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Ecotoxicological effects of salicylic acid in the freshwater fish Salmo trutta fario: antioxidant mechanisms and histological alterations

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Abstract

The presence of pharmaceutical drugs in aquatic ecosystems has been widely reported during the past years. Salicylic acid (SA) is mainly used in human medicine as an analgesic and antipyretic drug, being also active in preventing platelet aggregation. To study the ecotoxicological effects potentially elicited by SA in freshwater fish, brown trout individuals (Salmo trutta fario) were chronically exposed (28 days) to this drug, in order to evaluate the enzymatic and histological effects, in both gills and liver. A qualitative and semi-qualitative evaluation of the gills and liver was performed, and also a quantitative evaluation of various lamellar structures. Oxidative stress was quantified trough the determination of glutathione S-transferases (GSTs), glutathione reductase (GRed), total and selenium-dependent glutathione peroxidase (GPx) and Catalase (Cat) activities. Lipid peroxidative damage was also assessed by the quantification of thiobarbituric acid reactive substances (TBARS) in the liver. The here-obtained data showed the occurrence of oxidative stress, reflected by an increased activity of GPx and GRed in the liver; additionally, it was possible to observe non-specific histological changes in gills. The global significance of the entire set of results is discussed, giving emphasis to the ecological relevance of the responses.

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References

  • Aebi H (1984) Catalase in vitro. Method Enzymol 6:105–121

    Google Scholar 

  • Alazemi BM, Lewis JW, Andrews EB (1996) Gill damage in the fresh water fish Gnathonemus petersii (Family: Mormyridae) exposed to selected pollutants: an ultrastructural study. Environ Technol 17(3):225–238

    Article  CAS  Google Scholar 

  • Antunes A, Ferrand N, Alexandrino P (2000) A highly polymorphic plasma protein locus in brown trout (Salmo trutta L.) populations from Portugal. Biochem Genet 38(7–8):217–226

    Article  CAS  Google Scholar 

  • Antunes SC, Marques SM, Pereira R, Gonçalves F, Nunes B (2010) Testing procedures for the determination of several biomarkers in different species, for environmental assessment of pollution. J Environ Monitor 12(8):1625–1630

    Article  CAS  Google Scholar 

  • Arnott JA, Planey SL (2012) The influence of lipophilicity in drug discovery and design. Expert Opin Drug Discov 7(10):863–875

    Article  CAS  Google Scholar 

  • Arthur JR (2000) The glutathione peroxidases. Cell Mol Life Sci 57(13–14):1825–1835

    CAS  Google Scholar 

  • Authman MMN, Ibrahim SA, El-Kasheif MA, Gaber HS (2013) Heavy metals Ppollution and their effects on gills and liver of the Nile catfish inhabiting El-Rahawy Drain, Egypt. Global Vet 10(2):103–115

    CAS  Google Scholar 

  • Barnes KK, Kolpin DW, Furlong ET, Zaugg SD, Meyer MT, Barber LB (2008) A national reconnaissance of pharmaceuticals and other organic wastewater contaminants in the United States—I) Groundwater. Sci Total Environ 402(2–3):192–200

    Article  CAS  Google Scholar 

  • Benotti MJ, Trenholm RA, Vanderford BJ, Holady JC, Stanford BD, Snyder SA (2009) Pharmaceuticals and endocrine disrupting compounds in U.S. drinking water. Environ Sci Technol 43(3):597–603

    Article  CAS  Google Scholar 

  • Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34

    Article  Google Scholar 

  • Besse J-P, Garric J (2008) Human pharmaceuticals in surface waters Implementation of a prioritization methodology and application to the French situation. Toxicol Lett 176:104–123

    Article  CAS  Google Scholar 

  • 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 72:248–254

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Method Enzymol 52:302–310

    Article  CAS  Google Scholar 

  • Carlberg I, Mannervik B (1985) Glutathione reductase. Method Enzymol 113:484–490

    Article  CAS  Google Scholar 

  • Carrola J, Fontaínhas-Fernandes A, Matos P, Rocha E (2009) Liver histopathology in brown trout (Salmo trutta f. fario) from the Tinhela river, subjected to mine drainage from the abandoned Jales mine (Portugal). B Environ Contam Toxicol 83(1):35–41

    Article  CAS  Google Scholar 

  • Cleuvers M (2003) Aquatic ecotoxicity of pharmaceuticals including the assessment of combination effects. Toxicol Lett 142(3):185–194

    Article  CAS  Google Scholar 

  • Contardo-Jara V, Lorenza C, Pflugmacher S, Nützmann G, Kloas W, Wiegand C (2011) Exposure to human pharmaceuticals Carbamazepine, Ibuprofen and Bezafibrate causes molecular effects in Dreissena polymorpha. Aquat Toxicol 105(3–4):428–437

    Article  CAS  Google Scholar 

  • Daughton CG, Ternes TA (1999) Pharmaceuticals and personal care products in the environment: agents of subtle changes? Environ Health Perspect 107(6):907–938

    Article  CAS  Google Scholar 

  • Davison C (1971) Salicylate metabolism in man. Ann NY Acad Sci 179:249–268

    Article  CAS  Google Scholar 

  • Doi H, Horie T (2010) Salicylic acid-induced hepatotoxicity triggered by oxidative stress. Chem-Biol Interact 183(3):363–368

    Article  CAS  Google Scholar 

  • Doi H, Iwasaki H, Masubuchi Y, Nishigaki R, Horie T (2002) Chemiluminescence associated with the oxidative metabolism of salicylic acid in rat liver microsomes. Chem-Biol Interact 140(2):109–119

    Article  CAS  Google Scholar 

  • El-Bassat RA, Touliabah HE, Harisa GI (2012) Toxicity of four pharmaceuticals from different classes to isolated plankton species. Afr J Aquat Sci 37(1):71–80

    Article  CAS  Google Scholar 

  • Fent K, Weston AA, Caminada D (2006) Ecotoxicology of human pharmaceuticals. Aquat Toxicol 76(2):122–159

    Article  CAS  Google Scholar 

  • Fernandes MN, Mazon AF (2003) Environmental pollution and fish gill morphology. In: Val AL, Kapoor BG (eds) Fish adaptations. Science Publishers, Enfield, pp 203–231

    Google Scholar 

  • Fischer-Scherl T, Hoffman RW (1988) Gill morphology of native brown trout Salmo trutta m. fario experiencing acute and chronic acidification of a brook in Bavaria, FRG. Dis Aquatic Organ 4:43–51

    Article  Google Scholar 

  • Flohé L, Günzler WA (1984) Assays of glutathione peroxidase. Method Enzymol 105:114–121

    Article  Google Scholar 

  • Focazio MJ, Kolpin DW, Barnes KK, Furlong ET, Meyer MT, Zaugg SD, Barber LB, Thurman ME (2008) A national reconnaissance for pharmaceutical sand other organic wastewater contaminants in the United States—II. Untreated drinking water sources. Sci Total Environ 402(2–3):201–216

    Article  CAS  Google Scholar 

  • Gagné F, Blaise C, André C (2006) Occurrence of pharmaceutical products in a municipal effluent and toxicity to rainbow trout (Oncorhynchus mykiss) hepatocytes. Ecotoxicol Environ Safe 64:329–336

    Article  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione-S-transferases—the first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139

    CAS  Google Scholar 

  • Halling-Sorensen B, Nors Nielsen S, Lanzky PF, Ingerslev F, Holten Lutzhoft HC, Jorgensen SE (1998) Occurrence, fate and effects of pharmaceutical substances in the environment—a review. Chemosphere 36(2):357–393

    Article  CAS  Google Scholar 

  • Hawkins WE, Overstreet RM, Provancha MJ (1984) Effects of space shuttle exhaust plumes on gills of some estuarine fishes: a light and electron microscopic study. Harold W. Manter Lab Parasitol 7:297–309

    Google Scholar 

  • Hinton DE, Segner H, Au DWT, Kullman SW, Hardman RC (2008) Liver toxicity (Chapter VII). In: DiGiulio RT, Hinton DE (eds) The toxicology of fishes. CRC Press, Boca Raton, Florida, USA

  • Hughes CM (1984) General anatomy of the gills. In: Hoar RDJ, Marshal WS (eds) Fish physiology. Academic Press, New York, pp 1–72

    Google Scholar 

  • Hughes GM, Perry SF (1976) Morphometric study of trout gills: a light-microscope method suitable for the evaluation of pollutant action. J Exp Biol 64:447–460

    Google Scholar 

  • Huschek G, Hansen PD, Maurer HH, Krengel D, Kayser A (2004) Environmental risk assessment of medicinal products for human use according to European Commission recommendations. Environ Toxicol 19(3):226–240

    Article  CAS  Google Scholar 

  • Imayama S, Ueda S, Isoda M (2000) Histologic changes in the skin of hairless mice following peeling with salicylic acid. Arch Dermatol 136(11):1390–1395

    Article  CAS  Google Scholar 

  • Isidori M, Lavorgna M, Nardelli A, Parrella A, Previtera L, Rubino M (2005) Ecotoxicity of naproxen and its phototransformation products. Sci Total Environ 348(1–3):93–101

    Article  CAS  Google Scholar 

  • Jagoe CH, Haines TA (1983) Alterations in gill epithelial morphology of yearling Sunapee trout exposed to acute acid stress. Trans Am Fish Soc 112:689–695

    Article  CAS  Google Scholar 

  • Johnson AC, Williams RJ, Matthiessen P (2006) The potential steroid hormone contribution of farm animals to freshwaters, the United Kingdom as a case study. Sci Total Environ 362(1–3):166–178

    Article  CAS  Google Scholar 

  • Kim Y, Choi K, Jung J, Park S, Kim P, Park GJ (2007) Aquatic toxicity of acetaminophen, carbamazepine, cimetidine, diltiazem and six major sulfonamides, and their potential ecological risks in Korea. Environ Int 33(3):275–370

    Article  Google Scholar 

  • Larsson DGJ, Pedro C, Paxeus N (2007) Effluent from drug manufactures contains extremely high levels of pharmaceuticals. J Hazard Mater 148(3):751–755

    Article  CAS  Google Scholar 

  • Lin AY-C, Tsai Y-T (2009) Occurrence of pharmaceuticals in Taiwan’s surface waters: impact of waste streams from hospitals and pharmaceutical production facilities. Sci Total Environ 407(12):3793–3802

    Article  CAS  Google Scholar 

  • Mallatt J (1985) Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can J Fish Aquat Sci 42(4):630–648

    Article  CAS  Google Scholar 

  • Meland S, Farmen E, Heier LS, Rosseland BO, Salbu B, Song Y, Tollefsen KE (2011) Hepatic gene expression profile in brown trout (Salmo trutta) exposed to traffic related contaminants. Science Total Environ 409(8):1430–1443

    Article  CAS  Google Scholar 

  • Moldovan Z (2006) Occurrences of pharmaceutical and personal care products as micropollutants in rivers from Romania. Chemosphere 64(11):1808–1817

    Article  CAS  Google Scholar 

  • Moon TW, Walsh PJ, Mommsen TP (1985) Fish hepatocytes: a model metabolic system. Can J Fish Aquat Sci 42(11):1772–1782

    Article  CAS  Google Scholar 

  • Nero V, Farwell A, Lee LEJ, Van Meer T, MacKinnon MD, Dixon DG (2006) The effects of salinity on naphthenic acid toxicity to yellow perch: Gill and liver histopathology. Ecotoxicol Environ Safe 65(2):252–264

    Article  CAS  Google Scholar 

  • Norambuena F, Mackenzie S, Bell JG, Callol A, Estévez A, Duncan N (2012) Prostaglandin (F and E, 2- and 3-series) production and cyclooxygenase (COX-2) gene expression of wild and cultured broodstock of Senegalese sole (Solea senegalensis). Gen Comp Endocrinol 177(2):256–262

    Article  CAS  Google Scholar 

  • OECD (1992) OECD Guideline for testing of chemicals: Fish, Short-term Toxicity Test on Embryo and Sac-fry Stages

  • Osman A, Reheem A, AbuelFadl K, Rab A (2010) Enzymatic and histopathologic biomarkers as indicators of aquatic pollution in fishes. Nat Sci 2:1302–1311

    CAS  Google Scholar 

  • Pamplona JH, Oba ET, da Silva TA, Ramos LP, Ramsdorf WA, Cestari MM, Oliveira Ribeiro CA, Zampronio AR, Silva de Assis HC (2011) Subchronic effects of dipyrone on the fish species Rhamdia quelen. Ecotoxicol Environ Safe 74(3):342–349

    Article  CAS  Google Scholar 

  • Poleksic V, Mitrovic-Tutundzic V (1994) Fish gills as a monitor of sublethal and chronic effects of pollution. In: Müller R, Lloyd R (eds) Sublethal and chronic effects of pollutants on freshwater fish. Fishing News Books, Oxford

    Google Scholar 

  • Pomati F, Netting AG, Calamari D, Neilan BA (2004) Effects of erythromycin, tetraycline and ibuprofen on the growth of Synechocystis sp. and Lemna minor. Aquat Toxicol 67(4):387–396

    Article  CAS  Google Scholar 

  • Quinn B, Schmidt W, O’Rourke K, Hernan R (2011) Effects of the pharmaceuticals gemfibrozil and diclofenac on biomarker expression in the zebra mussel (Dreissena polymorpha) and their comparison with standardised toxicity tests. Chemosphere 84:657–663

    Article  CAS  Google Scholar 

  • Rendon MI, Berson DS, Cohen JL, Roberts WE, Starker I, Wang B (2010) Evidence and considerations in the application of chemical peels in skin disorders and aesthetic resurfacing. J Clin Aesthet Dermatol 3(7):32–43

    Google Scholar 

  • Rocha E, Monteiro RAF, Pereira CA (1995) Microanatomical organization of the hepatic stroma of the brown trout, Salmo trutta fario (Teleostei, Salmonidae): a qualitative and quantitative approach. J Morphol 223:1–11

    Article  Google Scholar 

  • Rosety-Rodríguez M, Ordoñez FJ, Rosety M, Rosety JM, Ribelles A, Carrasco C (2002) Morpho-histochemical changes in the gills of turbot, Scophthalmus maximus L., induced by sodium dodecyl sulfate. Ecotoxicol Environ Safe 51 (3): 223–228

  • Sacher F, Lange FT, Brauch H-J, Blankenhorn I (2001) Pharmaceuticals in groundwaters. Analytical methods and results of a monitoring program in Baden-Württemberg, Germany. J Chromatogr A 938(1–2):199–210

    Article  CAS  Google Scholar 

  • SanJuan-Reyes N, Gómez-Oliván LM, Galar-Martínez M, Vieyra-Reyes P, García-Medina S, Islas-Flores H, Neri-Cruz N (2013) Effluent from an NSAID-manufacturing plant in Mexico induces oxidative stress on Cyprinus carpio. Water Air Soil Pollut 224:1689

    Article  Google Scholar 

  • Sayed H-A. H.M (2013) Some Morphological Studies on the Respiratory System of Tilapia nilotica (Oreochromus niloticus) and African catfish (Clarias gariepinus). Thesis

  • Schmidt W, O’Rourke K, Hernan R, Quinn B (2011) Effects of the pharmaceuticals gemfibrozil and diclofenac on the marine mussel (Mytilus spp.) and their comparison with standardized toxicity tests. Mar Pollut Bull 62(7):1389–1395

    Article  CAS  Google Scholar 

  • Schomburg D, Salzmann M (1991) Enzyme handbook. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Schwaiger J, Ferling H, Mallow U, Wintermayr H, Negele RD (2004) Toxic effects of the non-steroidal anti-inflammatory drug diclofenac: Part I. Histopathological alterations and bioaccumulation in rainbow trout. Aquat Toxicol 68:141–150

    Article  CAS  Google Scholar 

  • Stackelberg PE, Furlong ET, Meyer MT, Zaugg SD, Henderson AK, Reissman DB (2004) Persistence of pharmaceutical compounds and other organic wastewater contaminants in a conventional drinking-water-treatment plant. Sci Total Environ 329(1–3):99–113

    Article  CAS  Google Scholar 

  • Stevens ED (1992) Gill morphometry of the red drum, Sciaenops ocellatus. Fish Physiol Biochem 10(2):169–176

    Article  Google Scholar 

  • Temmink JHM, Bouwmeister PJ, de Jong P, van den Berg JHJ (1983) An ultrastructural study of chromate induced hyperplasia in the gills of rainbow trout (Salmo gairdneri). Aquat Toxicol 4:165–179

    Article  CAS  Google Scholar 

  • Tietge J, Johnson R, Bergman H (1988) Morphometric changes in gill secondary lamellae of brook trout (Salvelinus fontinalis) after long-term exposure to acid and aluminum. Can J Aquat Sci 45:1643–1648

    Article  CAS  Google Scholar 

  • Triebskorn R, Casper H, Heyd A, Eikemper R, Köhler H-R, Schwaiger J (2004) Toxic effects of the non-steroidal anti-inflammatory drug diclofenac: Part II. Cytological effects in liver, kidney, gills and intestine of rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 68(2):151–166

    Article  CAS  Google Scholar 

  • Ugurlucan M, Cagçar MI, Turhan FN, Ziyade S, Karatepe Yildiz Y, Zencirci E, Ugurlucan FG, Arslan HA, Korkmaz S, Filizcan U, Cicek S (2012) Aspirin: from a historical perspective. Rec Pat Cardiovasc Drug Disc 7:71–76

    Article  CAS  Google Scholar 

  • van Anholt RD, Spanings T, Koven W, Wendelaar BSE (2003) Effects of acetylsalicylic acid treatment on thyroid hormones, prolactins, and the stress response of tilapia (Oreochromis mossambicus). Am J Physiol Regul Integr Comp Physiol 285(5):R1098–106

    Google Scholar 

  • Vane JR, Botting RM (1998) Mechanism of action of antiinflammatory drugs. Int J Tissue React 20(1):3–15

    CAS  Google Scholar 

  • Velisek J, Svobodova Z, Piackova V (2009) Effects of acute exposure to bifenthrin on some haematological, biochemical and histopathological parameters of rainbow trout (Oncorhynchus mykiss). Vet Med-Czech 54(3):131–137

    CAS  Google Scholar 

  • Warner TD, Mitchell JA (2002) Cyclooxygenase-3 (COX-3): filling in the gaps toward COX continuum? Proc Natl Acad Sci J 99(21):13371–13373

    Article  CAS  Google Scholar 

  • Weigel S, Kuhlmann J, Hühnerfuss H (2002) Drugs and personal care products as ubiquitous pollutants: occurrence and distribution of clofibric acid, caffeine and DEET in the North Sea. Sci Total Environ 295(1–3):131–141

    Article  CAS  Google Scholar 

  • Weiss S, Antunes A, Schlötterer C, Alexandrino P (2000) Mitochondrial haplotype diversity among Portuguese brown trout Salmo trutta L. populations: relevance to the post-Pleistocene recolonization of northern Europe. Mol Ecol 9(6):691–698

    Article  CAS  Google Scholar 

  • Wilson JM, Bunte RM, Anthony J, Carty AJ (2009) Evaluation of rapid cooling and tricaine methanesulfonate (MS222) as methods of euthanasia in zebrafish (Danio rerio). J Am Assoc Lab An Sci 48(6):785–789

    CAS  Google Scholar 

  • Winston GW, Di Giulio RT (1991) Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat Toxicol 19(2):137–161

    Article  CAS  Google Scholar 

  • Yasser AG, Naser MD (2011) Impact of pollutants on fish collected from different parts of Shatt Al-Arab River: a histopathological study. Environ Monitor Assess 181(1–4):175–182

    Article  Google Scholar 

  • Zou J, Neumann NF, Holland JW, Belosevic M, Cunningham C, Secombes CJ, Rowley AF (1999) Fish macrophages express a cyclo-oxygenase-2 homologue after activation. Biochem J 340:153–159

    Article  CAS  Google Scholar 

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Acknowledgements

This research was supported by the European Regional Development Fund (ERDF) through the COMPETE — Operational Competitiveness Program and by national funds through FCT – Foundation for Science and Technology, under the projects PEst-C/MAR/LA0015/2013 and PTDC/AMB/70431/2006.

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Nunes, B., Campos, J.C., Gomes, R. et al. Ecotoxicological effects of salicylic acid in the freshwater fish Salmo trutta fario: antioxidant mechanisms and histological alterations. Environ Sci Pollut Res 22, 667–678 (2015). https://doi.org/10.1007/s11356-014-3337-2

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