017). Resistencia antimicrobiana: evolución y perspectivas actuales ante el enfoque «Una salud». Revista Cubana de Medicina Tropical, 69(3), 1-17. http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S0375-07602017000300009
Ramos, S., Silva, V., Dapkevicius, M., Caniça, M., Tejedor-Junco, M., Igrejas, G. y Poeta, P. (2020). Escherichia coli as commensal and pathogenic bacteria among food-producing animals: health implications of extended spectrum β-lactamase (ESBL) production. Animals, 10(12), 2239. https://doi.org/10.3390/ani10122239
Redding, L., Cubas-Delgado, F., Sammel, M., Smith, G., Galligan, D., Levy, M. y Hennessy, S. (2014). The use of antibiotics on small dairy farms in rural Peru. Preventive Veterinary Medicine, 113(1), 88-95. https://doi.org/10.1016/j.prevetmed.2013.10.012
Reist, M., Geser, N., Hächler, H., Schärrer, S. y Stephan, R. (2013). ESBL-producing Enterobacteriaceae: occurrence, risk factors for fecal carriage and strain traits in the Swiss slaughter cattle population younger than 2 years sampled at abattoir level. PloS One, 8(8), e71725. https://doi.org/10.1371/journal.pone.0071725
Resolución Directoral n.º 0072-2013-MINAGRI-SENASA-DIAIA, que prohíben importación y comercialización de diversos principios activos, así como el uso de los mismos en la fabricación de productos veterinarios o alimentos para animales destinados al consumo humano y establecen otras disposiciones. Diario Oficial El Peruano (23 de septiembre de 2013). https://www.midagri.gob.pe/portal/download/pdf/marcolegal/normaslegales/resolucionesdirectorales/2013/setiembre/rd72-2013-minagri-senasa-diaia.pdf
Resolución Directoral N.° 0091-2019-MINAGRI-SENASA-DIAIA, que disponen prohibir la importación, comercialización, fabricación o elaboración de productos veterinarios que contengan el principio activo colistina (Polimixina E) o cualquiera de sus sales y dictan diversas disposiciones. Diario Oficial El Peruano (2 de diciembre de 2019). https://cdn.www.gob.pe/uploads/document/file/5478518/4886940-rd-0091-2019-minagri-senasa-diaia.pdf?v=1700857823
Ruiz-Roldán, L., Martínez-Puchol, S., Gomes, C., Palma, N., Riveros, M., Ocampo, K., Durand, D., Ochoa, T., Ruiz, J. y Pons, M. (2018). Presencia de Enterobacteriaceae y Escherichia coli multirresistente a antimicrobianos en carne adquirida en mercados tradicionales en Lima. Revista Peruana de Medicina Experimental y Salud Pública, 35(3), 425-432. http://dx.doi.org/10.17843/rpmesp.2018.353.3737
Sanou, S., Ouedraogo, A. S., Lounnas, M., Zougmore, A., Pooda, A., Zoungrana, J. y Godreuil, S. (2022). Epidemiology and molecular characterization of Enterobacteriaceae producing extended-spectrum β-lactamase in intensive and extensive breeding animals in Burkina Faso. PAMJ-One Health, 8(4). https://www.one-health.panafrican-med-journal.com/content/article/8/4/full/
Seral, C., Pardos, M. y Castillo, F. (2010). Betalactamasas de espectro extendido en enterobacterias distintas de Escherichia coli y Klebsiella. Enfermedades Infecciosas y Microbiología Clínica, 28(supl. 1), 12-18. https://doi.org/10.1016/S0213-005X(10)70003-3
Sudarwanto, M., Lukman, D., Latif, H., Pisestyani, H., Sukmawinata, E., Akineden, Ö. y Usleber, E. (2016). CTX-M producing Escherichia coli isolated from cattle feces in Bogor slaughterhouse, Indonesia. Asian Pacific Journal of Tropical Biomedicine, 6(7), 605-608. https://doi.org/10.1016/j.apjtb.2016.05.001
Tadesse, D., Li, C., Mukherjee, S., Hsu, C., Bodeis, S., Gaines, S., Kabera, C., Loneragan, G., Torrence, M., Harhay, D. McDermott, P. y Zhao, S.(2018). Whole-Genome sequence analysis of CTX-M containing Escherichia coli isolates from retail meats and cattle in the United States. Microbial Drug Resistance, 24(7), 939-948. https://doi.org/10.1089/mdr.2018.0206
United States Department of Agriculture [USDA]; Food Safety and Inspection Service (2023). MLG 31.01: Isolating bacteria from food animals for antimicrobial resistance surveillance. En Microbiology Laboratory Guidebook (pp. 1-17). https://www.fsis.usda.gov/sites/default/files/media_file/documents/MLG_31.01.pdf
Van Boeckel, T., Glennon, E., Chen, D., Gilbert, M., Robinson, T., Grenfell, B., Levin, S., Bonhoeffer, S. y Laxminarayan, R. (2017). Reducing antimicrobial use in food animals. Science, 357(6358), 1350-1352. https://doi.org/10.1126/science.aao1495
Wang, W., Wei, X., Wu, L., Shang, X., Cheng, F., Li, B., Zhou, X. y Zhang, J. (2021). The occurrence of antibiotic resistance genes in the microbiota of yak, beef and dairy cattle characterized by a metagenomic approach. The Journal of Antibiotics, 74(8), 508-518. https://doi.org/10.1038/s41429-021-00425-2
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