Abstract
Benzimidazoles (BZ) are among the most used drugs to treat parasitic diseases in both human and veterinary medicine. In this study, solutions fortified with albendazole (ABZ), fenbendazole (FBZ), and thiabendazole (TBZ) were subjected to photoperoxidation (UV/H2O2). The hydroxyl radicals generated by the process removed up to 99% of ABZ, and FBZ, in the highest dosage of H2O2 (i.e., 1.125 mmol L-1; 4.8 kJ L-1). In contrast, 20% of initial TBZ concentration remained in the residual solution. In the first 5 min of reaction (i.e., up to 0.750 mmol L-1 of H2O2), formation of the primary metabolites of ABZ—ricobendazole (RBZ), albendazole sulfone (ABZ-SO2), and oxfendazole (OFZ)—was observed. However, these reaction products were converted after the reaction time was doubled. The residual ecotoxicity was investigated using the Raphidocelis subcapitata microalgae and the marine bacteria Vibrio fischeri. The results for both microorganisms evidence that the residual solutions are less harmful to these microorganisms. However, after 30 min of reaction, the treated solution still presents a toxic effect for V. fischeri, meaning that longer reaction times are required to achieve an innocuous effluent.
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Data availability
All data generated or analyzed during this study are included in this published article and its supplementary information files. The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Associação Brasileira de Normas Técnicas, ABNT. (2018). NBR 12648: Ecotoxicologia aquática—Toxicidade crônica—Método de ensaio com algas (Chlophyceae) ( 2nd ed., 27pp). Rio de Janeiro: Author.
Caianelo M, Rodrigues-Silva C, Maniero MG, Guimarães JR (2016) Antimicrobial activity against Gram-positive and Gram-negative bacteria during gatifloxacin degradation by hydroxyl radicals. Environ Sci Pollut Res. 24:6288–6298. https://doi.org/10.1007/s11356-016-6972-y
Cao J, Jiang R, Wang J, Sun J, Feng Q, Zhao Z, Chen G, Zhou C, Yin E (2018) Study on the interaction mechanism between cefradine and Chlamydomonas reinhardtii in water solutions under dark condition. Ecotoxicol Environ Saf 159:56–62. https://doi.org/10.1016/j.ecoenv.2018.04.068
Carusso S, Juárez AB, Moretton J, Magdaleno A (2018) Effects of three veterinary antibiotics and their binary mixtures on two green alga species. Chemosphere 194:821–827. https://doi.org/10.1016/j.chemosphere.2017.12.047
Chassaing C, Berger M, Heckeroth A, Ilg T, Jaeger M, Kern C, Schmid K, Uphoff M (2008) Highly water-soluble prodrugs of anthelmintic benzimidazole carbamates: synthesis, pharmacodynamics, and pharmacokinetics. J Med Chem 51:1111–1114. https://doi.org/10.1021/jm701456r
Cho C, Jeon Y, Pham TPT, Vijayaraghavan K, Yun Y (2008) The ecotoxicity of ionic liquids and traditional organic solvents on microalga Selenastrum capricornutum. Ecotoxicology and Environmental Safety 71:166–171
Costa CR, Olivi P, Botta CMR, Espindola ELG (2008) A toxicidade em ambientes aquáticos: discussão e métodos de avalia̧ão. Quim Nova 31:1820–1830. https://doi.org/10.1590/S0100-40422008000700038
Diniz V, Reyes GM, Rath S, Cunha DG (2020) Caffeine reduces the toxicity of albendazole and carbamazepine to the microalgae Raphidocelis subcapitata (Sphaeropleales, Chlorophyta). Int Rev Hydrobiol 105:151–161. https://doi.org/10.1002/iroh.201902024
Gottschall DW, Theodorides VJ, Wang R (1990) The metabolism of benzimidazole. Parasitol Today 6:10
Horvat AJM, Babić S, Pavlović DM, Ašperger D, Pelko S, Kaštelan-Macan M, Petrović M, Mance AD (2012) Analysis, occurrence and fate of anthelmintics and their transformation products in the environment. TrAC - Trends Anal Chem 31:61–84. https://doi.org/10.1016/j.trac.2011.06.023
ISO - 11348-3 - Water Quality – Determination of the inhibitory effect of water samples on the light emission of Vibrio fischeri (luminescent Bacteria Test) Part3: Method using freeze-dried bacteria (1998)
Jacob RS, Santos LVS, d'Auriol M, Lebron YAR, Moreira VR, Lange LC (2020) Diazepam, metformin, omeprazole and simvastatin: a full discussion of individual and mixture acute toxicity. Ecotoxicology 29:1062–1071. https://doi.org/10.1007/s10646-020-02239-8
Jung Y, Gi W, Yoon Y et al (2012) Science of the total environment removal of amoxicillin by UV and UV/H2O2 processes. Sci Total Environ 420:160–167. https://doi.org/10.1016/j.scitotenv.2011.12.011
Kanakaraju D, Glass BD, Oelgemöller M (2018) Advanced oxidation process-mediated removal of pharmaceuticals from water: a review. Journal of Environmental Management 219:189–207
Khan J, Shah NS, Khan HM (2015) Decomposition of atrazine by ionizing radiation : Kinetics , degradation pathways and influence of radical scavengers. Sep Purif Technol 156:140–147. https://doi.org/10.1016/j.seppur.2015.09.064
Koschorreck J, de Knecht J (2002) Environmental risk assessment of pharmaceuticals in the EU — a regulatory perspective. Pharm Environ 131:289–310. https://doi.org/10.1007/978-3-662-09259-0_22
Liu P, Zhang H, Feng Y et al (2014) Removal of trace antibiotics from wastewater : a systematic study of nanofiltration combined with ozone-based advanced oxidation processes 240:211–220. https://doi.org/10.1016/j.cej.2013.11.057
Malato S, Fernández-Ibáñez P, Maldonado MI, Blanco J, Gernjak W (2009) Decontamination and disinfection of water by solar photocatalysis: recent overview and trends. Catal Today 147:1–59. https://doi.org/10.1016/j.cattod.2009.06.018
Mansano AS, Moreira R, Vieira EM et al (2017) Effects of diuron and carbofuran and their mixtures on the microalgae Raphidocelis subcapitata. Ecotoxicol Environ Saf 142:312–321. https://doi.org/10.1016/j.ecoenv.2017.04.024
Miazek K, Brozek-pluska B (2019) Effect of PHRs and PCPs on microalgal growth , metabolism and microalgae-based bioremediation processes : a review. Int J Mol Sci 20:1–51
Nogueira RFP, Oliveira MC, Paterlini WC (2005) Simple and fast spectrophotometric determination of H2O2 in photo-Fenton reactions using metavanadate. Talanta 66:86–91. https://doi.org/10.1016/j.talanta.2004.10.001
Nogueira V, Lopes I, Rocha-Santos TAP, Rasteiro MG, Abrantes N, Gonçalves F, Soares AMVM, Duarte AC, Pereira R (2015) Assessing the ecotoxicity of metal nano-oxides with potential for wastewater treatment. Environmental Science and Pollution Research 22:13212–13224
Nygaard G, Komárek J, Kristiansen J, Skulberg OM (1987) Taxonomic designations of the bioassay alga NIVA-CHL 1 (“Selenastrum capricornutum”) and some related strains /. Opera Bot 90:1–46
Organization for Economic Cooperation & Development (OECD). (2011). OECD guideline for testing of chemicals, 201 (Alga, Growth Inhibition Test), Paris, France.
Oh SJ, Park J, Lee MJ, Park SY, Lee JH, Choi K (2006) Ecological hazard assessment of major veterinary benzimidazoles: acute and chronic toxicities to aquatic microbes and invertebrates. Environ Toxicol Chem 25:2221–2226. https://doi.org/10.1897/05-493R.1
WHO (World Health Organization) (2017) Guidelines for drinking-water quality: fourth edition incorporating the first addendum. World Health Organization, Geneva
Peteffi GP, Fleck JD, Kael IM, Girardi V, Bündchen R, Krajeski DM, Demoliner M, Silva FP, da Rosa DC, Antunes MV, Linden R (2018) Caffeine levels as a predictor of Human mastadenovirus presence in surface waters—a case study in the Sinos River basin—Brazil. Environ Sci Pollut Res 25:15774–15784. https://doi.org/10.1007/s11356-018-1649-3
Petrović M, Škrbić B, Živančev J, Ferrando-Climent L, Barcelo D (2014) Determination of 81 pharmaceutical drugs by high performance liquid chromatography coupled to mass spectrometry with hybrid triple quadrupole-linear ion trap in different types of water in Serbia. Sci Total Environ 468–469:415–428. https://doi.org/10.1016/j.scitotenv.2013.08.079
Pinto AC, Barreiro EJ (2013) Desafios da indústria farmacêutica Brasileira. Quim Nova 36:1557–1560. https://doi.org/10.1590/S0100-40422013001000012
Porto RS, Rodrigues-Silva C, Schneider J, Rath S (2019) Benzimidazoles in wastewater: analytical method development, monitoring and degradation by photolysis and ozonation. J Environ Manage 232:729–737. https://doi.org/10.1016/j.jenvman.2018.11.121
Ribeiro AR, Sures B, Schmidt TC (2018) Ecotoxicity of the two veterinarian antibiotics ceftiofur and cefapirin before and after photo-transformation. Sci Total Environ 619–620:866–873. https://doi.org/10.1016/j.scitotenv.2017.11.109
Rico A, Zhao W, Gillissen F, Lürling M, van den Brink PJ (2018) Effects of temperature, genetic variation and species competition on the sensitivity of algae populations to the antibiotic enrofloxacin. Ecotoxicol Environ Saf 148:228–236. https://doi.org/10.1016/j.ecoenv.2017.10.010
Saggioro EM, Oliveira AS, Buss DF, Magalhães DP, Pavesi T, Jimenéz M, Maldonado MI, Ferreira LFV, Moreira JC (2015) Photo-decolorization and ecotoxicological effects of solar compound parabolic collector pilot plant and artificial light photocatalysis of indigo carmine dye. Dyes and Pigments 113:571–580
SANASA Sociedade de Abastecimento de Água e Saneamento (2020) Report of results of analysis of treated water - central laboratory - TTA. 23 ed, available in: https://www.sanasa.com.br/document/analiseagua/2_2_2020922.pdf
Santos LHMLM, Araújo AN, Fachini A, Pena A, Delerue-Matos C, Montenegro MCBSM (2010) Ecotoxicological aspects related to the presence of pharmaceuticals in the aquatic environment. J Hazard Mater 175:45–95. https://doi.org/10.1016/j.jhazmat.2009.10.100
Seoane M, Esperanza M, Cid Á (2017) Cytotoxic e ff ects of the proton pump inhibitor omeprazole on the non-target marine microalga Tetraselmis suecica. Aquat Toxicol 191:62–72. https://doi.org/10.1016/j.aquatox.2017.08.001
Sharma S, Ruparelia JP, Patel ML (2011) A general review on advanced oxidation processes for waste water treatment. Inst Technol 382–481:8–10
Sim WJ, Kim HY, Choi SD, Kwon JH, Oh JE (2013) Evaluation of pharmaceuticals and personal care products with emphasis on anthelmintics in human sanitary waste, sewage, hospital wastewater, livestock wastewater and receiving water. J Hazard Mater 248–249:219–227. https://doi.org/10.1016/j.jhazmat.2013.01.007
Spina-Cruz M, Maniero MG, Guimarães JR (2019) Advanced oxidation processes on doxycycline degradation: monitoring of antimicrobial activity and toxicity. Environ Sci Pollut Res 26:27604–27619. https://doi.org/10.1007/s11356-018-2149-1
Tan C, Gao N, Deng Y, Zhang Y, Sui M, Deng J, Zhou S (2013) Degradation of antipyrine by UV , UV/H2O2 and UV / PS. J Hazard Mater 260:1008–1016. https://doi.org/10.1016/j.jhazmat.2013.06.060
Terzic S, Udikovic-Kolic N, Jurina T, Krizman-Matasic I, Senta I, Mihaljevic I, Loncar J, Smital T, Ahel M (2018) Biotransformation of macrolide antibiotics using enriched activated sludge culture: kinetics, transformation routes and ecotoxicological evaluation. J Hazard Mater 349:143–152. https://doi.org/10.1016/j.jhazmat.2018.01.055
Välitalo P, Kruglova A, Mikola A, Vahala R (2017) Toxicological impacts of antibiotics on aquatic micro-organisms: a mini-review. Int J Hyg Environ Health 220:558–569. https://doi.org/10.1016/j.ijheh.2017.02.003
Von Sperling M (2007) Wastewater characteristics, treatment and disposal, vol 6. IWA publishing. https://doi.org/10.2166/9781780402086
Wagil M, Maszkowska J, Białk-Bielińska A, Stepnowski P, Kumirska J (2015) A comprehensive approach to the determination of two benzimidazoles in environmental samples. Chemosphere 119:S35–S41. https://doi.org/10.1016/j.chemosphere.2014.04.106
Yuan F, Hu C, Hu X, Wei D, Chen Y, Qu J (2011) Photodegradation and toxicity changes of antibiotics in UV and UV/H2O2 process. J Hazard Mater 185:1256–1263. https://doi.org/10.1016/j.jhazmat.2010.10.040
Zhang X, Li R, Jia M, Wang S, Huang Y, Chen C (2015) Degradation of ciprofloxacin in aqueous bismuth oxybromide (BiOBr) suspensions under visible light irradiation: a direct hole oxidation pathway. Chem Eng J 274:290–297. https://doi.org/10.1016/j.cej.2015.03.077
Zrnčić M, Gros M, Babić S, Kaštelan-Macan M, Barcelo D, Petrović M (2014) Analysis of anthelmintics in surface water by ultra high performance liquid chromatography coupled to quadrupole linear ion trap tandem mass spectrometry. Chemosphere 99:224–232. https://doi.org/10.1016/j.chemosphere.2013.10.091
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The authors acknowledge the financial support provided by FAPESP, CAPES, and CNPq. The detailed funding grant number is highlighted in the “Funding” section.
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This study is funded by the Brazilian agencies: The São Paulo Research Foundation – FAPESP, BRAZIL (grants #2013/09543-7, #2018/03571-2, and INCTAA-FAPESP #2014/50951-4). Scholarships were awarded to W.A.L.V and M.S for Coordination for the Improvement of Higher Education Personnel (CAPES) and C.R.-S. National Council for Scientific and Technological Development (CNPq, grant #154061/2018-2).
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All authors contributed to the study conception and design. Wilson Augusto Lima Venancio: methodology, validation, formal analysis, investigation, and visualization. Caio Rodrigues-Silva: methodology, supervision, visualization, writing—original draft, writing—review and editing, resources, and formal analysis. Mylena Spina: methodology, validation, and formal analysis. Vinicius Diniz: formal analysis, writing—original draft, writing—review and editing, and visualization. José Roberto Guimarães: supervision, project administration, and funding acquisition. The first draft of the manuscript was written by Caio Rodrigues-Silva and Vinicius Diniz; all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Venancio, W.A.L., Rodrigues-Silva, C., Spina, M. et al. Degradation of benzimidazoles by photoperoxidation: metabolites detection and ecotoxicity assessment using Raphidocelis subcapitata microalgae and Vibrio fischeri. Environ Sci Pollut Res 28, 23742–23752 (2021). https://doi.org/10.1007/s11356-020-11294-x
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DOI: https://doi.org/10.1007/s11356-020-11294-x