Skip to main content
Log in

Drugs of environmental concern modify Solea senegalensis physiology and biochemistry in a temperature-dependent manner

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The alerted presence in recent decades of pharmaceuticals has become an issue of environmental concern, and most of the mechanisms of biotransformation and biochemical and physiological responses to them in fish are still unknown, as well as the influence of water temperature in their ability to cope with them. This study aims to detect the main effects of two of the most widespread drugs on a set of physiological and biochemical markers in Solea senegalensis. Sole juveniles acclimatized at 15 and 20 °C were administered an intraperitoneal injection of the non-steroidal anti-inflammatory drug ibuprofen (IB; 10 mg/kg) and the anti-convulsant drug carbamazepine (CBZ; 1 mg/kg). Two days after the injection, liver, muscle and plasma were sampled. Liver enzymatic activities of 15 °C acclimated fish were more responsive to pharmaceuticals than those acclimated at 20 °C, especially for CYP450-related activities (7-ethoxyresorufin (EROD), 7-methoxyresorufin (MROD), 3-cyano-7-ethoxycoumarin (CECOD) and 7-benzyloxy-4-[trifluoromethyl]-coumarin-O-debenzyloxylase (BFCOD)) and uridine diphosphate glucuronosyltransferase (UDPGT). Cytosolic anti-oxidant enzyme activities and glutathione S-transferase (GST) did not show a clear effect of temperature. Glucose and transferase activities in plasma were not affected by the treatments, while ammonium, osmolality and lactate were affected by both pharmaceuticals. Plasma triglycerides were affected in a temperature-dependent manner, and creatinine was only responsive to CBZ injection. HSP70 levels in muscle were only affected by CBZ injection. Some of the physiological identified responses to IB and CBZ are proposed as endpoints in further chronic studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alfirevic A, Mills T, Harrington P, Pinel T, Sherwood J, Jawaid A, Smith JC, March RE, Barratt BJ, Chadwick DW, Kevin Park B, Pirmohamed M (2006) Serious carbamazepine-induced hypersensitivity reactions associated with the HSP70 gene cluster. Pharmacogenet Genomics 16(4):287–296

    Article  CAS  Google Scholar 

  • Álvarez-Muñoz D, Rodríguez-Mozaz S, Maulvault AL, Tediosi A, Fernández-Tejedor M, Van den Heuvel F, Barceló D (2015) Occurrence of pharmaceuticals and endocrine disrupting compounds in macroalgaes, bivalves, and fish from coastal areas in Europe. Environmental Research Part B 143:56–64. doi:10.1016/j.envres.2015.09.018

    Article  Google Scholar 

  • Ambrósio AF, Soares-da-Silva P, Carvalho CM, Carvalho AP (2002) Mechanisms of action of carbamazepine and its derivatives, oxcarbazepine, BIA 2-093, and BIA 2-024. Neurochem Res 27(1–2):121–130. doi:10.1023/A:1014814924965

    Article  Google Scholar 

  • Arjona FJ, Ruiz-Jarabo I, Vargas-Chacoff L, del Río MPM, Flik G, Mancera JM, Klaren PHM (2010) Acclimation of Solea senegalensis to different ambient temperatures: implications for thyroidal status and osmoregulation. Mar Biol 157(6):1325–1335

    Article  CAS  Google Scholar 

  • Arjona FJ, Vargas-Chacoff L, Martín del Río MP, Flik G, Mancera JM, Klaren PHM (2011) Effects of cortisol and thyroid hormone on peripheral outer ring deiodination and osmoregulatory parameters in the Senegale sole (Solea senegalensis). J Endocrinol 208:323–330. doi:10.1530/JOE-10-0416

    CAS  Google Scholar 

  • Artom, N., Oddo, S., Pende, A., Ottonello, L., Giusti, M., and Dallegri, F. (2013). Syndrome of inappropriate antidiuretic hormone secretion and ibuprofen, a rare association to be considered: role of tolvaptan. Case Reports in Endocrinology. Vol. 2013, Article ID 818259, 4 pages. doi: 10.1155/2013/818259

  • Avgerinos A, Hutt AJ (1990) Interindividual variability in the enantiomeric disposition of ibuprofen following the oral administration of the racemic drug to healthy volunteers. Chirality 2(4):249–256. doi:10.1002/chir.530020410

    Article  CAS  Google Scholar 

  • Balment RJ, Warne JM, Tierney M, Hazon N (1993) Arginine vasotocin and fish osmoregulation. Fish Physiol Biochem 11(1–6):189–194. doi:10.1007/BF00004566

    Article  CAS  Google Scholar 

  • Bartoskova M, Dobsikova R, Stancova V, Zivna D, Blahova J, Marsalek P, Faggio C (2013) Evaluation of ibuprofen toxicity for zebrafish (Danio rerio) targeting on selected biomarkers of oxidative stress. Neuroendocrinol Lett 34(SUPPL. 2):102–108

    CAS  Google Scholar 

  • Bertilsson L (1978) Clinical pharmacokinetics of carbamazepine. Clin Pharmacokinet 3(2):128–143. doi:10.2165/00003088-197803020-00003

    Article  CAS  Google Scholar 

  • Blair B, Nikolaus A, Hedman C, Klaper R, Grundl T (2015) Evaluating the degradation, sorption, and negative mass balances of pharmaceuticals and personal care products during wastewater treatment. Chemosphere 134:395–401. doi:10.1016/j.chemosphere.2015.04.078

    Article  CAS  Google Scholar 

  • Boix C, Ibáñez M, Sancho JV, Parsons JR, Voogt P d, Hernández F (2016) Biotransformation of pharmaceuticals in surface water and during waste water treatment: identification and occurrence of transformation products. J Hazard Mater 302:175–187. doi:10.1016/j.jhazmat.2015.09.053

    Article  CAS  Google Scholar 

  • Boxall ABA, Keller VDJ, Straub JO, Monteiro SC, Fussell R, Williams RJ (2014) Exploiting monitoring data in environmental exposure modelling and risk assessment of pharmaceuticals. Environ Int 73:176–185. doi:10.1016/j.envint.2014.07.018

    Article  CAS  Google Scholar 

  • Brandão, F. P., Rodrigues, S., Castro, B. B., Gonçalves, F., Antunes, S. C. Nunes, B. (2013). Short-term effects of neuroactive pharmaceutical drugs on a fish species: biochemical and behavioral effects. Aquatic Toxicology, 144–145, 218–22910.1016/j.aquatox.2013.10.005

  • Brozinski J, Lahti M, Meierjohann A, Oikari A, Kronberg L (2013a) The anti-inflammatory drugs diclofenac, naproxen and ibuprofen are found in the bile of wild fish caught downstream of a wastewater treatment plant. Environ Sci Technol 47(1):342–348. doi:10.1021/es303013j

    Article  CAS  Google Scholar 

  • Brozinski J, Lahti M, Oikari A, Kronberg L (2013b) Identification and dose dependency of ibuprofen biliary metabolites in rainbow trout. Chemosphere 93(9):1789–1795. doi:10.1016/j.chemosphere.2013.06.018

    Article  CAS  Google Scholar 

  • Chen H, Zha J, Liang X, Li J, Wang Z (2014) Effects of the human antiepileptic drug carbamazepine on the behavior, biomarkers, and heat shock proteins in the Asian clam Corbicula fluminea. Aquat Toxicol 155:1–8. doi:10.1016/j.aquatox.2014.06.001

    Article  Google Scholar 

  • Collier AC, Tingle MD, Keelan JA, Paxton JW, Mitchell MD (2000) A highly sensitive fluorescent microplate method for the determination of UDP-glucuronosyl transferase activity in tissues and placental cell lines. Drug Metab Dispos 28(10):1184–1186

    CAS  Google Scholar 

  • Connors KA, Du B, Fitzsimmons PN, Chambliss CK, Nichols JW, Brooks BW (2013a) Enantiomer-specific in vitro biotransformation of select pharmaceuticals in rainbow trout (Oncorhynchus mykiss). Chirality 25(11):763–767. doi:10.1002/chir.22211

    Article  CAS  Google Scholar 

  • Connors KA, Du B, Fitzsimmons PN, Hoffman AD, Chambliss CK, Nichols JW, Brooks BW (2013b) Comparative pharmaceutical metabolism by rainbow trout (Oncorhynchus mykiss) liver S9 fractions. Environ Toxicol Chem 32(8):1810–1818. doi:10.1002/etc.2240

    Article  CAS  Google Scholar 

  • Contardo-Jara V, Lorenz 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. doi:10.1016/j.aquatox.2011.07.017

    Article  CAS  Google Scholar 

  • Corcoran J, Lange A, Winter MJ, Tyler CR (2012) Effects of pharmaceuticals on the expression of genes involved in detoxification in a carp primary hepatocyte model. Environmental Science & Technology 46(11):6306–6314. doi:10.1021/es3005305

    Article  CAS  Google Scholar 

  • Corcoran J, Winter MJ, Tyler CR (2010) Pharmaceuticals in the aquatic environment: a critical review of the evidence for health effects in fish. Crit Rev Toxicol 40(4):287–304. doi:10.3109/10408440903373590

    Article  CAS  Google Scholar 

  • Costas B, Aragão C, Ruiz-Jarabo I, Vargas-Chacoff L, Arjona FJ, Mancera JM, Conceição LEC (2012) Different environmental temperatures affect amino acid metabolism in the eurytherm teleost Senegalese sole (Solea senegalensis, Kaup, 1858) as indicated by changes in plasma metabolites. Amino Acids 43:327–335. doi:10.1007/s00726-011-1082-0

    Article  CAS  Google Scholar 

  • Crane M, Watts C, Boucard T (2006) Chronic aquatic environmental risks from exposure to human pharmaceuticals. Sci Total Environ 367(1):23–41

    Article  CAS  Google Scholar 

  • Daughton CG (2016) Pharmaceuticals and the environment (PiE): evolution and impact of the published literature revealed by bibliometric analysis. Sci Total Environ 562:391–426. doi:10.1016/j.scitotenv.2016.03.109

    Article  CAS  Google Scholar 

  • Evans A. M (2001) Comparative pharmacology of S(+)-ibuprofen and R(−)-ibuprofen. Clin Rheumatol 20(1):9–14. doi:10.1007/BF03342662

    Article  Google Scholar 

  • Ferrari B, Paxéus N, Giudice RL, Pollio A, Garric J (2003) Ecotoxicological impact of pharmaceuticals found in treated wastewaters: study of carbamazepine, clofibric acid, and diclofenac. Ecotoxicol Environ Saf 55(3):359–370. doi:10.1016/S0147-6513(02)00082-9

    Article  CAS  Google Scholar 

  • Gaw S, Thomas KV, Hutchinson TH (2014) Sources, impacts and trends of pharmaceuticals in the marine and coastal environment. Philos Trans R Soc B 369:20130572. doi:10.1098/rstb.2013.0572

    Article  Google Scholar 

  • Gomez CF, Constantine L, Huggett DB (2010) The influence of gill and liver metabolism on the predicted bioconcentration of three pharmaceuticals in fish. Chemosphere 81(10):1189–1195. doi:10.1016/j.chemosphere.2010.09.043

    Article  CAS  Google Scholar 

  • Gomez CF, Constantine L, Moen M, Vaz A, Wang W, Huggett DB (2011) Ibuprofen metabolism in the liver and gill of rainbow trout, Oncorhynchus mykiss. Bull Environ Contam Toxicol 86(3):247–251. doi:10.1007/s00128-011-0200-8

    Article  CAS  Google Scholar 

  • Gravel A, Vijayan MM (2007) Non-steroidal anti-inflammatory drugs disrupt the heat shock response in rainbow trout. Aquat Toxicol 81(2):197–206. doi:10.1016/j.aquatox.2006.12.001

    Article  CAS  Google Scholar 

  • Gravel A, Wilson JM, Pedro DFN, Vijayan MM (2009) Non-steroidal anti-inflammatory drugs disturb the osmoregulatory, metabolic and cortisol responses associated with seawater exposure in rainbow trout. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 149(4):481–490. doi:10.1016/j.cbpc.2008.11.002

    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-Sørensen B, Nors Nielsen S, Lanzky PF, Ingerslev F, Holten Lützhøft HC, Jørgensen SE (1998) Occurrence, fate and effects of pharmaceutical substances in the environment- a review. Chemosphere 36(2):357–393. doi:10.1016/S0045-6535(97)00354-8

    Article  Google Scholar 

  • Hamman MA, Thompson GA, Hall SD (1997) Regioselective and stereoselective metabolism of ibuprofen by human cytochrome P450 2C. Biochem Pharmacol 54(1):33–41. doi:10.1016/S0006-2952(97)00143-3

    Article  CAS  Google Scholar 

  • Heberer T (2002a) Occurrence, fate, and removal of pharmaceutical residues in the aquatic environment: a review of recent research data. Toxicol Lett 131(1–2):5–17

    Article  CAS  Google Scholar 

  • Heberer T (2002b) Tracking persistent pharmaceutical residues from municipal sewage to drinking water. J Hydrol 266(3–4):175–189. doi:10.1016/S0022-1694(02)00165-8

    Article  CAS  Google Scholar 

  • Hill, R. W. Wyse, G. A. Anderson, M (2012). Animal physiology, Third Edition. Sunderland, MA, USA. Sinauer Associates. ISBN: 978-0-87893-559-8.

  • Jeffries KM, Brander SM, Britton MT, Fangue NA, Connon RE (2015) Chronic exposures to low and high concentrations of ibuprofen elicit different gene response patterns in a euryhaline fish. Environ Sci Pollut Res 22(22):17397–17413. doi:10.1007/s11356-015-4227-y

    Article  CAS  Google Scholar 

  • James MO, Stuchal LD, Nyagode BA (2008) Glucuronidation and sulfonation, in vitro, of the major endocrine-active metabolites of methoxychlor in the channel catfish, Ictalurus punctatus, and induction following treatment with 3-methylcholanthrene. Aquat Toxicol 86:227–238. doi:10.1016/j.aquatox.2007.11.003

    Article  CAS  Google Scholar 

  • Jones HS, Trollope HT, Hutchinson TH, Panter GH, Chipman JK (2012) Metabolism of ibuprofen in zebrafish larvae. Xenobiotica 42(11):1069–1075. doi:10.3109/00498254.2012.684410

    Article  CAS  Google Scholar 

  • Jones E (2007) Drug-induced syndrome of inappropriate antidiuretic hormone. Canadian Pharmacists Journal 140(6):397–399. doi:10.3821/1913-701X(2007)140[397:DSOIAH]2.0.CO;2

    Article  Google Scholar 

  • Kepp DR, Sidelmann UG, Hansen SH (1997) Isolation and characterization of major phase I and II metabolites of ibuprofen. Pharm Res 14(5):676–680. doi:10.1023/A:1012125700497

    Article  CAS  Google Scholar 

  • Koenig S, Solé M (2012) Natural variability of hepatic biomarkers in Mediterranean deep-sea organisms. Mar Environ Res 79:122–131. doi:10.1016/j.marenvres.2012.06.005

    Article  CAS  Google Scholar 

  • Lahti M, Brozinski JM, Jylhä A, Kronberg L, Oikariy A (2011) Uptake from water, biotransformation, and biliary excretion of pharmaceuticals by rainbow trout. Environ Toxicol Chem 30(6):1403–1411. doi:10.1002/etc.501

    Article  CAS  Google Scholar 

  • Lee WH, Kim K, Kim MG, Lee SB (1995) Enzymatic resolution of racemic ibuprofen esters: effects of organic cosolvents and temperature. J Ferment Bioeng 80(6):613–615. doi:10.1016/0922-338X(96)87742-7

    Article  CAS  Google Scholar 

  • Li J, Zhang N, Ye B, Ju W, Orser B, Fox JEM, Lu W (2007) Non-steroidal anti-inflammatory drugs increase insulin release from beta cells by inhibiting ATP-sensitive potassium channels. Br J Pharmacol 151(4):483–493. doi:10.1038/sj.bjp.0707259

    Article  CAS  Google Scholar 

  • Li Z, Velisek J, Zlabek V, Grabic R, Machova J, Kolarova J, Randak T (2010a) Hepatic antioxidant status and hematological parameters in rainbow trout, Oncorhynchus mykiss, after chronic exposure to carbamazepine. Chem Biol Interact 183(1):98–104. doi:10.1016/j.cbi.2009.09.009

    Article  CAS  Google Scholar 

  • Li Z, Zlabek V, Grabic R, Velisek J, MacHova J, Randak T (2010b) Enzymatic alterations and RNA/DNA ratio in intestine of rainbow trout, Oncorhynchus mykiss, induced by chronic exposure to carbamazepine. Ecotoxicology 19(5):872–878. doi:10.1007/s10646-010-0468-1

    Article  CAS  Google Scholar 

  • Li Z, Zlabek V, Velisek J, Grabic R, Machova J, Kolarova J, Randak T (2011) Acute toxicity of carbamazepine to juvenile rainbow trout (Oncorhynchus mykiss): effects on antioxidant responses, hematological parameters and hepatic EROD. Ecotoxicol Environ Saf 74(3):319–327. doi:10.1016/j.ecoenv.2010.09.008

    Article  CAS  Google Scholar 

  • Li Z, Zlabek V, Velisek J, Grabic R, Machova J, Randak T (2009) Responses of antioxidant status and Na+–K+-ATPase activity in gill of rainbow trout, Oncorhynchus mykiss, chronically treated with carbamazepine. Chemosphere 77(11):1476–1481. doi:10.1016/j.chemosphere.2009.10.031

    Article  CAS  Google Scholar 

  • Librán-Pérez M, Figueiredo-Silva AC, Panserat S, Geurden I, Míguez JM, Polakof S, Soengas JL (2013) Response of hepatic lipid and glucose metabolism to a mixture or single fatty acids: possible presence of fatty acid-sensing mechanisms. Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology 164(1):241–248

    Article  Google Scholar 

  • López-Rodríguez R, Novalbos J, Gallego-Sandín S, Román-Martínez M, Torrado J, Gisbert JP, Abad-Santos F (2008) Influence of CYP2C8 and CYP2C9 polymorphisms on pharmacokinetic and pharmacodynamic parameters of racemic and enantiomeric forms of ibuprofen in healthy volunteers. Pharmacol Res 58(1):77–84. doi:10.1016/j.phrs.2008.07.004

    Article  Google Scholar 

  • Maranho LA, Baena-Nogueras RM, Lara-Martín PA, DelValls TA, Martín-Díaz ML (2014) Bioavailability, oxidative stress, neurotoxicity and genotoxicity of pharmaceuticals bound to marine sediments. The use of the polychaete Hediste diversicolor as bioindicator species. Environ Res 134:353–365. doi:10.1016/j.envres.2014.08.014

    Article  CAS  Google Scholar 

  • Moreno-González R, Rodríguez-Mozaz S, Huerta B, Barceló D, León VM (2016) Do pharmaceuticals bioaccumulate in marine molluscs and fish from a coastal lagoon? Environ Res 146:282–298. doi:10.1016/j.envres.2016.01.001

    Article  Google Scholar 

  • Noyes PD, McElwee MK, Miller HD, Clark BW, Van Tiem LA, Walcott KC, Erwin KN, Levin ED (2009) The toxicology of climate change: environmental contaminants in a warming world. Environ Int 35:971–986. doi:10.1016/j.envint.2009.02.006

    Article  CAS  Google Scholar 

  • Patrignani P, Patrono C (2015) Cyclooxygenase inhibitors: from pharmacology to clinical read-outs. Biochim Biophys Acta Mol Cell Biol Lipids 1851(4):422–432. doi:10.1016/j.bbalip.2014.09.016

    Article  CAS  Google Scholar 

  • Rainsford, K. D. (2005). Ibuprofen: a critical bibliographic review. London, UK. Taylor & Francis 0-203-37518-1.

  • Rainsford, K. D (2012) Ibuprofen: pharmacology, therapeutics and side effects. Springer Heidelberg New York Dordrecht London 978-3-0348-0495-0 10.1007/978-3-0348-0496-7.

  • Ramirez AJ, Mottaleb MA, Brooks BW, Chambliss CK (2007) Analysis of pharmaceuticals in fish using liquid chromatography-tandem mass spectrometry. Anal Chem 79(8):3155–3163. doi:10.1021/ac062215i

    Article  CAS  Google Scholar 

  • Riva R, Albani F, Contin M, Baruzzi A (1996) Pharmacokinetic interactions between antiepileptic drugs. Clinical considerations. Clin Pharmacokinet 31(6):470–493

    Article  CAS  Google Scholar 

  • Roche, C., Ragot, C., Moalic, J. L., Simon, F. Oliver, M (2013). Ibuprofen can induce syndrome of inappropriate diuresis in healthy young patients. Case Reports in Medicine 2013 167267, 4 10.1155/2013/167267

  • Rodrigues, L. C., Van den Bergh, J. C. J. M., Loureiro, M. L., Nunes, P. A. L. D. Rossi, S (2016). The cost of Mediterranean sea warming and acidification: a choice experiment among scuba divers at Medes Islands, Spain Environ Resour Econ 63(2) 289 311 10.1007/s10640-015-9935-8

    Article  Google Scholar 

  • Rudy AC, Knight PM, Brater DC, Hall SD (1991) Stereoselective metabolism of ibuprofen in humans: administration of R-, S- and racemic ibuprofen. J Pharmacol Exp Ther 259(3):1133–1139

    CAS  Google Scholar 

  • Santos JL, Aparicio I, Callejón M, Alonso E (2009) Occurrence of pharmaceutically active compounds during 1-year period in wastewaters from four wastewater treatment plants in Seville (Spain). J Hazard Mater 164(2–3):1509–1516. doi:10.1016/j.jhazmat.2008.09.073

    Article  CAS  Google Scholar 

  • 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(1–3):45–95. doi:10.1016/j.jhazmat.2009.10.100

    Article  CAS  Google Scholar 

  • Saravanan M, Devi KU, Malarvizhi A, Ramesh M (2012) Effects of ibuprofen on hematological, biochemical and enzymological parameters of blood in an Indian major carp, Cirrhinus mrigala. Environ Toxicol Pharmacol 34(1):14–22. doi:10.1016/j.etap.2012.02.005

    Article  CAS  Google Scholar 

  • Smith EM, Wilson JY (2010) Assessment of cytochrome P450 fluorometric substrates with rainbow trout and killifish exposed to dexamethasone, pregnenolone-16α-carbonitrile, rifampicin, and ß-naphthoflavone. Aquat Toxicol 97(4):324–333. doi:10.1016/j.aquatox.2010.01.005

    Article  CAS  Google Scholar 

  • Solé M, Fortuny A, Mañanós E (2014a) Effects of selected xenobiotics on hepatic and plasmatic biomarkers in juveniles of Solea senegalensis. Environ Res 135:227–235. doi:10.1016/j.envres.2014.09.024

    Article  Google Scholar 

  • Sole M, Livingstone DR (2005) Components of the cytochrome P450-dependent monooxygenase system and ‘NADPH-independent benzo[a]pyrene hydroxylase’ activity in a wide range of marine invertebrate species. Comparative Biochemistry and Physiology C-Toxicology & Pharmacology 141:20–31

    Article  Google Scholar 

  • Solé M, Sanchez-Hernandez JC (2015) An in vitro screening with emerging contaminants reveals inhibition of carboxylesterase activity in aquatic organisms. Aquat Toxicol 169:215–222. doi:10.1016/j.aquatox.2015.11.001

    Article  Google Scholar 

  • Solé M, Varó I, González-Mira A, Torreblanca A (2014b) Xenobiotic metabolism modulation after long-term temperature acclimation in juveniles of Solea senegalensis. Mar Biol 162(2):401–412. doi:10.1007/s00227-014-2588-2

    Article  Google Scholar 

  • Suwalsky M, Mennickent S, Norris B, Cardenas H (2006) The antiepileptic drug carbamazepine affects sodium transport in toad epithelium. Toxicol in Vitro 20(6):891–898

    Article  CAS  Google Scholar 

  • Tan SC, Patel BK, Jackson SHD, Swift CG, Hutt AJ (2002) Stereoselectivity of ibuprofen metabolism and pharmacokinetics following the administration of the racemate to healthy volunteers. Xenobiotica 32(8):683–697. doi:10.1080/00498250210142994

    Article  CAS  Google Scholar 

  • Tate SK, Depondt C, Sisodiya SM, Cavalleri GL, Schorge S, Soranzo N, Goldstein DB (2005) Genetic predictors of the maximum doses patients receive during clinical use of the anti-epileptic drugs carbamazepine and phenytoin. Proc Natl Acad Sci U S A 102(15):5507–5512. doi:10.1073/pnas.0407346102

    Article  CAS  Google Scholar 

  • Thibaut R, Schnell S, Porte C (2006) The interference of pharmaceuticals with endogenous and xenobiotic metabolizing enzymes in carp liver: an in vitro study. Environ Sci Technol 40(16):5154–5460. doi:10.1021/es0607483

    Article  CAS  Google Scholar 

  • Thomas PM, Foster GD (2004) Determination of nonsteroidal anti-inflammatory drugs, caffeine, and triclosan in wastewater by gas chromatography–mass spectrometry. Journal of Environmental Science and Health-Part A Toxic/Hazardous Substances and Environmental Engineering 39(8):1969–1978

    Article  Google Scholar 

  • Thorn CF, Leckband SG, Kelsoe J, Steven Leeder J, Müller DJ, Klein TE, Altman RB (2011) PharmGKB summary: carbamazepine pathway. Pharmacogenet Genomics 21(12):906–910. doi:10.1097/FPC.0b013e328348c6f2

    Article  CAS  Google Scholar 

  • Uno T, Ishizuka M, Itakura T (2012) Cytochrome P450 (CYP) in fish. Environmental Toxicology and Pharmacology 34(1):1–13. doi:10.1016/j.etap.2012.02.004

    Article  CAS  Google Scholar 

  • Varó I, Nunes B, Amat F, Torreblanca A, Guilhermino L, Navarro JC (2007) Effect of sublethal concentrations of copper sulphate on seabream Sparus aurata fingerlings. Aquat Living Resour 20(3):263–270. doi:10.1051/alr:2007039

    Article  Google Scholar 

  • Velasco Cano MV, Runkle de la Vega I (2010) Current aspects of the syndrome of inappropriate secretion of the antidiuretic hormone/syndrome of inappropriate antidiuresis. Endocrinol Nutr 57(2):22–29 in Spanish

    Article  Google Scholar 

  • Vernouillet G, Eullaffroy P, Lajeunesse A, Blaise C, Gagné F, Juneau P (2010) Toxic effects and bioaccumulation of carbamazepine evaluated by biomarkers measured in organisms of different trophic levels. Chemosphere 80(9):1062–1068. doi:10.1016/j.chemosphere.2010.05.010

    Article  CAS  Google Scholar 

  • Wang LQ, Falany CN, James MO (2004) Triclosan as a substrate and inhibitor of 3′-phosphoadenosine 5′-phosphosulfate-sulfotransferase and UDP-glucuronosyl transferase in human liver fractions. Drug Metab Dispos 32:1162–1169. doi:10.1124/dmd.104.000273

    Article  CAS  Google Scholar 

  • Weigel S, Berger U, Jensen E, Kallenborn R, Thoresen H, Hühnerfuss H (2004) Determination of selected pharmaceuticals and caffeine in sewage and seawater from Tromsø/Norway with emphasis on ibuprofen and its metabolites. Chemosphere 56(6):583–592. doi:10.1016/j.chemosphere.2004.04.015

    Article  CAS  Google Scholar 

  • Yu Y, Wu L (2014) Determination and occurrence of endocrine disrupting compounds, pharmaceuticals and personal care products in fish (Morone saxatilis). Frontiers of Environmental Science & Engineering 9(3):475–481. doi:10.1007/s11783-014-0640-6

    Article  Google Scholar 

  • Zenker A, Cicero MR, Prestinaci F, Bottoni P, Carere M (2014) Bioaccumulation and biomagnification potential of pharmaceuticals with a focus to the aquatic environment. J Environ Manag 133:378–387. doi:10.1016/j.jenvman.2013.12.017

    Article  CAS  Google Scholar 

  • Zhou Q, Chen P, Devaraneni PK, Martin GM, Olson EM, Shyng S (2014) Carbamazepine inhibits ATP-sensitive potassium channel activity by disrupting channel response to MgADP. Channels 8(4):376–382. doi:10.4161/chan.29117

    Article  Google Scholar 

  • 19th WHO Model List of Essential Medicines April 2015. http://www.who.int/medicines/publications/essentialmedicines/EML2015_8-May-15.pdf

Download references

Acknowledgments

This work was financed by the Ministry of Science and Innovation of Spain (Ref: CTM2010-16611). S. Piñeiro and L. Cabrera from Planta de Acuarios-SCSIE University of Valencia are acknowledged for the fish maintenance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A Torreblanca.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González-Mira, A., Varó, I., Solé, M. et al. Drugs of environmental concern modify Solea senegalensis physiology and biochemistry in a temperature-dependent manner. Environ Sci Pollut Res 23, 20937–20951 (2016). https://doi.org/10.1007/s11356-016-7293-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-7293-x

Keywords

Navigation