ESBL superbacteria in fresh waters of Tungurahua: risks and regulatory gaps
DOI:
https://doi.org/10.56294/saludcyt20251717Keywords:
Fresh Water, Drug Resistance, Microbial, Extended-Spectrum Beta-Lactamases (ESBL), One Health, Environmental Legislation – TULSMA, Public HealthAbstract
Introduction: currently, antimicrobial resistance and more specifically extended-spectrum beta-lactamase (ESBL)-producing bacteria are a growing global threat. The fresh waters of Tungurahua-Ecuador are very important because of the diversity of uses they provide and could also be a source and dissemination route of ESBL with a potential risk to public health and the environment.
Methods: a descriptive, qualitative-quantitative observational study was carried out in the province of Tungurahua. Thirty points (5 rivers, 25 pools) were analyzed by non-probabilistic sampling. Physicochemical variables (pH, chlorine, temperature) were measured in situ and in the laboratory. Bacteria were isolated and phenotypically characterized. A qualitative regulatory analysis was performed to detect regulatory gaps in antimicrobial resistance and ESBL.
Results: ESBL phenotype was detected in 28 of the 30 sites (93,3 %): 5 rivers and 23 of the 25 pools. In rivers, E. coli ESBL (72,7 %) and KEC (Klebsiella, Enterobacter, Citrobacter) (27,3 %) were the most frequent. In swimming pools, Acinetobacter ESBL (60,6 %), KEC (15,2 %), Pseudomonas (15,2 %) and E. coli (9,1 %) were the most frequent. Regulatory analysis revealed that TULSMA lacked specific AMR/ESBL parameters, mandatory periodic monitoring and alert thresholds.
Conclusions: the evidence revealed severe contamination by ESBL, linked to wastewater and agricultural discharges, which increases the health and environmental risk. There is an urgent need to improve water treatment, discharge controls and monitoring. The TULSMA lacks parameters for AMR, ESBL, ARGs and “One Health” approach; it requires PCR and intersectoral surveillance and active training.
References
1. Pérez Aldas LV, Guachamin Zambrano SN, Acurio Arcos LP, Robalino Martínez D, Fuentes EM. Study of the Influence of Anthropogenic Sources on the Water Quality of the Ambato River, Tungurahua - Ecuador. A Growing Environmental Problem. Lecture Notes in Networks and Systems. 2022 Jan 1;379:101–10. https://doi.org/10.1007/978-3-030-94262-5_10
2. Infoandina. Inventario y diagnóstico del recurso hídrico. Provincia de Tungurahua [Internet]. 2004 [cited 2025 Apr 12]. Available from: http://infoandina.org/infoandina/es/content/inventario-y-diagn%C3%B3stico-del-recurso-h%C3%ADdrico-provincia-de-tungurahua.
3. Organización Panamericana de la Salud, Ministerio de Salud de Argentina. Enfoque Una Salud: estudios ambientales de la resistencia a los antimicrobianos Iniciativas en Argentina [Internet]. 2023 [cited 2025 Apr 12]. Available from: https://www.argentina.gob.ar/sites/default/files/bancos/2023-11/enfoque_-una_salud_estudios_ambientales_resistencia_antimicrobianos_6112023.pdf
4. Tang KWK, Millar BC, Moore JE. Antimicrobial Resistance (AMR). Br J Biomed Sci. 2023 Jun 28;80. https://doi.org/10.3389/bjbs.2023.11387
5. Cho S, Jackson CR, Frye JG. Freshwater environment as a reservoir of extended-spectrum β-lactamase-producing Enterobacteriaceae. J Appl Microbiol. 2023 Mar 1;134(3). https://doi.org/10.1093/JAMBIO/LXAD034
6. Song H, Yoo JS, Unno T. Discerning the dissemination mechanisms of antibiotic resistance genes through whole genome sequencing of extended-spectrum beta-lactamase (ESBL)-producing E. coli isolated from veterinary clinics and farms in South Korea. Science of The Total Environment [Internet]. 2024 May 20;926:172068. https://doi.org/10.1016/J.SCITOTENV.2024.172068
7. González-Osorio BB, Saá-Yánez LM, Simba-Ochoa LF, Barragán-Monrroy R, Cadme-Arevalo ML. Vegetación riparia y la calidad del recurso hídrico en la zona centro del litoral Ecuatoriano. REVISTA TERRA LATINOAMERICANA. 2022 Nov 19;40. https://doi.org/10.28940/terra.v40i0.1070
8. Osisiogu EU, Appiah CA, Mahmoud FC, Bawa FK, Nattah EM. Detection and Phenotypic Characterization of Colistin-Resistant Bacteria in Water. Science International. 2023 Jul 3;11(1):9–17. https://doi.org/10.17311/SCIINTL.2023.09.17
9. Menchaca M, Alvarado E. Anthropogenic effects caused by water users in the Pixquiac river micro-basin. Rev Mex De Cienc Agric [Internet]. 2011 Aug 31;85–96. Available from: https://www.scielo.org.mx/pdf/remexca/v2nspe1/v2spe1a7.pdf
10. Franz E, Veenman C, van Hoek AHAM, Husman A de R, Blaak H. Pathogenic Escherichia coli producing Extended-Spectrum β-Lactamases isolated from surface water and wastewater. Sci Rep. 2015 Sep 24;5(1):14372. https://doi.org/10.1038/srep14372
11. Solaiman S, Handy E, Brinks T, Goon K, Bollinger C, Sapkota AR, et al. Extended Spectrum β-Lactamase Activity and Cephalosporin Resistance in Escherichia coli from U.S. Mid-Atlantic Surface and Reclaimed Water. Villanueva L, editor. Appl Environ Microbiol. 2022 Aug 9;88(15):e00837-22. https://doi.org/10.1128/aem.00837-22
12. Ali AS, Gari SR, Goodson ML, Walsh CL, Dessie BK, Ambelu A. Fecal Contamination in the Wastewater Irrigation System and its Health Threat to Wastewater-Based Farming Households in Addis Ababa, Ethiopia. Environ Health Insights. 2023 Jan 20;17. https://doi.org/10.1177/11786302231181307
13. Skórczewski P, Jan Mudryk Z, Jankowska M, Perliński P, Zdanowicz M, Jan Mudryk Z, et al. Antibiotic resistance of fecal coliform bacteria Antibiotic resistance of neustonic and planktonic fecal coliform bacteria isolated from two water basins differing in the level of pollution. Hidrobiológica. 2013;23(3):431–9. Available from: https://www.scielo.org.mx/pdf/hbio/v23n3/v23n3a17.pdf
14. Mallin MA. Effect of Human Land Development on Water Quality. In: Handbook of Water Purity and Quality. Elsevier; 2009. p. 67–94. https://doi.org/10.1016/B978-0-12-374192-9.00004-2
15. Peluso J, Martínez Chehda A, Olivelli MS, Ivanic FM, Butler M, Aparicio V, et al. Impacts of cattle management and agricultural practices on water quality through different approaches: physicochemical and ecotoxicological parameters. Environmental Science and Pollution Research. 2024 Jul 3;31(32):45177–91. https://doi.org/10.1007/s11356-024-34059-2
16. Zhao B, van Bodegom PM, Trimbos KB. Antibiotic Resistance Genes in Interconnected Surface Waters as Affected by Agricultural Activities. Biomolecules. 2023 Jan 24;13(2):231. https://doi.org/10.3390/biom13020231
17. Ministerio del Ambiente. TEXTO UNIFICADO DE LEGISLACION SECUNDARIA DE MEDIO AMBIENTE - TULSMA [Internet]. 2017 [cited 2025 Mar 31]. Available from: https://www.ambiente.gob.ec/wp-content/uploads/downloads/2018/05/TULSMA.pdf
18. Agencia de Regulación y Control del Agua. Norma técnica para el control a la Calidad del agua de consumo humano - Regulación Nro. DIR-ARCA-RG-012-2022 [Internet]. Quito; 2022 [cited 2025 Apr 12]. Available from: https://www.regulacionagua.gob.ec/wp-content/uploads/downloads/2022/07/Regulacio%CC%81n-DIR-ARCA-RG-012-2022-Calidad-del-agua_-signed.pdf
19. Zhang L, Ma X, Luo L, Hu N, Duan J, Tang Z, et al. The Prevalence and Characterization of Extended-Spectrum β-Lactamase- and Carbapenemase-Producing Bacteria from Hospital Sewage, Treated Effluents and Receiving Rivers. Int J Environ Res Public Health. 2020 Feb 13;17(4):1183. https://doi.org/10.3390/ijerph17041183
20. Czatzkowska M, Wolak I, Harnisz M, Korzeniewska E. Impact of Anthropogenic Activities on the Dissemination of ARGs in the Environment—A Review. Int J Environ Res Public Health. 2022 Oct 7;19(19):12853. https://doi.org/10.3390/ijerph191912853
21. Sivalingam P, Sabatino R, Sbaffi T, Corno G, Fontaneto D, Borgomaneiro G, et al. Anthropogenic pollution may enhance natural transformation in water, favouring the spread of antibiotic resistance genes. J Hazard Mater. 2024 Aug 15;475:134885. https://doi.org/10.1016/j.jhazmat.2024.134885
22. Pauta-Calle G, Velasco M, Vázquez G, Abril A, Torres S. Analysis and risk assessment of arsenic in the water sources of the cities Cuenca and Azogues, Ecuador. MASKANA. 2021 Dec 24;12(2):71–9. https://doi.org/
23. Ortega-Paredes D, Barba P, Mena-López S, Espinel N, Crespo V, Zurita J. High quantities of multidrug-resistant Escherichia coli are present in the Machángara urban river in Quito, Ecuador. J Water Health. 2020 Feb 1;18(1):67–76. https://doi.org/
24. Romero Borja EW. Caracterización de la resistencia antimicrobiana en Escherichia coli productora de β-lactamasas de espectro extendido (BLEE) aislada de aguas residuales descargadas en el río Chimbo del cantón San Miguel-provincia Bolívar-Ecuador [Internet]. 2020. Available from: http://www.dspace.uce.edu.ec/handle/25000/22406
25. Toledo Z, Simaluiza RJ, Fernández H. Occurrence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from domestic animals from Southern Ecuador. Ciência Rural. 2018 Nov 1;48(11):e20180003. https://doi.org/10.1590/0103-8478cr20180003
26. Moretto VT, Cordeiro SM, Bartley PS, Silva LK, Ponce-Terashima R, Reis MG, et al. Antimicrobial-resistant enterobacteria in surface waters with fecal contamination from urban and rural communities. Rev Soc Bras Med Trop. 2021;54. https://doi.org/10.1590/0037-8682-0724-2020
27. Koskeroglu K, Barel M, Hizlisoy H, Yildirim Y. Biofilm formation and antibiotic resistance profiles of water-borne pathogens. Res Microbiol. 2023;174(5). https://doi.org/10.1016/j.resmic.2023.104056
28. Mandujano A, Cortés-Espinosa DV, Vásquez-Villanueva J, Guel P, Rivera G, Juárez-Rendón K, et al. Extended-Spectrum β-Lactamase-Producing Escherichia coli Isolated from Food-Producing Animals in Tamaulipas, Mexico. Antibiotics. 2023 Jun 5;12(6):1010. https://doi.org/10.3390/antibiotics12061010
29. Hashim NHF, Mohamed Yusoff MA, Gunggang RAT, Abdul Razak R, Jaafar MZ, Yahaya NKEM. Water Quality and Prevalence of Extended Spectrum Beta Lactamase Producing Escherichia coli (ESBL E. coli) in Sungai Terengganu, Malaysia. Malaysian Applied Biology. 2024;53(4):65–75. https://doi.org/10.55230/mabjournal.v53i4.3088
30. Sabença C, de la Rivière R, Barros P, Cabral JA, Sargo R, Sousa L, et al. Assessment of Antibiotic Resistance Among Isolates of Klebsiella spp. and Raoultella spp. in Wildlife and Their Environment from Portugal: A Positive Epidemiologic Outcome. Pathogens. 2025;14(1). https://doi.org/10.3390/pathogens14010099
31. Milenkov M, Proux C, Rasolofoarison TL, Rakotomalala FA, Rasoanandrasana S, Rahajamanana VL, et al. Implementation of the WHO Tricycle protocol for surveillance of extended-spectrum β-lactamase producing Escherichia coli in humans, chickens, and the environment in Madagascar: a prospective genomic epidemiology study. Lancet Microbe. 2024 Aug 1;5(8):100850. https://doi.org/10.1016/S2666-5247(24)00065-X
32. Jimenez Quiceno JN, Rodríguez EA. Resistencia bacteriana en ambientes acuáticos: origen e implicaciones para la salud pública. Revista Facultad Nacional de Salud Pública. 2023 Jul 10;41(3):e351453. https://doi.org/10.17533/udea.rfnsp.e351453
33. Herrmann P. Management Conflicts in the Ambato River Watershed, Tungurahua Province, Ecuador. BioOne Digital Library. 2002 Nov 1;22(4):338–40. https://doi.org/10.1659/0276-4741(2002)022[0338:MCITAR]2.0.CO;2
34. Alawi M, Smyth C, Drissner D, Zimmerer A, Leupold D, Müller D, et al. Private and well drinking water are reservoirs for antimicrobial resistant bacteria. npj Antimicrobials and Resistance 2024 2:1. 2024 Mar 18;2(1):1–16. https://doi.org/10.1038/s44259-024-00024-9
35. Organización Mundial de la Salud (OMS). Desarrollo de Reglamentos y Normas de Calidad Del Agua de Consumo Humano : Orientación General con Especial Atención a Los Países con Recursos Limitados. 2022 [cited 2025 Apr 20];69. Available from: https://iris.who.int/bitstream/handle/10665/353610/9789240048171-spa.pdf?sequence=1
36. Organización Mundial de la Salud (OMS). One Health Joint Plan of Action (2022-2026) - Working together for the health of humans, animals, plants and the environment. 2022 Nov 1 [cited 2025 Apr 12]; Available from: https://doc.woah.org/dyn/portal/index.xhtml?page=alo&aloId=42869
37. Organización Mundial de la Salud. Plan de acción mundial sobre la resistencia a los antibióticos. OMS [Internet]. 2016 [cited 2025 Apr 14];30. Available from: https://www.who.int/es/publications/i/item/9789241509763
38. Ministerio de Salud Pública del Ecuador. Plan Nacional para la prevención y control de la resistencia antimicrobiana - Registro Oficial No 25 [Internet]. 2019 [cited 2025 Apr 12]. Available from: www.msp.gob.ec
39. Hart A, Warren J, Wilkinson H, Schmidt W. Environmental surveillance of antimicrobial resistance (AMR), perspectives from a national environmental regulator in 2023. Eurosurveillance. 2023 Mar 16;28(11). https://doi.org/10.2807/1560-7917.ES.2023.28.11.2200367
40. Díaz-Gavidia C, Barría C, Rivas L, García P, Alvarez FP, González-Rocha G, et al. Isolation of Ciprofloxacin and Ceftazidime-Resistant Enterobacterales From Vegetables and River Water Is Strongly Associated With the Season and the Sample Type. Front Microbiol. 2021;12. https://doi.org/10.3389/fmicb.2021.604567
41. Pazos C, Gualoto M, Oña T, Velarde E, Portilla K, Cabrera-García S, et al. Molecular Detection of blaTEM and blaSHV Genes in ESBL-Producing Acinetobacter baumannii Isolated from Antarctic Soil. Microorganisms. 2025 Feb 21;13(3):482. https://doi.org/10.3390/microorganisms13030482
42. Ramaite K, Ekwanzala MD, Momba MNB. Prevalence and Molecular Characterisation of Extended-Spectrum Beta-Lactamase-Producing Shiga Toxin-Producing Escherichia coli, from Cattle Farm to Aquatic Environments. Pathogens. 2022;11(6). https://doi.org/10.3390/pathogens11060674
43. Singh NS, Singhal N, Kumar M, Virdi JS. High Prevalence of Drug Resistance and Class 1 Integrons in Escherichia coli Isolated From River Yamuna, India: A Serious Public Health Risk. Front Microbiol. 2021;12. https://doi.org/10.3389/fmicb.2021.621564
44. Chotinantakul K, Chusri P, Okada S. Detection and characterization of ESBL-producing Escherichia coli and additional co-existence with mcr genes from river water in northern Thailand. PeerJ. 2022;10. https://doi.org/10.7717/peerj.14408
45. Gobierno de México; Secretaría de Agricultura y Desarrollo Rural (SADER); Servicio Nacional de Sanidad Inocuidad y Calidad Agroalimentaria (SENASICA). Plan estratégico contra la Resistencia a los Antimicrobianos (RAM) [Internet]. 2023 [cited 2025 Apr 20]. Available from: https://www.gob.mx/cms/uploads/attachment/file/847156/Plan_Estrategico_RAM_VF.pdf
46. Kayode AJ, Semerjian L, Osaili T, Olapade O, Okoh AI. Occurrence of Multidrug-Resistant Listeria monocytogenes in Environmental Waters: A Menace of Environmental and Public Health Concern. Front Environ Sci. 2021 Oct 12;9:737435. https://doi.org/10.3389/FENVS.2021.737435/BIBTEX
Published
Issue
Section
License
Copyright (c) 2025 Andrés Chérrez-Ramírez, Dra. Patricia Lorena Paredes, Dr- Alejandro Bravo Paredes, Dr. Iván Toapanta Yugcha (Author)
This work is licensed under a Creative Commons Attribution 4.0 International License.
The article is distributed under the Creative Commons Attribution 4.0 License. Unless otherwise stated, associated published material is distributed under the same licence.
