Resistencia antimicrobiana y ocurrencia de enteropatógenos bacterianos en estiércol de aves de corral y en suelos agrícolas en Uruguay
DOI:
https://doi.org/10.29155/VET.62.226.7Palabras clave:
Residuos avícolas, Zoonosis, Resistencia antimicrobiana, Multirresistencia, Suelos tratadosResumen
La aplicación agrícola de residuos de la producción avícola requiere estrategias de gestión seguras para evaluar y mitigar la diseminación de bacterias resistentes a los antimicrobianos y patógenos oportunistas en los agroecosistemas. Este estudio evaluó la presencia de patógenos zoonóticos y sus perfiles de resistencia antimicrobiana en residuos avícolas antes y después de tratamientos de compostaje, digestión anaerobia y lavado rápido, así como en suelos fertilizados con estas enmiendas. Todas las muestras fueron procesadas mediante aislamiento bacteriano, identificación molecular y pruebas de susceptibilidad frente a 17 antibióticos.
Se recolectaron y analizaron un total de 106 cepas. Predominaron las enterobacterias (98,6 %), principalmente Klebsiella spp. y E. coli. Entre las 37 cepas de E. coli, se identificaron genes de virulencia compatibles con EPEC en tres cepas y otros factores de virulencia en otras cuatro cepas. Se observó resistencia a los antibióticos en todas las cepas procedentes del estiércol tratado y del suelo, en particular contra los β-lactámicos, las quinolonas, los aminoglucósidos y la fosfomicina. Se identificaron doce cepas multirresistentes, sobre todo de Klebsiella spp., Enterobacter spp. y E. coli, con resistencia asociada a las β-lactamasas AmpC. No se detectó ninguno de los genes mcr-1, mcr-2, mcr-5 o mcr-9, responsables de la resistencia a la colistina.
Estos hallazgos demuestran la presencia de enterobacterias resistentes a los antibióticos en el suelo y el estiércol avícola, así como su persistencia tras tratamientos físicos, químicos y biológicos. La presencia de enterobacterias resistentes a los antibióticos resalta la necesidad de estrategias de monitoreo y mitigación para controlar la propagación ambiental de la resistencia a los antimicrobianos.
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Abreu, R., Semedo-Lemsaddek, T., Cunha, E., Tavares, L., & Oliveira, M. (2023). Antimicrobial Drug Resistance in Poultry Production: Current Status and Innovative Strategies for Bacterial Control. Microorganisms, 11(4), 953. https://doi.org/10.3390/microorganisms11040953
Ayilara, M. S., Olanrewaju, O. S., Babalola, O. O., & Odeyemi, O. (2020). Waste management through composting: Challenges and potentials. Sustainability, 12(11), 4456. https://doi.org/10.3390/su12114456
Bado, I., Papa-Ezdra, R., Delgado-Blas, J. F., Gaudio, M., Gutiérrez, C., Cordeiro, N. F., García-Fulgueiras, V., Araújo Pirez, L., Seija, V., Medina, J. C., Rieppi, G., Gonzalez-Zorn, B., & Vignoli, R. (2018). Molecular characterization of carbapenem-resistant Acinetobacter baumannii in the intensive care unit of Uruguay’s university hospital identifies the first rmtC gene in the species. Microbial Drug Resistance, 24(7), 1012-1019. https://doi.org/10.1089/mdr.2017.0300
Betancor, L., Pereira, M., Martinez, A., Giossa, G., Fookes, M., Flores, K., Barrios, P., Repiso, V., Vignoli, R., Cordeiro, N., Algorta, G., Thomson, N., Maskell, D., Schelotto, F., & Chabalgoity, J. A. (2010). Prevalence of Salmonella enterica in poultry and eggs in Uruguay during an epidemic due to Salmonella enterica serovar Enteritidis. Journal of Clinical Microbiology, 48(7), 2413-2423. https://doi.org/10.1128/jcm.02137-09
Casaux, M. L., Caffarena, R. D., Schild, C. O., Giannitti, F., Riet-Correa, F., & Fraga, M. (2019). Antibiotic resistance in Salmonella enterica isolated from dairy calves in Uruguay. Brazilian Journal of Microbiology, 50(4), 1139-1144. https://doi.org/10.1007/s42770-019-00151-w
Casaux, M. L., D’Alessandro, B., Vignoli, R., & Fraga, M. (2023). Phenotypic and genotypic survey of antibiotic resistance in Salmonella enterica isolates from dairy farms in Uruguay. Frontiers in Veterinary Science, 10, 1055432. https://doi.org/10.3389/fvets.2023.1055432
Chala, B., & Hamde, F. (2021). Emerging and re-emerging vector-borne infectious diseases and the challenges for control: A review. Frontiers in Public Health, 9, 715759. https://doi.org/10.3389/fpubh.2021.715759
Chee-Sanford, J. C., Mackie, R. I., Koike, S., Krapac, I. G., Lin, Y.-F., Yannarell, A. C., Maxwell, S., & Aminov, R. I. (2009). Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. Journal of Environmental Quality, 38(3), 1086-1108. https://doi.org/10.2134/jeq2008.0128
Coppola, N., Cordeiro, N. F., Trenchi, G., Esposito, F., Fuga, B., Fuentes-Castillo, D., Lincopan, N., Iriarte, A., Bado, I., & Vignoli, R. (2022). Imported one-day-old chicks as trojan horses for multidrug-resistant priority pathogens harboring mcr-9, rmtG, and extended-spectrum β-Lactamase genes. Applied and Environmental Microbiology, 88(2), e01675-21. https://doi.org/10.1128/AEM.01675-21
Coppola, N., Freire, B., Umpiérrez, A., Cordeiro, N. F., Ávila, P., Trenchi, G., Castro, G., Casaux, M. L., Fraga, M., Zunino, P., Bado, I., & Vignoli, R. (2020). Transferable resistance to highest priority critically important antibiotics for human health in Escherichia coli strains obtained from livestock feces in Uruguay. Frontiers in Veterinary Science, 7, 588919. https://doi.org/10.3389/fvets.2020.588919
Echeverriborda, G., Mesa, F., Chalar, G., Kruk, C., & Piccini, C. (2022). Experiencia de aplicación de microorganismos efectivos nativos (MEN) para el tratamiento de aguas residuales. INNOTEC, (24), e623. https://doi.org/10.26461/24.06
Fernández, M., Casaux, M. L., Fraga, M., Vignoli, R., Bado, I., Zunino, P., & Umpiérrez, A. (2023). Shiga toxin-producing Escherichia coli (STEC) associated with calf mortality in Uruguay. Microorganisms, 11(7), 1704. https://doi.org/10.3390/microorganisms11071704
Franklin, A. M., Kariyawasam, S., Andrews, D. M., McLain, J. E., & Watson, J. E. (2024). Presence of antimicrobial-resistant bacteria and resistance genes in soil exposed to wastewater treatment plant effluent. Sustainability, 16(16), 7022. https://doi.org/10.3390/su16167022
García-Fulgueiras, V., Bado, I., Mota, M. I., Robino, L., Cordeiro, N. F., Varela, A., Algorta, G., Gutkind, G., Ayala, J. A., & Vignoli, R. (2011). Extended-spectrum β-lactamases and plasmid-mediated quinolone resistance in enterobacterial clinical isolates in the paediatric hospital of Uruguay. The Journal of Antimicrobial Chemotherapy, 66(8), 1725-1729. https://doi.org/10.1093/jac/dkr222
Gigliucci, F., Barbieri, G., Veyrunes, M., Chiani, P., Marra, M., Carollo, M., Knijn, A., Brambilla, G., & Morabito, S. (2025). Characterization of the resistome and antibiotic-resistant bacteria in top soil improvers and irrigation waters devoted to food production: a case study from Italy. Environmental Science and Pollution Research, 32(24), 14691-14705. https://doi.org/10.1007/s11356-025-36438-9
Gomez, S. A., Rapoport, M., Piergrossi, N., Faccone, D., Pasteran, F., De Belder, D., ReLAVRA-Group, Petroni, A., & Corso, A. (2016). Performance of a PCR assay for the rapid identification of the Klebsiella pneumoniae ST258 epidemic clone in Latin American clinical isolates. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 44, 145-146. https://doi.org/10.1016/j.meegid.2016.06.018
González Revello, A. (2020). Generación de métodos basados en genómica para detectar microorganismos nocivos en sistemas acuáticos (Tesis de maestría, Facultad de Ciencias, Universidad de la República). Repositorio Colibri. https://hdl.handle.net/20.500.12008/27665
Heuer, H., Solehati, Q., Zimmerling, U., Kleineidam, K., Schloter, M., Müller, T., Focks, A., Thiele-Bruhn, S., & Smalla, K. (2011). Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine. Applied and Environmental Microbiology, 77(7), 2527-2530. https://doi.org/10.1128/AEM.02577-10
Hu, H.-W., Wang, J.-T., Li, J., Li, J.-J., Ma, Y.-B., Chen, D., & He, J.-Z. (2016). Field-based evidence for copper contamination induced changes of antibiotic resistance in agricultural soils. Environmental Microbiology, 18(11), 3896-3909. https://doi.org/10.1111/1462-2920.13370
Hussein, N. H., Al-Kadmy, I. M. S., Taha, B. M., & Hussein, J. D. (2021). Mobilized colistin resistance (mcr) genes from 1 to 10: a comprehensive review. Molecular Biology Reports, 48(3), 2897-2907. https://doi.org/10.1007/s11033-021-06307-y
Kaper, J. B., Nataro, J. P., & Mobley, H. L. T. (2004). Pathogenic Escherichia coli. Nature Reviews Microbiology, 2(2), 123-140. https://doi.org/10.1038/nrmicro818
Kyakuwaire, M., Olupot, G., Amoding, A., Nkedi-Kizza, P., & Ateenyi Basamba, T. (2019). How safe is chicken litter for land application as an organic fertilizer?: A review. International Journal of Environmental Research and Public Health, 16(19), 3521. https://doi.org/10.3390/ijerph16193521
Leibler, J. H., Otte, J., Roland-Holst, D., Pfeiffer, D. U., Soares Magalhaes, R., Rushton, J., Graham, J. P., & Silbergeld, E. K. (2009). Industrial food animal production and global health risks: Exploring the ecosystems and economics of avian Influenza. EcoHealth, 6(1), 58-70. https://doi.org/10.1007/s10393-009-0226-0
Magiorakos, A.-P., Srinivasan, A., Carey, R. B., Carmeli, Y., Falagas, M. E., Giske, C. G., Harbarth, S., Hindler, J. F., Kahlmeter, G., Olsson-Liljequist, B., Paterson, D. L., Rice, L. B., Stelling, J., Struelens, M. J., Vatopoulos, A., Weber, J. T., & Monnet, D. L. (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection: The Official Publication of the European Society of Clinical Microbiology and Infectious Diseases, 18(3), 268-281. https://doi.org/10.1111/j.1469-0691.2011.03570.x
Martiny, H.-M., Munk, P., Brinch, C., Szarvas, J., Aarestrup, F. M., & Petersen, T. N. (2022). Global distribution of mcr gene variants in 214K metagenomic samples. mSystems, 7(2), e00105-22. https://doi.org/10.1128/msystems.00105-22
Ministerio de Ganadería, Agricultura y Pesca. (2018). Resolución N° 97/018 DGSA: Requisitos para el registro y control para la comercialización de insumos formulados a partir de materia prima de origen orgánico para uso agrícola. Dirección General de Servicios Agrícolas. https://www.gub.uy/ministerio-ganaderia-agricultura-pesca/institucional/normativa/resolucion-n-97018-dgsa-requisitos-para-registro-control-para
Ministerio de Salud Pública, Ministerio de Ambiente, & Ministerio de Ganadería, Agricultura y Pesca. (2025). Plan de acción Nacional único contra la resistencia a los antimicrobianos en Uruguay: Período 2024-2028. https://www.gub.uy/ministerio-ambiente/sites/ministerio-ambiente/files/documentos/publicaciones/2025%20Plan%20de%20accion%20Nacional%20unico%20contra%20la%20RAM%20en%20Uruguay%202024-2028.pdf
Mmatli, M., Mbelle, N. M., & Osei Sekyere, J. (2022). Global epidemiology, genetic environment, risk factors and therapeutic prospects of mcr genes: A current and emerging update. Frontiers in Cellular and Infection Microbiology, 12, 941358. https://doi.org/10.3389/fcimb.2022.941358
Motlhalamme, T., Paul, L., & Singh, V. (2024). Environmental Reservoirs, Genomic Epidemiology, and Mobile Genetic Elements. In V. Soni & A. S. Akhade (Eds.), Antimicrobial Resistance: Factors to Findings (pp. 239-273). Springer. https://doi.org/10.1007/978-3-031-65986-7_7
Niazadeh, M., Nikkhahi, F., Robatjazi, S., Javadi, A., Farzam, S. A., Babaei, S., & Zeynali, P. (2022). Evaluation of mechanisms of colistin resistance in Klebsiella pneumoniae strains isolated from patients with urinary tract infection in ICU. Iranian Journal of Microbiology, 14(1), 31-37. https://doi.org/10.18502/ijm.v14i1.8798
Octavia, S., & Lan, R. (2014). The family Enterobacteriaceae. In E. Rosenberg, E. F. DeLong, S. Lory, E. Stackebrandt, & F. Thompson (Eds.), The Prokaryotes (pp. 225-286). Springer.
Ongeng, D., Geeraerd, A. H., Springael, D., Ryckeboer, J., Muyanja, C., & Mauriello, G. (2015). Fate of Escherichia coli O157:H7 and Salmonella enterica in the manure-amended soil-plant ecosystem of fresh vegetable crops: a review. Critical Reviews in Microbiology, 41(3), 273–294. https://doi.org/10.3109/1040841X.2013.829415
Papa-Ezdra, R., Grill Diaz, F., Vieytes, M., García-Fulgueiras, V., Caiata, L., Ávila, P., Brasesco, M., Christophersen, I., Cordeiro, N. F., Algorta, G., Galiana, A., & Vignoli, R. (2020). First three Escherichia coli isolates harbouring mcr-1 in Uruguay. Journal of Global Antimicrobial Resistance, 20, 187-190. https://doi.org/10.1016/j.jgar.2019.07.016
Price, L. B., Graham, J. P., Lackey, L. G., Roess, A., Vailes, R., & Silbergeld, E. (2007). Elevated risk of carrying gentamicin-resistant Escherichia coli among U.S. poultry workers. Environmental Health Perspectives, 115(12), 1738-1742. https://doi.org/10.1289/ehp.10191
Samreen, I., Ahmad, I., Malak, H. A., & Abulreesh, H. H. (2021). Environmental antimicrobial resistance and its drivers: A potential threat to public health. Journal of Global Antimicrobial Resistance, 27, 101-111. https://doi.org/10.1016/j.jgar.2021.08.001
Szogi, A. A., Vanotti, M. B., & Ro, K. S. (2015). Methods for treatment of animal manures to reduce nutrient pollution prior to soil application. Current Pollution Reports, 1(1), 47-56. https://doi.org/10.1007/s40726-015-0005-1
Tamma, P. D., Aitken, S. L., Bonomo, R. A., Mathers, A. J., van Duin, D., & Clancy, C. J. (2021). Infectious diseases society of america guidance on the treatment of AmpC β-Lactamase-producing Enterobacterales, carbapenem-resistant Acinetobacter baumannii, and Stenotrophomonas maltophilia infections. Clinical Infectious Diseases, 74(12), 2089-2114. https://doi.org/10.1093/cid/ciab1013
Tamma, P. D., Doi, Y., Bonomo, R. A., Johnson, J. K., Simner, P. J., & Antibacterial Resistance Leadership Group. (2019). A primer on AmpC β-Lactamases: Necessary knowledge for an increasingly multidrug-resistant world. Clinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America, 69(8), 1446-1455. https://doi.org/10.1093/cid/ciz173
Tran, D. T. Q., Bradbury, M. I., Ogtrop, F. F. V., Bozkurt, H., Jones, B. J., & McConchie, R. (2020). Environmental drivers for persistence of Escherichia coli and Salmonella in manure-amended Soils: A meta-analysis. Journal of Food Protection, 83(7), 1234-1245. https://doi.org/10.4315/0362-028X.JFP-19-460
Ullah, S. R., Jamal, M., Rahman, A., & Andleeb, S. (2024). Comprehensive insights into Klebsiella pneumoniae: Unravelling clinical impact, epidemiological trends and antibiotic-resistance challenges. Journal of Antimicrobial Chemotherapy, 79(7), 1484-1492. https://doi.org/10.1093/jac/dkae184
Umpiérrez, A., Ernst, D., Cardozo, A., Torres, A., Fernández, M., Fraga, M., Vignoli, R., Bado, I., Vidal, R., & Zunino, P. (2022). Non-O157 Shiga toxin-producing Escherichia coli with potential harmful profiles to humans are isolated from the faeces of calves in Uruguay. Austral Journal of Veterinary Sciences, 54(2), 45-53. http://dx.doi.org/10.4067/S0719-81322022000200045
van den Bogaard, A. E., London, N., Driessen, C., & Stobberingh, E. E. (2001). Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. The Journal of Antimicrobial Chemotherapy, 47(6), 763-771. https://doi.org/10.1093/jac/47.6.763
Van Fan, Y., Lee, C. T., Klemeš, J. J., Chua, L. S., Sarmidi, M. R., & Leow, C. W. (2018). Evaluation of effective microorganisms on home scale organic waste composting. Journal of Environmental Management, 216, 41-48. https://doi.org/10.1016/j.jenvman.2017.04.019
World Health Organization. (2024). WHO bacterial priority pathogens list, 2024: bacterial pathogens of public health importance, to guide research, development, and strategies to prevent and control antimicrobial resistance. WHO. https://www.who.int/publications/i/item/9789240093461
Xu, L., Wang, N., Li, F., Yan, B., Pan, J., Jiang, S., Peng, H., Chen, A., Wu, G., Zhang, J., Zhang, L., Huang, H., & Luo, L. (2022). Evaluation of the synergistic effects of biochar and biogas residue on CO₂ and CH₄ emission, functional genes, and enzyme activity during straw composting. Bioresource Technology, 360, 127608. https://doi.org/10.1016/j.biortech.2022.127608
Zhu, Y.-G., Zhao, Y., Zhu, D., Gillings, M., Penuelas, J., Ok, Y. S., Capon, A., & Banwart, S. (2019). Soil biota, antimicrobial resistance and planetary health. Environment International, 131, 105059. https://doi.org/10.1016/j.envint.2019.105059
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