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Effect of ibuprofen exposure on blood, gill, liver, and brain on common carp (Cyprinus carpio) using oxidative stress biomarkers

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Abstract

Although trace concentrations of ibuprofen (IBP) have been detected in diverse water bodies, there is currently insufficient information on the potentially deleterious effects of this xenobiotic. The present study aimed to determine whether IBP induces oxidative stress in brain, liver, gill, and blood of the common carp Cyprinus carpio. To this end, the median lethal concentration at 96 h (96-h LC50) was determined and the lowest observed adverse effect level was established. Carp were exposed to the latter concentration (17.6 mg L−1) for 12, 24, 48, 72, and 96 h, and the following biomarkers were evaluated: lipid peroxidation (LPX) and activity of the antioxidant enzymes superoxide dismutase, catalase, and glutathione peroxidase. Results indicated that LPX and antioxidant enzymes’ activity increased significantly (p < 0.05) with respect to the control group in liver, gill, and blood, while no significant differences occurred in brain. In conclusion, IBP induced oxidative stress on C. carpio, the liver being the organ most affected by this damage.

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References

  • Abdollahi M, Mostafalou S, Pournourmohammadi S, Shadnia S (2004) Oxidative stress and cholinesterase inhibition in saliva and plasma of rats following sub-chronic exposure to malathion. Comp Biochem Physiol C Toxicol Pharmacol 137:29–34

    Article  Google Scholar 

  • Ahmad I, Hamid T, Fatima M, Chand HS, Jain SK, Athar M, Raisuddin S (2000) Induction of hepatic antioxidants in fresh-water catfish (Channa punctatus Bloch) is a biomarker of paper mill effluent exposure. Biochim Biophys Acta 1519:37–48

    Article  Google Scholar 

  • Andreozzi R, Raffaele M, Nicklas P (2003) Pharmaceuticals in STP effluents and their solar photodegradation in aquatic environment. Chemosphere 50:1319–1330

    Article  CAS  Google Scholar 

  • Antonić J, Heath E (2007) Determination of NSAIDs in river sediment samples. Anal Bioanal Chem 387:1337–1342

    Article  Google Scholar 

  • Asensio C, Levoin N, Guillaume C, Guerquin M, Rouguieg K, Chrétien F, Chapleur Y, Netter P, Minn A, Lapicque F (2007) Irreversible inhibition of glucose-6-phosphate dehydrogenase by the coenzyme A conjugate of ketoprofen: a key to oxidative stress induced by non-steroidal anti-inflammatory drugs? Biochem Pharmacol 73:405–416

    Article  CAS  Google Scholar 

  • Azzi A, Davies KJ, Kelly F (2004) Free radical biology—terminology and critical thinking. FEBS Lett 558(1):3–6

    Article  CAS  Google Scholar 

  • Bagnyukova TV, Chahrak OI, Lushchak VI (2006) Coordinated response of goldfish antioxidant defenses to environmental stress. Aquat Toxicol 78(4):325–331

    Article  CAS  Google Scholar 

  • Barata C, Varo I, Navarro JC, Arun S, Porte C (2005) Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds. Comp Biochem Physiol C Toxicol Pharmacol 140:175–186

    Article  Google Scholar 

  • Bendz D, Paxeus NA, Ginn TR, Loge FJ (2005) Occurrence and fate of pharmaceutically active compounds in the environment, a case study: Hoje River in Sweden. J Hazard Mater 122:195–204

    Article  CAS  Google Scholar 

  • Blanco G, Martínez C, García-Martín E, Agúndez JA (2005) Cytochrome P450 gene polymorphisms and variability in response to NSAIDs. Clin Res Regul Aff 22:57–81

    Article  Google Scholar 

  • Bound JP, Voulvoulis N (2005) Household disposal of pharmaceuticals as a pathway for aquatic contamination in the United Kingdom. Environ Health Perspect 113:1705–1711

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72(1):248–254

    Article  CAS  Google Scholar 

  • Brown JR, Paxéus N, Förlin L, Larsson DGJ (2007) Variations in bioconcentration of human pharmaceuticals from sewage effluents into fish blood plasma. Environ Toxicol Pharmacol 24:267–274

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Carey J (2002) Brain facts: A primer on the brain and nervous system. Society for Neuroscience, Washington DC

    Google Scholar 

  • Carlsson C, Johansson AK, Alvan G, Bergman K, Kuhler T (2006) Are pharmaceuticals potent environmental pollutants? Part I: environmental risk assessments of selected active pharmaceuticals ingredients. Sci Total Environ 364:67–87

    Article  CAS  Google Scholar 

  • Comisión Nacional del Agua (CNA) (1995) Feasibility study for the sanitation of the Valley of Mexico. Final report. December 1995, Mexico

  • Cordy GE, Duran NL, Bouwer H, Rice RC, Furlong ET, Zaugg SD, Meyer MT, Barber LB, Kolpin DW (2004) Do pharmaceuticals, pathogens, and other organic waste water compounds persist when waste water is used for recharge? Ground Water Monit Remediat 24:58–69

    Article  CAS  Google Scholar 

  • Davies NM (1998) Clinical pharmacokinetics of ibuprofen. The first 30 years. Clin Pharmacokinet 34:101–154

    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 140:109–119

    Article  CAS  Google Scholar 

  • Dröge W (2003) Free radicals in the physiological control of cell function. Physiol Rev 439:47–95

    Google Scholar 

  • Gómez MJ, Petrovic M, Férnandez-Alba AR, Barcelo D (2006) Determination of pharmaceuticals of various therapeutic classes by solid-phase extraction and liquid chromatography–tandem mass spectrometry analysis in hospital effluent wastewaters. J Chromatogr A 1114:224–233

    Article  Google Scholar 

  • Gomez C, Constantine L, Moen M, Vaz A, Huggett DB (2011) Ibuprofen metabolism in the liver and gill of rainbow trout, Oncorhynchus mykiss. Bull Environ Contam Toxicol 86:247–251

    Article  CAS  Google Scholar 

  • Gómez-Oliván LM, Neri-Cruz N, Galar-Martínez M, Vieyra-Reyes P, García-Medina S, Razo-Estrada C, Dublán-García O, Corral-Avitia AY (2012) Assessing the oxidative stress induced by paracetamol spiked in artificial sediment on Hyalella azteca. Water Air Soil Pollut 223:5097–5104

    Article  Google Scholar 

  • Gunzler W, Flohe-Clairborne A (1985) Glutathione peroxidase. In: Green-Wald RA (ed) Handbook of methods for oxygen radical research. CRC Press, Boca Raton, pp 285–290

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Halliwell B (2006) Oxidative stress and neurodegeneration: where are we now? J Neurochem 97:1634–1658

    Article  CAS  Google Scholar 

  • Han GH, Hur HG, Kim SD (2006) Ecotoxicological risk of pharmaceuticals from wastewater treatment plants in Korea: occurrence and toxicity to Daphnia magna. Environ Toxicol Chem 25:265–271

    Article  CAS  Google Scholar 

  • Hardman JG, Limbird LE, Goodman A (2003) The pharmacological basis of therapeutics, vol I, 10th edn. McGraw-Hill Interamericana, Mexico, p 1072 (in Spanish)

    Google Scholar 

  • Huang DJ, Zhang YM, Song G, Long J, Liu JH, Ji WH (2007) Contaminants-induced oxidative damage on the carp Cyprinus carpio collected from the Upper Yellow River, China. Environ Monit Assess 128:483–488

    Article  CAS  Google Scholar 

  • Islas-Flores H, Gómez-Oliván LM, Galar-Martínez M, Colín-Cruz A, Neri-Cruz N, García-Medina S (2013) Diclofenac-induced oxidative stress in brain, liver, gill and blood of common carp (Cyprinus carpio). Ecotoxicol Environ Saf 92:32–38

    Article  CAS  Google Scholar 

  • Jiménez BC, Landa H (1998) Physico-chemical and bacteriological characterization of wastewater from Mexico City. Water Sci Technol 37:1–8

    Article  Google Scholar 

  • Kasprzyk-Hordern B, Dinsdale RM, Guwy AJ (2008) The occurrence of pharmaceuticals, personal care products, endocrine disruptors and illicit drugs in surface water in South Wales UK. Water Res 42:3498–3518

    Article  CAS  Google Scholar 

  • Katzung B (2007) Basic and clinical pharmacology, 9th edn. Manual Moderno, Mexico, p 575 (in Spanish)

    Google Scholar 

  • Kreuzinger N, Clara M, Strenn B, Vogel B (2004) Investigation on the behavior of selected pharmaceuticals in the groundwater after infiltration of treated wastewater. Water Sci Technol 50:221–228

    CAS  Google Scholar 

  • la Farré M, Ferrer I, Ginebreda A, Figueras M, Olivella L, Tirapu L, Vilanova M, Barcelo D (2001) Determination of drugs in surface water and wastewater samples by liquid chromatography–mass spectrometry: methods and preliminary results including toxicity studies with Vibrio fischeri. J Chromatogr A 938:187–197

    Article  Google Scholar 

  • Lee HB, Peart TE, Svoboda ML (2005) Determination of endocrine-disrupting phenols, acidic pharmaceuticals, and personal care products in sewage by solid-phase extraction and gas chromatography–mass spectrometry. J Chromatogr A 1094:122–129

    Article  CAS  Google Scholar 

  • Livingstone DR, Forlin L, George S (1994) Molecular biomarkers and toxic consequences of impact by organic pollution in aquatic organisms. In: Sutcliffe DW (ed) Water quality and stress indicators in marine and freshwater systems: linking levels of organization. Freshwater Biological Association, Ambleside, pp 1171–1254

    Google Scholar 

  • Méndez-Arriaga F, Torres-Palma RA, Pétrier C, Esplugas S, Gimenez J, Pulgarin C (2008) Ultrasonic treatment of water contaminated with ibuprofen. Water Res 42:4243–4248

    Article  Google Scholar 

  • Metcalfe CD, Koenig BG, Bennie D, Servos M, Ternes TA, Hirsch R (2003) Occurrence of neutral and acidic drugs in the effluents of Canadian sewage treatment plants. Environ Toxicol Chem 22:2872–2880

    Article  CAS  Google Scholar 

  • Miranda MA, Morera I, Vargas F, Gómez-Lechón MJ, Castell JV (1991) In vitro assessment of the phototoxicity of anti-inflammatory 2-arylpropionic acids. Toxicol in Vitro 5:451–455

    Article  CAS  Google Scholar 

  • Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175

    CAS  Google Scholar 

  • Mohapatra DP, Brar SK, Tyagi RD, Picard P, Surampalli RY (2014) Analysis and advanced oxidation treatment of a persistent pharmaceutical compound in wastewater and wastewater sludge–carbamazepine. Sci Total Environ 470–471:58–75

    Article  Google Scholar 

  • Monteiro SM, Mancera JM, Fontáınhas-Fernandes A, Sausa M (2005) Copper induced alterations of biochemical parameters in the gill and plasma of Oreochromis niloticus. Comp Biochem Physiol C Toxicol Pharmacol 141:375–383

    Article  Google Scholar 

  • Morrow JD, Roberts LJ (2001) Lipid-derived autacoids: Eicosanoids and platelet-activating factor. In: Hardman JG, Limbird LE (eds) Goodman and Gilman’s “The pharmacological basis of therapeutics”. McGraw-Hill, New York, pp 669–686

    Google Scholar 

  • Oviedo-Gómez DGC, Galar-Martínez M, García-Medina S, Razo-Estrada C, Gómez-Oliván LM (2010) Diclofenac-enriched artificial sediment induces oxidative stress in Hyalella azteca. Environ Toxicol Pharmacol 29:39–43

    Article  Google Scholar 

  • Parolini M, Binelli A, Cogni D, Riva C, Provini A (2009) An in vitro biomarker approach for the evaluation of the ecotoxicity of non-steroidal anti-inflammatory drugs (NSAIDs). Toxicol in Vitro 23:935–942

    Article  CAS  Google Scholar 

  • Pomati F, Castiglioni S, Zuccato E, Fanelli R, Vigetti D, Calamari D (2006) Effects of a complex mixture of therapeutic drugs at environmental levels on human embryonic cells. Environ Sci Technol 40:2442–2447

    Article  CAS  Google Scholar 

  • Pounds N, Maclean S, Webley M, Pascoe D, Hutchinson T (2008) Acute and chronic effects of ibuprofen in the mollusc Planorbis carinatus (Gastropoda: Planorbidae). Ecotoxicol Environ Saf 70:47–52

    Article  CAS  Google Scholar 

  • Quinn B, Gagné F, Blaise C (2008) An investigation into the acute and chronic toxicity of eleven pharmaceuticals (and their solvents) found in wastewater effluent on the cnidarian, Hydra attenuata. Sci Total Environ 389:306–314

    Article  CAS  Google Scholar 

  • Radi R, Turrens JF, Chang LY, Bush KM, Carpo JD, Freeman BA (1991) Detection of catalase in rat heart mitochondria. J Biol Chem 26(32):22028–22034

    Google Scholar 

  • Richards S, Cole S (2006) A toxicity and hazard assessment of fourteen pharmaceuticals to Xenopus laevis larvae. Ecotoxicology 15:647–656

    Article  CAS  Google Scholar 

  • Roberts PH, Thomas KV (2006) The occurrence of selected pharmaceuticals in wastewater effluent and surface waters of the lower Tyne catchment. Sci Total Environ 356:143–153

    Article  CAS  Google Scholar 

  • Salgueiro-Pagadigorria C, Kelmer-Bracht A, Bracht A, Ishii-Iwamoto E (2004) Naproxen affects Ca2+ fluxes in mitochondria, microsomes and plasma membrane vesicles. Chem Biol Interact 147:49–63

    Article  CAS  Google Scholar 

  • Santos JL, Aparicio I, Alonso E, Callejon M (2005) Simultaneous determination of pharmaceutically active compounds in wastewater samples by solid phase extraction and high-performance liquid chromatography with diode array and fluorescence detectors. Anal Chim Acta 550:116–122

    Article  CAS  Google Scholar 

  • Santos LHMLM, Araujo AN, Fachini A, Pena A, Deleure-Matos C, Montenegro MCBSM (2010) Ecotoxicological aspects related to the presence of pharmaceuticals in the aquatic environment. J Hazard Mater 175:45–95

    Article  CAS  Google Scholar 

  • Sanyal AK, Roy D, Chowdhury B, Banerjee AB (1993) Ibuprofen, a unique anti-inflammatory compound with antifungal activity against dermatophytes. Lett Appl Microbiol 17:109–111

    Article  CAS  Google Scholar 

  • Saravanan M, Prabhu Kumar K, Ramesh M (2011) Haematological and biochemical responses of freshwater teleost fish Cyprinus carpio (Actinopterygii: Cypriniformes) during acute and chronic sublethal exposure to lindane. Pestic Biochem Physiol 100:206–211

    Article  CAS  Google Scholar 

  • Scheytt T, Mersmann P, Lindstädt R, Heberer T (2005) Determination of sorption coefficients of pharmaceutically active substances carbamazepine, diclofenac, and ibuprofen, in sandy sediments. Chemosphere 60:245–253

    Article  CAS  Google Scholar 

  • Siemens J, Huschek G, Siebe C, Kaupenjohann M (2008) Concentrations and mobility of human pharmaceuticals in the world’s largest wastewater irrigation system, Mexico City–Mezquital Valley. Water Res 42:2124–2134

    Article  CAS  Google Scholar 

  • Spencer JP, Jenner P, Daniel SE, Lees AJ, Marsden DC, Halliwell B (1998) Conjugates of catecholamines with cysteine and GSH in Parkinson’s disease: possible mechanisms of formation involving reactive oxygen species. J Neurochem 71:2112–2122

    Article  CAS  Google Scholar 

  • Stegeman JJ, Livingstone DR (1998) Forms and functions of cytochrome P450. Comp Biochem Physiol C: Pharmacol Toxicol Endocrinol 121:1–3

    CAS  Google Scholar 

  • Stephensen E, Svavarsson J, Sturve J, Ericson G, Adolfsson-Ena M, Forlin L (2000) Biochemical indicators of pollution exposure in shorthorn sculpin (Myoxocephalus scorpius), caught in four harbours on the southwest of Iceland. Aquat Toxicol 48:431–442

    Article  CAS  Google Scholar 

  • Takagi T, Ramachandran C, Bermejo M, Yamashita S, Yu LX, Amidon GL (2006) A provisional biopharmaceutical classification of the top 200 oral drug products in the United States, Great Britain, Spain and Japan. Mol Pharmacol 3:631–643

    Article  CAS  Google Scholar 

  • Ternes T, Joss A, Siegrist H (2004) Scrutinizing pharmaceuticals and personal care products in wastewater treatment. Environ Toxicol Chem 38:393–398

    Google Scholar 

  • Tixier C, Singer HP, Oellers S, Müller SR (2003) Occurrence and fate of carbamazepine, clofibric acid, diclofenac, ibuprofen, ketoprofen, and naproxen in surface waters. Environ Sci Technol 37(6):1061–1068

    Article  CAS  Google Scholar 

  • US EPA (2009) Estimation Programs Interface Suite™ for Microsoft Windows, v 4.00. United States Environmental Protection Agency, Washington DC

    Google Scholar 

  • Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf 64:178–189

    Article  CAS  Google Scholar 

  • Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

    Article  Google Scholar 

  • Verenitch SS, Lowe CJ, Mazumder A (2006) Determination of acidic drugs and caffeine in municipal wastewaters and receiving waters by gas chromotagraphy–ion trap tandem mass spectrometry. J Chromatogr A 1116:193–203

    Article  CAS  Google Scholar 

  • Verstraeten IM, Fetterman GS, Meyer MT, Bullen T, Sebree SK (2005) Use of tracers and isotopes to evaluate vulnerability of water in domestic wells to septic waste. Ground Water Monit Remediat 25:107–117

    Article  CAS  Google Scholar 

  • Vieno NM, Tuhkanen T, Kronberg L (2005) Seasonal variation in the occurrence of pharmaceuticals in effluents from a sewage treatment plant and in the recipient water. Environ Sci Technol 39:8220–8226

    Article  CAS  Google Scholar 

  • von Bruchhausen F, Dannhardt G, Ebel S, Frahm AW, Hackenthal E, Holzgrabe U (1994) In: Hagers Handbuch der Pharmazeutishchen Praxis, 5th edn, vol 9. Springer, Berlin, Heidelberg, New York

  • Yamanaka H, Sogabe A, Handoh IC, Kawabata Z (2011) The effectiveness of clove oil as an anaesthetic on adult common carp, Cyprinus carpio L. J Anim Vet Adv 10:210–213

    Article  Google Scholar 

  • Zanger UM, Turpeinen M, Klein K, Schwab M (2008) Functional pharmacogenetics/genomics of human cytochromes P450 involved in drug biotransformation. Anal Bioanal Chem 392:1093–1108

    Article  CAS  Google Scholar 

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Acknowledgments

This study was made possible through support from the Consejo Nacional de Ciencia y Tecnología (CONACyT-Mexico, project 151665) and the Secretaria de Investigación y Estudios Avanzados de la UAEM (SIEA-UAEM, project UAEM 3415/2013CHT).

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Correspondence to Leobardo Manuel Gómez-Oliván.

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Islas-Flores, H., Gómez-Oliván, L.M., Galar-Martínez, M. et al. Effect of ibuprofen exposure on blood, gill, liver, and brain on common carp (Cyprinus carpio) using oxidative stress biomarkers. Environ Sci Pollut Res 21, 5157–5166 (2014). https://doi.org/10.1007/s11356-013-2477-0

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