Resistance profile of Escherichia coli strains in micro-basins with different soil use and occupation, in the Northwest of Rio Grande do Sul, Brazil

Ubiratan Alegransi Bones; Genesio Mario da Rosa; Kauane Andressa Flach; Jefferson Alves da Costa Junior; Nelson Emanoel Freitas Endres

doi:10.5327/Z2176-94782175

Authors

Ubiratan Alegransi Bones Universidade Federal de Santa Maria (UFSM) - Brazil https://orcid.org/0000-0002-2220-5686
Genesio Mario da Rosa Universidade Federal de Santa Maria (UFSM) - Brazil https://orcid.org/0000-0003-1247-2286
Kauane Andressa Flach Universidade Federal de Santa Maria (UFSM) - Brazil https://orcid.org/0000-0001-8915-3289
Jefferson Alves da Costa Junior Universidade Federal de Santa Maria (UFSM) - Brazil https://orcid.org/0000-0001-7572-3930
Nelson Emanoel Freitas Endres Universidade Federal de Santa Maria (UFSM) - Brazil https://orcid.org/0009-0005-0574-1267

DOI:

https://doi.org/10.5327/Z2176-94782175

Keywords:

bacterial resistance; water contamination; sanitary effluents

Abstract

Escherichia coli, a highly adaptive microorganism, has gained scientific interest due to its rapid mutation and resistance to antimicrobial treatments. The primary sources that contribute to its rapid spread and the emergence of infections remain hotly debated. Thus, the objective of this research was to provide a baseline, as the first study in the region that analyzes the microbiological quality of water in micro-basins with different characteristics of land use and occupation. Intending to identify whether there is resistance in the isolated strains of E. coli and what their possible origins are, the study provides a behavior modeling of the studied area. To this end, three sampling campaigns were carried out, from which these microorganisms were isolated and identified by polymerase chain reaction, and were subsequently subjected to susceptibility tests with nine antibacterials widely used in the treatment of infections caused by this bacterial species. Theresultsrevealed that the watershed receiving urban sanitary effluents presented the highest contamination levels, with persistent multidrug-resistant strains throughout the collection period. Among all strains, 80% were resistant to ampicillin, while 33.3% showed resistance to cefazolin. Levofloxacinwas the most effective antibiotic, with 100% susceptibility. Micro-basins with predominant agricultural and pasture activities demonstrated less resistance than urban-impacted areas. Thishighlights the urgent need for constant monitoring and further studies to uncover the main determinants of this urgent ecological and public health problem.

.

Downloads

Download data is not yet available.

References

Alawi, M.; Torrijos, T. V.; Walsh, F., 2022. Plasmid-mediated antimicrobial resistance in drinking water. Environmental Advances, v. 8, 100191. https://doi.org/10.1016/j.envadv.2022.100191.

Associação de Criadores de Suínos do Rio Grande do Sul (ACSURS), 2019. Rebanho Suíno Efetivo RS – 2019 (Accessed February 07, 2024) at:. https://acsurs.com.br/wp-content/uploads/2021/03/Rebanho-Suino-Efetivo-RS-2019.pdf.

Astal, Z.; Sharif, F.A.; Abdallah, S.A.; Fahd, M.I., 2002. Multiresistant Escherichia coli isolated from women with community-acquired urinary tract infections in the Gaza Strip. Journal of chemotherapy (Florence, Italy), v. 14 (6), 637-638. https://doi.org/10.1179/joc.2002.14.6.637.

Balakumar, P.; Rohilla, A.; Thangathirupathi, A., 2010. Gentamicin-induced nephrotoxicity: do we have a promising therapeutic approach to blunt it? Pharmacological Research, v. 62 (3), 179-186. https://doi.org/10.1016/j.phrs.2010.04.004.

Barathe, P.; Kaur, K.; Reddy, S.; Shriram, V.; Kumar, V., 2024. Antibiotic pollution and associated antimicrobial resistance in the environment, Journal of Hazardous Materials Letters, v. 5, 100105. https://doi.org/10.1016/j.hazl.2024.100105.

Barnhart, E., 1989. Physicians' Desk Reference. 43rd ed. Medical Economics, Oradell, NJ, 303 p.

Bauer, A.W., 1966. Antibiotic susceptibility testing by a standardized single diffusion method. American Journal of Clinical Pathology, v. 45 (4), 493-496. PMID: 5325707.

Brasil, 2000. Ministério do Meio Ambiente (MMA). Resolução CONAMA nº 274, de 29 de novembro de 2000. Diário Oficial da União.

Brasil, 2005. Ministério do Meio Ambiente (MMA). Resolução CONAMA nº 357, de 15 de junho de 2005. Diário Oficial da União.

Brasil, 2013. Vigilância Ambiental em Saúde. Manual Prático de Análise de Água. Fundação Nacional de Saúde. Vigilância Ambiental em Saúde, Brasília.

Brasil, 2023. Ministério da Saúde. Dados surtos de DTHA - 2000 a 2021 (Accessed February 10, 2023) at:. https://docs.google.com/spreadsheets/d/1XT4iffaWUcMgU_t- Q0mKZhX1UHUJsJxi/edit#gid=1026946243.

Brazilian Committee on Antimicrobial Susceptibility Testing (BrCAST), 2022. Tabela pontos de corte clínicos (Accessed August 12, 2022) at:. https://brcast.org.br/documentos/documentos-3/.

Bundrick, W.; Heron, S.P.; Ray, P.; Schiff, W.M.; Tennenberg, A.M.; Wiesinger, B.A.; Wright, P.A.; Wu, S.C.; Zadeikis, N.; Kahn, J.B., 2003. Levofloxacin versus ciprofloxacin in the treatment of chronic bacterial prostatitis: a randomized double-blind multicenter study. Urology, v. 62 (3), 537-541. https://doi.org/10.1016/S0090-4295(03)00565-X.

Cao, S.T.; Tran, H.P.; Le, H.T.T.; Bui, H.P.K.; Nguyen, G.T.H.; Nguyen, L.T.; Nguyen, B T.; Luong, A.D., 2021. Impacts of effluent from different livestock farm types (pig, cow, and poultry) on surrounding water quality: a comprehensive assessment using individual parameter evaluation method and water quality indices. Environmental Science and Pollution Research, v. 28, 50302-50315. https://doi.org/10.1007/s11356-021-14284-9.

Centers for Disease Control and Prevention (CDC), 2019. Antibiotic resistance threats in the United States. US Department of Health and Human Services, Atlanta.

Center for Disease Control and Prevention (CDC), 2023. Understanding antibiotic resistance in water: a one health approach (Accessed January 08, 2023) at:. https://www.cdc.gov/onehealth/in-action/understanding-antibiotic-resistance-in- water.html.

Crisigiovanni, E.L.; Nascimento, E.A.; Godoy, R.F.B; Oliveira-Filho, P.C.; Vidal, C.M.S.; Martins, K.G., 2020. Inadequate riparian zone use directly decreases water quality of a low-order urban stream in southern Brazil. Revista Ambiente & Água, v. 15 (2), e2451. https://doi.org/10.4136/ambi-agua.2451.

Cycoń, M.; Mrozik, A.; Piotrowska-Seget, Z., 2019. Antibiotics in the soil environment—degradation and their impact on microbial activity and diversity. Frontiers in Microbiology, v. 10, 338. https://doi.org/10.3389/fmicb.2019.00338.

Dávalos-Almeyda, M.; Guerrero, A.; Medina, G.; Dávila-Barclay, A.; Salvatierra, G.; Calderón, M.; Gilman, R.H.; Tsukayama, P., 2022. Antibiotic use and resistance knowledge assessment of personnel on chicken farms with high levels of antimicrobial resistance: a cross-sectional survey in Ica, Peru. Antibiotics, v. 11 (2), 190. https://doi.org/10.3390/antibiotics11020190.

Food and Agriculture Organization of The United States (FAO), 2023. Agriculture: cause and victim of water pollution, but change is possible (Accessed March 28, 2023) at:. https://www.fao.org/land-water/news-archive/news-detail/en/c/1032702/.

Food and Agriculture Organization of The United States (FAO); United Nations Environment Programme (UNEP), 2020. The State of the World’s Forests 2020. Forests, biodiversity and people. FAO; UNEP, Rome.

Flach, K.A.; Bisognin, R.P.; Rosa, G.M. da; Bones, U.A.; Sipert, W.W., 2024. Avaliação do uso e cobertura da terra e da qualidade da água da Sub-bacia do Lajeado Pardo no Noroeste do Rio Grande do Sul. Revista de Geografia, 40 (3), 159-184. https://doi.org/10.51359/2238-6211.2023.258614.

Foulds, G., 1986. Pharmacokinetics of sulbactam/ampicillin in humans: a review. Reviews of Infectious Diseases, v. 8 (Supplement 5), S503-S511. https://doi.org/10.1093/clinids/8.supplement_5.503.

Geurtsen, J.; de Been, M.; Weerdenburg, E.; Zomer, A.; McNally, A.; Poolman, J., 2022. Genomics and pathotypes of the many faces of Escherichia coli. FEMS Microbiology Reviews, v. 46 (6), fuac031. https://doi.org/10.1093/femsre/fuac031

Gupta, D.; Dubey, J.; Kumar, M., 2016. Phytochemical analysis and antimicrobial activity of some medicinal plants against selected common human pathogenic microorganisms. Asian Pacific Journal of Tropical Disease, v. 6 (1), 15-20. https://doi.org/10.1016/S2222-1808(15)60978-1.

Hadifar, S.; Mohsen, M.; Nematollahi, S.; Ramazanzadeh, R.; Sedighi, M.; Salehi-Abargouei, A.; Miri, A., 2017. Epidemiology of multidrug resistant uropathogenic Escherichia coli in Iran: a systematic review and meta-analysis. Japanese Journal of Infectious Diseases, v. 70 (1), 19-25. https://doi.org/10.7883/yoken.JJID.2015.652.

Holcomb, D.A.; Stewart, J.R., 2020. Microbial indicators of fecal pollution: recent progress and challenges in assessing water quality. Current Environmental Health Reports, v. 7, 311-324. https://doi.org/10.1007/s40572-020-00278-1.

Instituto Brasileiro de Geografia e Estatística (IBGE), 2020. Monitoramento da Cobertura e Uso da Terra (Accessed February 05, 2023) at:. https://www.ibge.gov.br/geociencias/informacoes- ambientais/cobertura-e-uso-da-terra/15831-cobertura-e-uso-da-terra-do-brasil.html.

Instituto Brasileiro de Geografia e Estatística (IBGE), 2023. Instituto Brasileiro de Geografia e Estatística. Cidades e Estados: Frederico Westphalen. Frederico Westphalen (Accessed February 07, 2023) at:. https://www.ibge.gov.br/cidades-e-estados/rs/frederico-westphalen.html.

Instituto Nacional de Pesquisas Espaciais (INPE), 2022. Divisão de geração de imagens (Accessed January 12, 2023) at:. http://www2.dgi.inpe.br/catalogo/explore.

Jariyapamornkoon, N.; Nuanualsuwan, S.; Suanpairintr, N., 2024. In vitro antibacterial activities of fosfomycin against Escherichia coli isolates from canine urinary tract infection. Animals, v. 14 (13), 1916. https://doi.org/10.3390/ani14131916.

Kadri, K., 2019. Polymerase chain reaction (PCR): principle and applications. Synthetic Biology-New Interdisciplinary Science, London.

Kadykalo, S.; Thomas, J.; Parmley, E. J.; Pintar, K.; Fleury, M., 2020. Antimicrobial resistance of Salmonella and generic Escherichia coli isolated from surface water samples used for recreation and a source of drinking water in southwestern Ontario, Canada. Zoonoses and Public Health, v. 67 (5), 566-575. https://doi.org/10.1111/zph.12720.

Konzen, I.S.; Gamboa, A.; Gaida, W.; Rosa, G.M. da; Flach, K.A.; Bones, U.A.; Breunig, F.M.; Mendonça, Â.M.; Mahnke, M.R.; Maciel, D.H., 2024. Impact of anthropogenic activities and land use on water quality: an analysis in microbasins in Rio Grande do Sul, Brazil. Hygeia - Revista Brasileira de Geografia Médica e da Saúde, Uberlândia, v. 20, e2070. https://doi.org/10.14393/Hygeia2071633.

Kouadio-Ngbesso, N.; Atobla, K.; Attien, P.Y.; Kouame-Sina, M.; Koffi, R.A.; Adingra, A.A.; Dadié, A., 2019. Comparative biotypic and phylogenetic profiles of Escherichia coli isolated from resident stool and lagoon in Fresco (Côte d’Ivoire). International Journal of Microbiology, 9708494. https://doi.org/10.1155/2019/9708494.

Kuwiatz, M.E., 2021. A contribuição da suinocultura na economia do município de Taquaraçu do Sul/RS. Produção Intelectual – Uergs, Frederico Westphalen.

Larsson, D.G.J.; Flach, C.F., 2022. Antibiotic resistance in the environment. Nature Reviews Microbiology, v. 20, 257-269. https://doi.org/10.1038/s41579-021-00649-x.

Li, P.; Wu, J., 2019. Drinking water quality and public health. Exposure and Health, v. 11, 73-79. https://doi.org/10.1007/s12403-019-00299-8.

Manyi-Loh, C.; Mamphweli, S.; Meyer, E.; Okoh, A., 2018. Antibiotic use in agriculture and its consequential resistance in environmental sources: potential public health implications. Molecules (Basel, Switzerland), v. 23 (4), 795. https://doi.org/10.3390/molecules23040795.

Martins, W.A.; Martins, L.L.; Maria, I.C.D.; Moraes, J.F.L.; Pedro Júnior, M.J., 2021. Reduction of sediment yield by riparian vegetation recovery at distinct levels of soil erosion in a tropical watershed. Ciência e Agrotecnologia, v. 45, e028220. https://doi.org/10.1590/1413-7054202145028220.

Mbelle, N.M.; Feldman, C.; Sekyere, J.O.; Maningi, N.E.; Modipane, L.; Essack, S.Y., 2019. The resistome, mobilome, virulome and phylogenomics of multidrug-resistant Escherichia coli clinical isolates from Pretoria, South Africa. Scientific Reports, v. 9 (1), 16457. https://doi.org/10.1155/2019/9708494.

McDaniels, A.E.; Rice, E.W.; Reyes, A.L.; Johnson, C.H.; Haugland, R.A.; Stelma, G.N. Jr., 1996. Confirmational identification of Escherichia coli, a comparison of genotypic and phenotypic assays for glutamate decarboxylase and beta- D-glucuronidase. Applied and Environmental Microbiology, v. 62 (9), 3350- 3354. https://doi.org/10.1128/aem.62.9.3350-3354.1996.

Murray, C.J.L., 2022. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. The Lancet, v. 399 (10325), 629-655. https://doi.org/10.1016/S0140-6736(21)02724-0.

Odonkor, S.T.; Addo, K.K., 2018. Prevalence of multidrug-resistant Escherichia coli isolated from drinking water sources. International Journal of Microbiology, 7204013. https://doi.org/10.1155/2018/7204013.

Paitan, Y., 2018. Current trends in antimicrobial resistance of Escherichia coli. Current Topics in Microbiology and Immunology, v. 416, 181-211. https://doi.org/10.1007/82_2018_110.

Peng, X.; Yu, K.-Q.; Deng, G.-H.; Jiang, Y.-X.; Wang, Y.; Zhang, G.-X.; Zhou, H.-W., 2013. Comparison of direct boiling method with commercial kits for extracting fecal microbiome DNA by Illumina sequencing of 16S rRNA tags. Journal of Microbiological Methods, v. 95 (3), 455-462. https://doi.org/10.1016/j.mimet.2013.07.015.

Phillips, I.; King, A.; Rowe, B.; Eykyn, S.; Gransden, W.R.; Frost, J.A.; Gross, R.J., 1998. Epidemic multiresistant Escherichia coli infection in West Lambeth health district. The Lancet, 1988, v. 331 (8593), 1038-1041. https://doi.org/10.1016/S0140-6736(88)91853-3.

Pillonetto, M.; Jordão, R.T.S.; Andraus, G.S.; Bergamo, R.; Rocha, F.B.; Onishi, M.C.; Almeida, B.M.M.; Nogueira, K.S.; Dal Lin, A.; Dias, V.M.C.H.; Abreu, A.L., 2021. The experience of implementing a national antimicrobial resistance surveillance system in Brazil. Frontiers in Public Health, v. 8, 575536. https://doi.org/10.3389/fpubh.2020.575536.

Polianciuc, S.I.; Gurzău, A.E.; Kiss, B.; Ştefan, M.G.; Loghin, F., 2020. Antibiotics in the environment: causes and consequences. Medicine and Pharmacy Reports, v. 93 (3), 231-240. https://doi.org/10.15386/mpr-1742.

Porres-Osante, N.; Azcona-Gutiérrez, J.M.; Rojo-Bezares, B.; Undabeitia, E.; Torres, C.; Sáenz, Y., 2014. Emergence of a multiresistant KPC-3 and VIM-1 carbapenemase-producing Escherichia coli strain in Spain. Journal of Antimicrobial Chemotherapy, v. 69 (7), 1792-1795. https://doi.org/10.1093/jac/dku055.

Ram, S.; Vajpayee, P.; Tripathi, U.; Singh, R. L.; Seth, P. K.; Shanker, R., 2008. Determination of antimicrobial resistance and virulence gene signatures in surface water isolates of Escherichia coli. Journal of Applied Microbiology, v. 105 (6), 1899-1908. https://doi.org/10.1111/j.1365-2672.2008.03879.x.

Raman, G.; McMullan, B.; Taylor, P.; Mallitt, K.-A.; Kennedy, S.E., 2018. Multiresistant E. coli urine infections in children: a case– control study. Archives of Disease in Childhood, v. 103 (4), 336-340. https://doi.org/10.1136/archdischild-2017-312831.

Rice, E.W., 2012. Standard Methods for the Examination of Water and Wastewater. American Public Health Association, Washington, DC.

Ritter, L.G.; Renz, V.D.; Garlet, G.; Chagas, P.; Mancuso, M.A.; Haas, A.; Conceição, S.R., 2015. Manejo da Micro Bacia do Lajeado Pardo. HOLOS, v. 6, 123-130. https://doi.org/10.15628/holos.2015.1685.

Salleh, M.Z.; Nik Zuraina, N.M.N.; Hajissa, K.; Ilias, M.I.; Deris, Z.Z., 2022. Prevalence of multidrug-resistant diarrheagenic Escherichia coli in Asia: A systematic review and meta-analysis. Antibiotics, 11 (10), 1333. https://doi.org/10.3390/antibiotics11101333.

Savin, M.; Alexander, J.; Bierbaum, G.; Hammerl, J.A.; Hembach, N.; Schwartz, T.; Schmithausen, R.M.; Sib, E.; Voigt, A.; Kreyenschmidt, J., 2021. Antibiotic-resistant bacteria, antibiotic resistance genes, and antibiotic residues in wastewater from a poultry slaughterhouse after conventional and advanced treatments. Scientific Reports, v. 11 (1), 16622. https://doi.org/10.1038/s41598-021-96169-y.

Shah, N.W.; Baillie, B.R.; Bishop, K.; Ferraz, S.; Högbom, L.; Nettles, J., 2022. The effects of forest management on water quality. Forest Ecology and Management, v. 522, 120397. https://doi.org/10.1016/j.foreco.2022.120397.

Silva, J.C.A.; Porto, M.F.A.; Brandimarte, A.L.; Martins, J.R.S., 2015. Utilização de índices físicos, químicos e biológicos para avaliação da qualidade de corpos d-água em processo de recuperação: Córrego Ibiraporã, SP. RBRH: Revista Brasileira de Recursos Hídricos, v. 20, 959-969. https://doi.org/10.21168/rbrh.v20n4.p959-969.

Silva, L.O.P.; Estevam, L.B.; Rocha Nogueira, J.M., 2024. Disseminação da resistência aos antimicrobianos no contexto de saúde única: uma breve revisão. Revista Brasileira de Análises Clínicas, v. 56 (1), 5-11. https://doi.org/10.21877/2448-3877.202400149.

Sojo-Dorado, J.; López-Hernández, I.; Rosso-Fernandez, C.; Morales, I.M.; Palacios-Baena, Z.R.; Hernández-Torres, A.; Merino de Lucas, E.; Escolà-Vergé, L.; Bereciartua, E.; García-Vázquez, E.; Pintado, V.; Boix-Palop, L.; Natera-Kindelán, C.; Sorlí, L.; Borrell, N.; Giner-Oncina, L.; Amador-Prous, C.; Shaw, E.; Jover-Saenz, A.; Molina, J.; Martínez-Alvarez, R.M.; Dueñas, C.J.; Calvo-Montes, J.; Silva, J.T.; Cárdenes, M.A.; Lecuona, M.; Pomar, V.; Valiente de Santis, L.; Yagüe-Guirao, G.; Lobo-Acosta, M.A.; Merino-Bohórquez, V.; Pascual, A.; Rodríguez-Baño, J.; REIPI-GEIRAS-FOREST group, 2022. Effectiveness of fosfomycin for the treatment of multidrug-resistant Escherichia coli bacteremic urinary tract infections: a randomized clinical trial. JAMA Network Open, v. 5 (1), e2137277. https://doi/10.1001/jamanetworkopen.2021.37277.

United States Geological Survey (USGS), 2019. Agricultural Contaminants Report (Accessed February 07, 2024) at:. https://www.usgs.gov/mission-areas/water-resources/science/agricultural- contaminants#:~:text=Agricultural%20contaminants%20can%20impair%20the,streams

Wen, X.; Chen, F.; Lin, Y.; Zhu, H.; Yuan, F.; Kuang, D.; Jia, Z.; Yuan, Z., 2020. Microbial indicators and their use for monitoring drinking water quality—A review. Sustainability, v. 12, 2249. https://doi.org/10.3390/su12062249.

Woodford, N.; Kaufmann, M.E.; Karisik, E.; Hartley, J.W., 2007. Molecular epidemiology of multiresistant Escherichia coli isolates from community-onset urinary tract infections in Cornwall, England. Journal of Antimicrobial Chemotherapy, v. 59, 106-109. https://doi.org/10.1093/jac/dkl435.

World Health Organization (WHO). Record number of countries contribute data revealing disturbing rates of antimicrobial resistance. 2020 (Accessed January 05, 2023) at:. https://www.who.int/news/item/01-06-2020-record-number-of-countries-contribute- data-revealing-disturbing-rates-of-antimicrobial-resistance.

World Health Organization (WHO), 2021. Global antimicrobial resistance and use surveillance system (GLASS) report: 2021. WHO, Geneva.

World Health Organization (WHO). 2022 Global antimicrobial resistance and use surveillance system (GLASS) report 2022. WHO, Geneva.

World Organization for Animal Health (WOAH), 2023. Annual Report on Antimicrobial Agents Intended for Use in Animals 8th Report (Accessed February 07, 2024) at:. https://www.woah.org/app/uploads/2024/05/woah-amu-report-2024-final.pdf

Wright, E.D.; Perinpanayagam, R.M., 1987. Multiresistant invasive Escherichia coli infection in south London. The Lancet, v. 329 (8532), 556-557. https://doi.org/10.1016/s0140-6736(87)90190-5.

Xue, Z.; Xiang, Y.; Li, Y.; Yang, Q., 2021. A systematic review and meta-analysis of levofloxacin and ciprofloxacin in the treatment of urinary tract infection. Annals of Palliative Medicine, v. 10, 9765-9771. https://doi.org/ 10.21037/apm-21-2042.

Yamagishi, J.; Sato, Y.; Shinozaki, N.; Ye, B.; Tsuboi, A.; Nagasaki, M.; Yamashita, R., 2016. Comparison of boiling and robotics automation method in DNA extraction for metagenomic sequencing of human oral microbes. PLoS One, v. 11 (4), e0154389. https://doi.org/10.1371/journal.pone.0154389.

Zhanel, G.G.; Zhanel, M.A.; Karlowsky, J.A., 2018. Oral fosfomycin for the treatment of acute and chronic bacterial prostatitis caused by multidrug-resistant Escherichia coli. Canadian Journal of Infectious Diseases and Medical Microbiology, v. 2018, 1404813. https://doi.org/10.1155/2018/1404813.