Acta Limnologica Brasiliensia
https://app.periodikos.com.br/journal/alb/article/doi/10.1590/S2179-975X3323
Acta Limnologica Brasiliensia
Artigo Original

A multibiomarker approach to investigate paracetamol effects in the reproduction regulatory axis of a male Neotropical catfish Rhamdia quelen

Uma abordagem de multibiomarcadores para investigar os efeitos do paracetamol no eixo de regulação da reprodução de machos do bagre Neotropical Rhamdia quelen

Maiara Carolina Perussolo; Maiara Vicentini; Leonardo Skarbek Lyra; Lucicleide Ângelo Silva; Mayara dos Santos Rodrigues; Leticia da Silva Pereira Fernandes; Luis Fernando Fávaro; Helena Cristina Silva de Assis

http://dx.doi.org/10.1590/S2179-975X3323 Acta Limnol. Bras. (Online), vol.35, e27, 2023
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Abstract

Aim: Paracetamol (PCM), or acetaminophen, is one of the most used drugs for human treatment of pain and fever. Since it has often been found in the aquatic environment, the aim of this study was to investigate the effects of PCM on the reproductive axis of male Rhamdia quelen catfish.

Methods: Different biomarkers were evaluated in hypothalamus, liver and gonads, as well as the plasma sexual hormone quantification. The fish were exposed to three PCM concentrations: 0.25, 2.5 and 25 µg.L-1 and to a control group (solvent acetone 0.0003%). After 14 days of exposure, fish were anesthetized, for blood sampling and biometrics, and after euthanasia, the tissues were sampled. Plasma was used for 11- keto testosterone and 17β - estradiol quantification. The hypothalamus was collected for brain aromatase (cyp19a1b) gene expression; the liver for the vitellogenin (vtg) gene expression and biochemical biomarkers; and gonad for the biochemical and histological biomarkers analyses.

Results: No alterations were observed in the hormone’s levels, sexual maturation level or in cyp19a1b and vtg gene expression. In the liver the non-protein thiols concentration increased at 2.5 µg.L-1 of PCM, and the superoxide dismutase (SOD) activity was reduced at 0.25 µg.L-1 of PCM. In gonads, glutathione S-transferase (GST) activity decreased and SOD activity increased at 25 µg.L-1 of PCM, while the glutathione peroxidase (GPx) activity reduced after exposure to both PCM concentrations.

Conclusion: The results showed that environmental concentrations of PCM can cause alterations in the antioxidant system, mainly in the gonads of R. quelen males. However, without significant change in the hormones levels or in the expression of genes related to the reproduction axis. These alterations occurred at concentrations already found in aquatic environment, including in Brazil.

Keywords

acetaminophen, endocrine disruptor, emerging contaminant, fish

Resumo

Objetivo: O paracetamol (PCM), ou acetaminofeno, é um dos medicamentos mais utilizados no tratamento humano da dor e da febre. Por ser frequentemente encontrado no ambiente aquático, o objetivo deste estudo foi investigar os efeitos do PCM no eixo reprodutivo de machos do bagre Rhamdia quelen.

Métodos: Diferentes biomarcadores foram avaliados no hipotálamo, fígado e gônadas, bem como a quantificação de hormônios sexuais. Os peixes foram expostos a três concentrações de PCM: 0,25, 2,5 e 25 µg.L-1 e ao grupo controle (solvente acetona 0,0003%) e após 14 dias foram anestesiados para coleta de sangue e biometria, e a eutanásia foi feita para coleta de tecidos. Do sangue foi obtido plasma para quantificação de 11- keto testosterona e 17β - estradiol. O hipotálamo foi coletado para a expressão do gene da aromatase cerebral (cyp19a1b); o fígado para a expressão do gene da vitelogenina (vtg) e biomarcadores bioquímicos; e gônadas para os biomarcadores bioquímicos e histológicos.

Resultados: Não foram observadas alterações nos níveis hormonais, no nível de maturação sexual ou na expressão dos genes cyp19a1b e vtg. No fígado, a concentração de tióis não protéicos aumentou em 2,5 µg.L-1 de PCM, e a atividade da superóxido dismutase (SOD) foi reduzida em 0,25 µg.L-1 de PCM. Nas gônadas, a atividade da glutationa S-transferase (GST) diminuiu e a atividade da SOD aumentou em 25 µg.L-1 de PCM, enquanto a atividade da glutationa peroxidase (GPx) diminuiu após a exposição a ambas as concentrações de PCM.

Conclusões: Esses resultados mostraram que concentrações ambientais de PCM podem causar alterações no sistema antioxidante, principalmente nas gônadas de machos de R. quelen, porém sem alterar significativamente os níveis hormonais ou a expressão de genes relacionados ao eixo reprodutivo. Essas alterações podem ocorrer em concentrações já encontradas em ambientes aquáticos, inclusive no Brasil.
 

Palavras-chave

acetaminofeno, desregulador endócrino, contaminante emergente, peixe

Referências

Aebi, H., 1984. Catalase in vitro. Methods Enzymol. 105, 121-126. PMid:6727660. http://dx.doi.org/10.1016/S0076-6879(84)05016-3.

Araújo, N.B., & Tejerina-Garro, F.L., 2007. Fish diversity and composition in Cerrado streams, Ribeirão Ouvidor basin, upper Paraná River basin, Goiás, Brazil. Rev. Bras. Zool. 24(4), 981-990. http://dx.doi.org/10.1590/S0101-81752007000400014.

Aus der Beek, T., Weber, F., Bergmann, A., Hickmann, S., Ebert, I., Hein, A., & Küster, A., 2016. Pharmaceuticals in the environment: global occurrences and perspectives. Environ. Toxicol. Chem. 35(4), 823-835. PMid:26666847. http://dx.doi.org/10.1002/etc.3339.

Barbosa, I., Pizarro, I., Freitas, R., & Nunes, B., 2020. Antioxidative and neurotoxicity effects of acute and chronic exposure of the estuarine polychaete Hediste diversicolor to paracetamol. Environ. Toxicol. Pharmacol. 77, 103377. PMid:32251999. http://dx.doi.org/10.1016/j.etap.2020.103377.

Baumann, L., Holbech, H., Schmidt-Posthaus, H., Moissl, A.P., Hennies, M., Tiedmann, J., Weltje, L., Segner, H., & Braunbeck, T., 2020. Does hepatotoxicity interfere with endocrine activity in zebrafish (Danio rerio)? Chemosphere 238, 124589. PMid:31437630. http://dx.doi.org/10.1016/j.chemosphere.2019.124589.

Bradford, M., 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72(1-2), 248-254. PMid:942051. http://dx.doi.org/10.1016/0003-2697(76)90527-3.

Burke, M.D., & Mayer, R.T., 1974. Ethoxyresorufin: direct fluorimetric assay of a microsomal O-dealkylation which is preferentially inducible by 3-methylcholanthrene. Drug Metab. Dispos. 2(6), 583-588. PMid:4155680.

Calado, S.L.M., Esterhuizen-Londt, M., Assis, H.C.S., & Pflugmacher, S., 2019. Phytoremediation: green technology for the removal of mixed contaminants of a water supply reservoir. Int. J. Phytoremediation 21(4), 372-379. PMid:30656959. http://dx.doi.org/10.1080/15226514.2018.1524843.

Carvalho, B.M., Faria, L., Miiller, N.O.R., Spach, H.L., & Vitule, J.R.S., 2022. Length-weight relationships of native and non-native fishes in a subtropical coastal river of the Atlantic Rain Forest. Acta Limnol. Bras. 34, e5. http://dx.doi.org/10.1590/s2179-975x2821.

Casatti, L., & Castro, R.M.C., 2006. Testing the ecomorphological hypothesis in a headwater riffles fish assemblage of the rio São Francisco, southeastern Brazil. Neotrop. Ichthyol. 4(2), 203-214. http://dx.doi.org/10.1590/S1679-62252006000200006.

Cohen, I.V., Cirulli, E.T., Mitchell, M.W., Jonsson, T.J., Yu, J., Shah, N., Spector, T.D., Guo, L., Venter, J.C., & Telenti, A., 2018. Acetaminophen (paracetamol) use modifies the sulfation of sex hormones. EBioMedicine 28, 316-323. PMid:29398597. http://dx.doi.org/10.1016/j.ebiom.2018.01.033.

Corrêa, F., Claudino, M.C., & Garcia, A.M., 2010. Guia fotográfico e aspectos da biologia dos principais peixes de água doce do Parque Nacional da Lagoa do Peixe, RS. R. Eletr. Cad. Ecol. Aquat. 5, 28-43.

Dang, Z., 2014. Fish biomarkers for regulatory identification of endocrine disrupting chemicals. Environ. Pollut. 185, 266-270. PMid:24316064. http://dx.doi.org/10.1016/j.envpol.2013.11.006.

Dang, Z., Li, K., Yin, H., Hakkert, B., & Vermeire, T., 2011. Endpoint sensitivity in fish endocrine disruption assays: regulatory implications. Toxicol. Lett. 202(1), 36-46. PMid:21295121. http://dx.doi.org/10.1016/j.toxlet.2011.01.016.

Delbes, G., Blázquez, M., Fernandino, J.I., Grigorova, P., Hales, B.F., Metcalfe, C., Navarro-Martín, L., Parent, L., Robaire, B., Rwigemera, A., van Der Kraak, G., Wade, M., & Marlatt, V., 2022. Effects of endocrine disrupting chemicals on gonad development: mechanistic insights from fish and mammals. Environ. Res. 204(Pt B), 112040. PMid:34509487. http://dx.doi.org/10.1016/j.envres.2021.112040.

Ebele, A.J., Abdallah, M.A., & Harrad, S., 2017. Pharmaceuticals and personal care products (PPCPs) in the freshwater aquatic environment. Emerg. Contam. 3(1), 1-16. http://dx.doi.org/10.1016/j.emcon.2016.12.004.

Fernandes, L.P.S., Mathias, F.T., Richardi, V.S., & Silva de Assis, H.C., 2021. Cloning, partial sequencing and 17β-estradiol modulation of hepatic vitellogenin gene of the Neotropical catfish Rhamdia quelen. J. Appl. Ichthyology 37(4), 545. http://dx.doi.org/10.1111/jai.14203.

Forner-Piquer, I., Beato, S., Piscitelli, F., Santangeli, S., Di Marzo, V., Habibi, H.R., Maradonna, F., & Carnevali, O., 2020. Effects of BPA on zebrafish gonads: focus on the endocannabinoid system. Environ. Pollut. 264, 114710. PMid:32417572. http://dx.doi.org/10.1016/j.envpol.2020.114710.

Galus, M., Kirischian, N., Higgins, S., Purdy, J., Chow, J., Rangaranjan, S., Li, H., Metcalfe, C., & Wilson, J.Y., 2013. Chronic, low concentration exposure to pharmaceuticals impacts multiple organ systems in zebrafish. Aquat. Toxicol. 132-133, 200-211. PMid:23375851. http://dx.doi.org/10.1016/j.aquatox.2012.12.021.

Gao, R., Yuan, Z., Zhao, Z., & Gao, X., 1998. Mechanism of pyrogallol autoxidation and determination of superoxide dismutase enzyme activity. Bioelectrochem. Bioenerg. 45(1), 41-45. http://dx.doi.org/10.1016/S0302-4598(98)00072-5.

Gomes, L.C., Golombieski, J.I., Gomes, A.R.C., & Baldisserotto, B., 2000. Biologia do jundiá Rhamdia quelen (Teleostei, Pimelodidae). Cienc. Rural 30(1), 179-185. http://dx.doi.org/10.1590/S0103-84782000000100029.

Guerini, S., Prado, G.P., & Passos, M.G., 2014. Hábito alimentar de Rhamdia quelen (Siluriformes: Pimelodidae) em um trecho do Rio Bonito no município de São Domingos, Santa Catarina. Uningá Rev. 18, 10-15.

Guiloski, I.C., Ribas, J.L.C., Piancini, L.D.S., Dagostim, A.C., Cirio, S.M., Fávaro, L.F., Boschen, S.L., Cestari, M.M., Cunha, C., & Assis, H.C.S., 2017. Paracetamol causes endocrine disruption and hepatotoxicity in male fish Rhamdia quelen after subchronic exposure. Environ. Toxicol. Pharmacol. 53, 111-120. PMid:28545014. http://dx.doi.org/10.1016/j.etap.2017.05.005.

Gutiérrez-Noya, V.M., Gómez-Oliván, L.M., Ramírez-Montero, M.C., Islas-Flores, H., Galar-Martínez, M., & García-Medina, S., 2021. Survival and malformations rates, oxidative status in early life stages of Cyprinus carpio due to exposure to environmentally realistic concentrations of paracetamol. Sci. Total Environ. 768, 144585. PMid:33454465. http://dx.doi.org/10.1016/j.scitotenv.2020.144585.

Hachfi, L., Couvray, S., Simide, R., Tarnowska, K., Pierre, S., Gaillard, S., Richard, S., Coupé, S., Grillasca, J., & Prévot-D’Alvise, N., 2012. Impact of Endocrine Disrupting Chemicals [EDCs] on Hypothalamic-Pituitary-Gonad-Liver [HPGL] axis in fish. World J. Fish Mar. Sci. 4, 14-30.

Hafeman, D.G., Sunde, R.A., & Hoekstra, W.C., 1974. Effect of dietary selenium on erythrocyte and liver glutathione peroxidase in the rat. J. Nutr. 104(5), 580-587. PMid:4823943. http://dx.doi.org/10.1093/jn/104.5.580.

Hamed, R.R., Saleh, N.S.M., Shokeer, A., Guneidy, R.A., & Abdel-Ghany, S.S., 2016. Glutathione and its related enzymes in the gonad of Nile Tilapia (Oreochromis niloticus). Fish Physiol. Biochem. 42(1), 353-364. PMid:26476660. http://dx.doi.org/10.1007/s10695-015-0143-9.

Jiang, Z.Y., Hunt, J.V., & Wolff, S.P., 1992. Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein. Anal. Biochem. 202(2), 384-389. PMid:1519766. http://dx.doi.org/10.1016/0003-2697(92)90122-N.

Juin, S.K., Sarkar, S., Maitra, S., & Nath, P., 2017. Effect of fish vitellogenin on the growth of juvenile catfish, Clarias gariepinus (Burchell,1822). Aquacult. Rep. 7, 16-26. http://dx.doi.org/10.1016/j.aqrep.2017.05.001.

Kar, S., Sangem, P., Anusha, N., & Senthilkumaran, B., 2021. Endocrine disruptors in teleosts: evaluating environmental risks and biomarkers. Aquac. Fish. 6(1), 1-26. http://dx.doi.org/10.1016/j.aaf.2020.07.013.

Keen, J.H., Habig, W.H., & Jakoby, W.B., 1976. Mechanism for the several activities of the glutathione S-transferases. J. Biol. Chem. 251(20), 6183-6188. PMid:977564. http://dx.doi.org/10.1016/S0021-9258(20)81842-0.

Kim, P., Park, Y., Ji, K., Seo, J., Lee, S., Choi, K., Kho, Y., Park, J., & Choi, K., 2012. Effect of chronic exposure to acetaminophen and lincomycin on Japanese medaka (Oryzias latipes) and freshwater cladocerans Daphnia magna and Moina macrocopa, and potential mechanisms of endocrine disruption. Chemosphere 89(1), 10-18. PMid:22560975. http://dx.doi.org/10.1016/j.chemosphere.2012.04.006.

Kyamer, R.D., Mizukawa, A., Ide, A.H., Marcante, L.O., Santos, M.M., & Azevedo, J.C.R., 2015. Determination of anti-inflammatory in water and sediment and its relations with water quality in Alto Iguaçu watershed, Curitiba-PR. R. Bras. Recur. Hidr. 20, 657-667.

Lin, W., Guo, H., Li, Y., Wang, L., Zhang, D., Hou, J., Wu, X., Li, L., Li, D., & Zhang, X., 2018. Single and combined exposure of microcystin-LR and nitrite results in reproductive endocrine disruption via hypothalamic-pituitary-gonadal-liver axis. Chemosphere 211, 1137-1146. PMid:30223329. http://dx.doi.org/10.1016/j.chemosphere.2018.08.049.

Liu, S., Ding, R., & Nie, X., 2019. Assessment of oxidative stress of paracetamol to Daphnia magna via determination of Nrf1 and genes related to antioxidant system. Aquat. Toxicol. 211, 73-80. PMid:30954018. http://dx.doi.org/10.1016/j.aquatox.2019.03.014.

Livak, K.J., & Schmittgen, T.D., 2001. Analysis of relative gene expression data using real time quantitative PCR and the 2-ΔΔCT method. Methods 25(4), 402-408. PMid:11846609. http://dx.doi.org/10.1006/meth.2001.1262.

Masteling, R.P., Castro, B.B., Antunes, S.C., & Nunes, B., 2016. Whole-organism and biomarker endpoints in Daphnia magna show uncoupling of oxidative stress and endocrine disruption in phenolic derivatives. Ecotoxicol. Environ. Saf. 134, 64-71. http://dx.doi.org/10.1016/j.ecoenv.2016.08.012.

Montanha, F. P., Nagashima, J. C., & Kirnew, M. D., 2011. The physiological characteristics and reproductive of Rhamdia quelen. R. Ci. Eletr. Med. Vet. 9(17), 1-8.

Mushirobira, Y., Kamegai, K., Amagai, T., Murata, R., Nagae, M., & Soyano, K., 2021. Expression profiles of hepatic vitellogenin and gonadal zona pellucida subtypes in gray mullet (Mugil cephalus) with 17α-ethinylestradiol-induced gonadal abnormality. Aquat. Toxicol. 237, 105863. PMid:34082271. http://dx.doi.org/10.1016/j.aquatox.2021.105863.

Negrelli, D.C., Vieira, D.H.M.D., Tagliavini, V.P., Abdallah, V.D., & Azevedo, R.K., 2019. Molecular and morphological analysis of Henneguya jundiai n. sp. (Cnidaria: Myxosporea), a new parasite of the gills of Rhamdia quelen in Brazil. Acta Trop. 197, 105053. PMid:31173737. http://dx.doi.org/10.1016/j.actatropica.2019.105053.

Nunes, B., Antunes, S.C., Santos, J., Martins, L., & Castro, B.B., 2014. Toxic potential of paracetamol to freshwater organisms: a headache to environmental regulators? Ecotoxicol. Environ. Saf. 107, 178-185. PMid:24949899. http://dx.doi.org/10.1016/j.ecoenv.2014.05.027.

Oksanen, J.F., Blanchet, G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., & Wagner, H., 2015. Vegan: Community Ecology Package. R Package, version 2.3-0. Vienna: R Foundation for Statistical Computing.

Okuyama, J., Galvão, T., & Silva, M., 2022. Estimates of paracetamol poisoning in Brazil: analysis of official records from 1990s to 2020. Front. Pharmacol. 13, 829547. PMid:35350767. http://dx.doi.org/10.3389/fphar.2022.829547.

Parolini, M., 2020. Toxicity of the Non-Steroidal Anti-Inflammatory Drugs (NSAIDs) acetylsalicylic acid, paracetamol, diclofenac, ibuprofen and naproxen towards freshwater invertebrates: a review. Sci. Total Environ. 740, 140043. PMid:32559537. http://dx.doi.org/10.1016/j.scitotenv.2020.140043.

Perussolo, M.C., Guiloski, I.C., Lirola, J.R., Fockink, D.H., Corso, C.R., Bozza, D.C., Prodocimo, V., Mela, M., Ramos, L.P., Cestari, M.M., Acco, A., & Assis, H.C.S., 2019. Integrated biomarker response index to assess toxic effects of environmentally relevant concentrations of paracetamol in a neotropical catfish (Rhamdia quelen). Ecotoxicol. Environ. Saf. 182, 109438. PMid:31310901. http://dx.doi.org/10.1016/j.ecoenv.2019.109438.

Phong Vo, H.N., Le, G.K., Hong Nguyen, T.M., Bui, X., Nguyen, K.H., Rene, E.R., Vo, T.D.H., Thanh Cao, N.D., & Mohan, R., 2019. Acetaminophen micropollutant: historical and current occurrences, toxicity, removal strategies and transformation pathways in different environments. Chemosphere 236, 124391. PMid:31545194. http://dx.doi.org/10.1016/j.chemosphere.2019.124391.

Pizzol, T.S.D., Tavares, N.U.L., Bertoldi, A.D., Farias, M.R., Arrais, P.S.D., Oliveira, M.A., Luiza, V.L., & Mengue, S.S., 2016. Use of medicines and other products for therapeutic purposes among children in Brazil. Rev. Saude Publica 50(Suppl. 2), 12s. http://dx.doi.org/10.1590/s1518-8787.2016050006115.

Ramachandran, A., & Jaeschke, H., 2019. Acetaminophen hepatotoxicity: a mitochondrial perspective. Adv. Pharmacol. 85, 195-219. PMid:31307587. http://dx.doi.org/10.1016/bs.apha.2019.01.007.

Ramos, A.S., Correia, A.T., Antunes, S.C., Gonçalves, F., & Nunes, B., 2014. Effect of acetaminophen exposure in Oncorhynchus mykiss gills and liver: detoxification mechanisms, oxidative defense system and peroxidative damage. Environ. Toxicol. Pharmacol. 37(3), 1221-1228. PMid:24816177. http://dx.doi.org/10.1016/j.etap.2014.04.005.

Rico, A., Oliveira, R., Nunes, G.S.S., Rizzi, C., Villa, S., López-Heras, I., Vighi, M., & Waichman, A.V., 2021. Pharmaceuticals and other urban contaminants threaten Amazonian freshwater ecosystems. Environ. Int. 155, 106702. PMid:34139589. http://dx.doi.org/10.1016/j.envint.2021.106702.

Saide, K., Sherwood, V., & Wheeler, G.N., 2019. Paracetamol-induced liver injury modelled in Xenopus laevis embryos. Toxicol. Lett. 302, 83-91. PMid:30282005. http://dx.doi.org/10.1016/j.toxlet.2018.09.016.

Santos, P.R.O., Costa, M.J., Santos, A.C.A., Silva-Zacarín, E.C.M., & Nunes, B., 2020. Neurotoxic and respiratory effects of human use drugs on a Neotropical fish species, Phalloceros harpagos. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 230, 108683. PMid:31874287. http://dx.doi.org/10.1016/j.cbpc.2019.108683.

Sedlak, J., & Lindsay, R.H., 1968. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal. Biochem. 25(1), 192-205. PMid:4973948. http://dx.doi.org/10.1016/0003-2697(68)90092-4.

Silva de Assis, H.C., Navarro-Martín, L., Fernandes, L.S.P., Cardoso, C.C., Pavoni, D.P., & Trudeau, V.L., 2018. Cloning, partial sequencing and expression analysis of the neural form of P450 aromatase (cyp19a1b) in the South America catfish Rhamdia quelen. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 221-222, 11-17. PMid:29655871. http://dx.doi.org/10.1016/j.cbpb.2018.04.001.

Starling, M.C.V.M., Amorim, C.C., & Leão, M.M.D., 2019. Occurrence, control and fate of contaminants of emerging concern in environmental compartments In Brazil. J. Hazard. Mater. 372, 17-36. PMid:29728279. http://dx.doi.org/10.1016/j.jhazmat.2018.04.043.

Szöcs, E., & Schäfer, R.B., 2015. Ecotoxicology is not normal: a comparison of statistical approaches for analysis of count and proportion data in ecotoxicology. Environ. Sci. Pollut. Res. Int. 22(18), 13990-13999. PMid:25953608. http://dx.doi.org/10.1007/s11356-015-4579-3.

Venancio, A.C.P., Aguiar, G.R., Lopes, P.S., & Alves, D.R., 2010. Metazoan parasites of Mandi-amarelo Pimelodus maculatus and of Jundiá Rhamdia quelen (Osteichthyes: Siluriformes) of Paraíba do Sul River, Volta Redonda, Rio de Janeiro. Rev. Bras. Parasitol. Vet. 19(3), 157-163. http://dx.doi.org/10.1590/S1984-29612010000300006.

Veras, T.B., Paiva, A.L.R., Duarte, M.M.M.B., Napoleão, D.C., & Cabral, J.J.S.P., 2019. Analysis of the presence of anti-inflammatories drugs in surface water: a case study in Beberibe river - PE, Brazil. Chemosphere 222, 961-969. http://dx.doi.org/10.1016/j.chemosphere.2019.01.167.

Vicentini, M., Fernandes, L.S.P., Marques, A.E.M.L., Osório, F.H.T., Baika, L.M., Risso, W.E., Martinez, C.B.R., Grassi, M.T., Fávaro, L.F., Mela, M., Cestari, M.M., & Silva de Assis, H.C., 2022. Effects of cadmium on the female reproductive axis of a Neotropical fish. Chemosphere 286(Pt 1), 131639. PMid:34346330. http://dx.doi.org/10.1016/j.chemosphere.2021.131639.

Wang, N., 2018. Increasing the reliability and reproducibility of aquatic ecotoxicology: learn lessons from aquaculture research. Ecotoxicol. Environ. Saf. 161, 785-794. PMid:29960649. http://dx.doi.org/10.1016/j.ecoenv.2018.06.044.

Wilkinson, J.L., Boxall, A.B.A., Kolpin, D.W., Leung, K.M.Y., Lai, R.W.S., Galbán-Malagón, C., Adell, A.D., Mondon, J., Metian, M., Marchant, R.A., Bouzas-Monroy, A., Cuni-Sanchez, A., Coors, A., Rojo, P.C.M., Gordon, C., Cara, M., Moermond, M., Luarte, T., Petrosyan, V., Perikhanyan, Y., Mahon, C.S., McGurk, C.J., Hofmann, T., Kormoker, T., Iniguez, V., Guzman-Otazo, J., Tavares, J.L., Figueiredo, F.G., Razzolini, M.T.P., Dougnon, V., Gbaguidi, G., Traoré, O., Blais, J.M., Kimpe, L.E., Wong, M., Wong, D., Ntchantcho, R., Pizarro, J., Ying, G., Chen, C., Páez, M., Martínez-Lara, J., Otamonga, J., Poté, J., Ifo, S.A., Wilson, P., Echeverría-Sáenz, S., Udikovic-Kolic, N., Milakovic, M., Fatta-Kassinos, D., Ioannou-Ttofa, L., Belušová, V., Vymazal, J., Cárdenas-Bustamante, M., Kassa, B.A., Garric, J., Chaumot, A., Gibba, P., Kunchulia, I., Seidensticker, S., Lyberatos, G., Halldórsson, H.P., Melling, M., Shashidhar, T., Lamba, M., Nastiti, A., Supriatin, A., Pourang, N., Abedini, A., Abdullah, O., Gharbia, S.S., Pilla, F., Chefetz, B., Topaz, T., Marcellin, K.Y., Aubakirova, B., Beisenova, R., Olaka, L., Mulu, J.K., Chatanga, P., Ntuli, V., Blama, N.T., Sherif, S., Aris, A.Z., Looi, L.J., Niang, M., Traore, S.T., Oldenkamp, R., Ogunbanwo, O., Ashfaq, M., Iqbal, M., Abdeen, Z., O’Dea, A., Morales-Saldaña, J.M., Custodio, M., Cruz, H., Navarrete, I., Carvalho, F., Gogra, A.B., Koroma, B.M., Cerkvenik-Flajs, V., Gombač, M., Thwala, M., Choi, K., Kang, H., Ladu, J.L.C., Rico, A., Amerasinghe, P., Sobek, A., Horlitz, G., Zenker, A.K., King, A.C., Jiang, J., Kariuki, R., Tumbo, M., Tezel, U., Onay, T.T., Lejju, J.B., Vystavna, Y., Vergeles, Y., Heinzen, H., Pérez-Parada, A., Sims, D.B., Figy, M., Good, D., & Teta, C., 2022. Pharmaceutical pollution of the world’s rivers. Proc. Natl. Acad. Sci. USA 119(8), e2113947119. PMid:35165193. http://dx.doi.org/10.1073/pnas.2113947119.
 

Submetido em:
13/04/2023

Aceito em:
14/09/2023

Publicado em:
30/10/2023

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