Resistance to cephalosporins and quinolones by Escherichia coli isolated from irrigation water from eastern Lima, Perú

Authors

  • Mónica Huamán Iturrizaga Laboratorio de Ecología Microbiana, Facultad de Ciencias Biológicas de Universidad Nacional Mayor de San Marcos, Lima, Perú. Oficina de Epidemiología y Salud Ambiental, Instituto Nacional Materno Perinatal, Lima Perú. https://orcid.org/0000-0001-7369-2325
  • Gina Salvador-Luján Laboratorio de Ecología Microbiana, Facultad de Ciencias Biológicas de Universidad Nacional Mayor de San Marcos, Lima, Perú. Laboratorio de Microbiología, Hospital Militar Central “Luis Arias Schereiber”, Lima, Perú. https://orcid.org/0000-0001-6617-6402
  • Liliana Morales Laboratorio de Microbiología Hospital Nacional Guillermo Almenara Irigoyen, Lima, Perú. https://orcid.org/0000-0003-1435-5593
  • Jeanne Alba Luna Laboratorio de Ecología Microbiana, Facultad de Ciencias Biológicas de Universidad Nacional Mayor de San Marcos, Lima, Perú https://orcid.org/0000-0003-4304-1403
  • Lino Velasquez Garcia Laboratorio de Ecología Microbiana, Facultad de Ciencias Biológicas de Universidad Nacional Mayor de San Marcos, Lima, Perú https://orcid.org/0009-0006-7553-3268
  • Julio Daniel Pacheco Perez Laboratorio de Ecología Microbiana, Facultad de Ciencias Biológicas de Universidad Nacional Mayor de San Marcos, Lima, Perú https://orcid.org/0009-0008-3996-8090
  • Maria J. Pons Laboratorio de Genética Molecular y Bioquímica. Universidad Científica del Sur, Lima, Perú https://orcid.org/0000-0001-8384-2315

DOI:

https://doi.org/10.17843/rpmesp.2024.412.13246

Keywords:

Escherichia coli, antibiotic resistance, irrigation water, ESBL-producers, diarrhoeagenic E. coli

Abstract

Objetives. Bacterial resistance to antibiotics is a public health problem, however, few studies are performed in natural water ecosystems in middle-low-income countries. The objective of this study was to evaluate the presence and sensitivity to antimicrobials of Escherichia coli strains isolated from 24 irrigation water samples from the Rimac River in eastern Lima. Materials and methods. E.coli were identified by PCR. Antibiotic susceptibility was determined by disk diffusion method.  The extended-spectrum beta-lactamase (ESBL), quinolones and virulence involved genes were  determined by PCR. Results. All samples exceeded the permissible limits established in the Environmental Quality Standards for vegetable irrigation. Of the 94 strains, 72.3% showed resistance to at least one antibiotic, 24.5% were multidrug-resistant (MDR), and 2.1% were extremely drug resistant. The highest percentages of resistance were observed against nalidixic acid (50%), trimethoprim-sulfamethoxazole (35.5%) and ciprofloxacin (20.4%). Among the isolates, 3.2% presented ESBL phenotype related to blaCTX-M-15 gene. The transferable mechanisms of resistance to quinolones, qnrB were more frequent (20.4%), and 2.04% had the qnrS. It was determined that 5.3% were diarrheagenic E. coli and of these, 60% were enterotoxigenic E. coli, 20% were enteropathogenic E. coli and 20% were enteroaggregative E. coli. Conclusions. Our results show the existence  diarrheagenic pathotypes in water used to irrigate fresh produce and highlights the presence of ESBL-producers and MDR E. coli, demonstrating the role that irrigation water plays in disseminating resistance genes in Peru.

 

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References

Pons MJ, de Toro M, Medina S, Sáenz Y, Ruiz-Blázquez J. Antimicrobials, antibacterial resistance and sustainable health. South Sustainability. 2020; 1(1), e001 doi: 10.21142/SS-0101-2020-001.

Marti E, Variatza E, Balcazar JL. The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends Microbiol.2014;22(1):36-41. doi: 10.1016/j.tim.2013.11.001.

Freitas DY, Araújo S, Folador ARC, Ramos RTJ, Azevedo JSN, Tacão M, et al. Extended Spectrum Beta-Lactamase-Producing Gram-Negative Bacteria Recovered From an Amazonian Lake Near the City of Belém, Brazil. Front Microbiol.2019; 28;10:364. doi: 10.3389/fmicb.2019.00364.

Larsson DGJ, Flach CF. Antibiotic resistance in the environment. Nat Rev Microbiol.2022;20(5):257-269. doi: 10.1038/s41579-021-00649-x.

Duarte AC, Rodrigues S, Afonso A, Nogueira A, Coutinho P. Antibiotic Resistance in the Drinking Water: Old and New Strategies to Remove Antibiotics, Resistant Bacteria, and Resistance Genes. Pharmaceuticals (Basel). 2022;24;15(4):393. doi: 10.3390/ph15040393.

Blaustein RA, Shelton DR, Van Kessel JA, Karns JS, Stocker MD, Pachepsky YA. Irrigation waters and pipe-based biofilms as sources for

antibiotic-resistant bacteria. Environ Monit Assess.2016; 188(1):56. doi: 10.1007/s10661-015-5067-4.

Li Y, Zhang C, Mou X, Zhang P, Liang J, Wang Z. Distribution characteristics of antibiotic resistance bacteria and related genes in urban recreational lakes replenished by different supplementary water source. Water Sci Technol. 2022; 85(4):1176-1190. doi: 10.2166/wst.2022.018

Jiao YN, Chen H, Gao RX, Zhu YG, Rensing C. Organic compounds stimulate horizontal transfer of antibiotic resistance genes in mixed wastewater treatment systems. Chemosphere.2017; 184:53-61. doi: 10.1016/j.chemosphere.2017.05.149.

Gupta S, Graham DW, Sreekrishnan TR, Ahammad SZ. Effects of heavy metals pollution on the co-selection of metal and antibiotic resistance in urban rivers in UK and India. Environ Pollut. 2022; 28:119326. doi: 10.1016/j.envpol.2022.119326.

Poirel L, Kämpfer P, Nordmann P Chromosome-encoded Ambler class A beta-lactamase of Kluyvera georgiana, a probable progenitor of a subgroup of CTX-M extended-spectrum beta-lactamases. Antimicrob Agents Chemother. 2002; 46(12):4038-40. doi: 10.1128/AAC.46.12.4038-4040.2002

Riego MdDAy. Resultado del monitoreo de la calidad del agua en la cuenca del río Rímac: Informe técnico. Informe Técnico. Lima: Autoridad Nacional del Agua, Dirección de Gestión de Calidad de los Recursos Hídricos; 2012.

Castillo AK, Espinoza K, Chaves AF, Guibert F, Ruiz J, Pons MJ. Antibiotic susceptibility among non-clinical Escherichia coli as a marker of antibiotic pressure in Peru (2009-2019): one health approach. Heliyon.2022; 9;8(9):e10573. doi: 10.1016/j.heliyon.2022.e10573.

Foudraine DE, Strepis N, Stingl C, Ten Kate MT, Verbon A, Klaassen CHW, et al. Exploring antimicrobial resistance to beta-lactams, aminoglycosides and fluoroquinolones in E. coli and K. pneumoniae using proteogenomics. Sci Rep. 2021; 14;11(1):12472. doi: 10.1038/s41598-021-91905-w.

Palma N, Pons MJ, Gomes C, Mateu J, Riveros M, García W, et al. Resistance to quinolones, cephalosporins and macrolides in Escherichia coli causing bacteraemia in Peruvian children. J Glob Antimicrob Resist.2017; 11:28-33. doi: 10.1016/j.jgar.2017.06.011.

DIGESA. Protocolo para la toma de muestra. Resolución Directoral. Lima: Ministerio de Salud; 2016.

Bej AK, DiCesare JL, Haff L, Atlas RM. Detection of Escherichia coli and Shigella spp. in water by using the polymerase chain reaction and gene probes for uid. Appl Environ Microbiol. 1991;57(4):1013-7. doi: 10.1128/aem.57.4.1013-1017.

Clinical and Laboratory Standards Institute (CLSI) Performance Standards for Antimicrobial Susceptibility Testing. 31st ed. CLSI supplement M100 (ISBN 978-1-68440-105-5. Clinical and Laboratory Standards Institute, USA, 2021.

Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect.2012; 18:268-81. doi: 10.1111/j.1469-0691.2011.03570.

Guion CE, Ochoa TJ, Walker CM, Barletta F, Cleary TG. Detection of diarrheagenic Escherichia coli by use of melting-curve analysis and

real-time multiplex PCR. J Clin Microbiol, 2008; 46, 5, 1752–1757. doi: 10.1128/JCM.02341-07.

Pons MJ, Vubil D, Guiral E et al. Characterisation of extended-spectrum β-lactamases among Klebsiella pneumoniae isolates causing bacteraemia and urinary tract infection in Mozambique. J Glob Antimicrob Resist. 2015; 3(1):19-25. doi: 10.1016/j.jgar.2015.01.004.

Karkman A, Pärnänen K, Larsson DGJ. Fecal pollution can explain antibiotic resistance gene abundances in anthropogenically impacted environments. Nat Commun. 2019; 8;10(1):80. doi: 10.1038/s41467-018-07992-3.

Vega-Sánchez V, Talavera-Rojas M, Barba-León J, Zepeda-Velázquez AP, Reyes-Rodríguez NE. La resistencia antimicrobiana en Escherichia coli aislada de canales y heces bovinas de rastros en el centro de México. Rev Mex Cienc Pecu. 2020;11(4): 991-1003. doi: 10.22319/rmcp.v11i4.5073.

Ambiente Md. Aprueban Estándares de Calidad Ambiental (ECA) para Agua y Establecen Disposiciones Complementarias. DS N°

-2017-MINAM. Lima: MINAM; 2017

Riego MdDAy. Resultado del monitoreo de la calidad del agua en la cuenca del río Rímac: Informe técnico. Informe Técnico. Lima: Autoridad Nacional del Agua, Dirección de Gestión de Calidad de los Recursos Hídricos; 2012.

Graczyk Z, Graczyk TK, Naprawska A. A role of some food arthropods as vectors of human enteric infections. Cent Eur J Biol 2011; 6, 145–149. doi: 10.2478/s11535-010-0117-y.

Escobedo C, Ariza E. Nivel de contaminación fecal en hortalizas expedidas en mercados de Huanuco y su relación en el riego con aguas residuales no tratadas. Investigación Valdizana; 2014; 8(2).

Rojas-Aedo J, Morales O, Jara M, Morales O, Martínez MC. Detección de Salmonella spp. y E. coli diarreogénico en cursos de aguas superficiales de la Región Metropolitana por Ultrafiltración Tangencial. In Conference: Sociedad de Microbiología de Chile Chile. 2013; 1.

Ochoa TJ, Ecker L, Barletta F, Mispireta ML, Gil AI, Contreras C. Age-related susceptibility to infection with diarrheagenic Escherichia coli among infants from Periurban areas in Lima, Peru. Clin Infect Dis. 2009 1;49(11):1694-702. doi: 10.1086/648069.

Deblonde T, Cossu-Leguille C, Hartemann P. Emerging pollutants in wastewater: a review of the literature. Int J Hyg Environ Health.

;214(6):442-8. doi: 10.1016/j.ijheh.2011.08.002.

Duffy EA, Lucia LM, Kells JM, Castillo A, Pillai SD, Acuff GR. Concentrations of Escherichia coli and genetic diversity and antibiotic resistance profiling of Salmonella isolated from irrigation water, packing shed equipment, and fresh produce in Texas. J Food Prot.200568(1):70-9. doi: 10.4315/0362-028x-68.1.70.

Díaz-Gavidia C, Barría C, Weller DL, Salgado-Caxito M, Estrada EM, Araya A. Humans and Hoofed Livestock Are the Main Sources of Fecal Contamination of Rivers Used for Crop Irrigation: A Microbial Source Tracking Approach. Front Microbiol. 2022; 30;13:768527. doi: 10.3389/fmicb.2022.768527.

Nnadozie CF, Odume ON. Freshwater environments as reservoirs of antibiotic resistant bacteria and their role in the dissemination of antibiotic resistance genes. Environ Pollut. 2019; 254(Pt B):113067. doi: 10.1016/j.envpol.2019.11306.

Fahrenfeld N, Ma Y, O’Brien M, Pruden A. Reclaimed water as a reservoir of antibiotic resistance genes: distribution system and irrigation implications. Front Microbiol. 2013; 28;4:130. doi: 10.3389/fmicb.2013.00130.

Riaz L, Mahmood T, Khalid A, Rashid A, Ahmed-Siddique MB, Kamal A, et al. Fluoroquinolones in the environment: A review on their abundance, sorption and toxicity in soil. Chemosphere.2018; 191:704-720. doi: 10.1016/j.chemosphere.2017.10.09.

Pons M, Mosquito S, Gomes C, Del Valle LJ, Ochoa TJ, Ruiz J. Analysis of quinolone-resistance in commensal and diarrheagenic Escherichia coli isolates from infants in Lima, Peru. Trana R Soc Trop Med Hyg. 2014; 108(1):22-8. doi: 10.1093/trstmh/trt106.

Pons M, Mosquito S, Ochoa T. Niveles de Resistencia a antimicrobianos, en especial a quinolonas, en cepas de Escherichia coli comensales en niños de la zona periurbana de Lima, Perú. Rev Peru Med Exp Salud Pública. 2012;29(1):82-6.

Miranda CD, Concha C, Godoy FA, Lee MR. Aquatic Environments as Hotspots of Transferable Low-Level Quinolone Resistance and Their Potential Contribution to High-Level Quinolone Resistance. Antibiotics. 2022; 11(11):1487. doi: 10.3390/antibiotics11111487.

Kraupner N, Ebmeyer S, Bengtsson-Palme J, Fick J, Kristiansson E, Flach CF, et al. Selective concentration for ciprofloxacin resistance in Escherichia coli grown in complex aquatic bacterial biofilms. Environ Int. 2018;116:255-268. doi: 10.1016/j.envint.2018.04.029.

Dong Z, Wang J, Wang L, Zhu L, Wang J, Zhao X. Distribution of quinolone and macrolide resistance genes and their co-occurrence with heavy metal resistance genes in vegetable soils with long-term application of manure. Environ Geochem Health. 2021: 24. doi: 10.1007/s10653-021-01102-x.

Palacios Farias, SE. 2019 “Frecuencia de Escherichia coli resistente a antibióticos aisladas del agua del río Piura, Perú en un tramo de la ciudad”. Universidad Nacional de Piura. http://repositorio.unp.edu.pe/handle/UNP/1957

Montero L, Irazabal J, Cardenas P, Graham JP, Trueba G. Extended-Spectrum Beta-Lactamase Producing-Escherichia coli Isolated From Irrigation Waters and Produce in Ecuador. Front Microbiol. 2021; 4;12:709418. doi: 10.3389/fmicb.2021.709418. Erratum in: Front Microbiol. 2022 Jun 14;13:926514. PMID: 34671324.

Published

2024-06-21

Issue

Section

Original Article

How to Cite

1.
Huamán Iturrizaga M, Salvador-Luján G, Morales L, Luna JA, Velasquez Garcia L, Pacheco Perez JD, et al. Resistance to cephalosporins and quinolones by Escherichia coli isolated from irrigation water from eastern Lima, Perú. Rev Peru Med Exp Salud Publica [Internet]. 2024 Jun. 21 [cited 2024 Jul. 25];41(2):114-20. Available from: https://rpmesp.ins.gob.pe/index.php/rpmesp/article/view/13246

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