Environmental Science and Pollution Research

, Volume 23, Issue 20, pp 20937–20951 | Cite as

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

Research Article

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.

Keywords

Sole Plasma metabolites CYP enzymes Anti-oxidant enzymes HSP70 Ibuprofen Carbamazepine 

References

  1. 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):287–296CrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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):1325–1335CrossRefGoogle Scholar
  5. 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 Google Scholar
  6. 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
  7. 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 CrossRefGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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):102–108Google Scholar
  10. Bertilsson L (1978) Clinical pharmacokinetics of carbamazepine. Clin Pharmacokinet 3(2):128–143. doi:10.2165/00003088-197803020-00003 CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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 CrossRefGoogle Scholar
  14. 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.2013.10.005Google Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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 CrossRefGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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):1184–1186Google Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. Crane M, Watts C, Boucard T (2006) Chronic aquatic environmental risks from exposure to human pharmaceuticals. Sci Total Environ 367(1):23–41CrossRefGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. Evans A. M (2001) Comparative pharmacology of S(+)-ibuprofen and R(−)-ibuprofen. Clin Rheumatol 20(1):9–14. doi:10.1007/BF03342662 CrossRefGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. 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 CrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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
  34. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione-S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139Google Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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 CrossRefGoogle Scholar
  37. 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):5–17CrossRefGoogle Scholar
  38. 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 CrossRefGoogle Scholar
  39. Hill, R. W. Wyse, G. A. Anderson, M (2012). Animal physiology, Third Edition. Sunderland, MA, USA. Sinauer Associates. ISBN: 978-0-87893-559-8.Google Scholar
  40. 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 CrossRefGoogle Scholar
  41. 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 CrossRefGoogle Scholar
  42. 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 CrossRefGoogle Scholar
  43. 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 CrossRefGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. 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 CrossRefGoogle Scholar
  46. 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 CrossRefGoogle Scholar
  47. 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 CrossRefGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. 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 CrossRefGoogle Scholar
  50. 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 CrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 CrossRefGoogle Scholar
  53. 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):241–248CrossRefGoogle Scholar
  54. 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 CrossRefGoogle Scholar
  55. 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 CrossRefGoogle Scholar
  56. 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 CrossRefGoogle Scholar
  57. 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 CrossRefGoogle Scholar
  58. 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 CrossRefGoogle Scholar
  59. Rainsford, K. D. (2005). Ibuprofen: a critical bibliographic review. London, UK. Taylor & Francis 0-203-37518-1.Google Scholar
  60. 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.Google Scholar
  61. 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 CrossRefGoogle Scholar
  62. Riva R, Albani F, Contin M, Baruzzi A (1996) Pharmacokinetic interactions between antiepileptic drugs. Clinical considerations. Clin Pharmacokinet 31(6):470–493CrossRefGoogle Scholar
  63. 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 10.1155/2013/167267Google Scholar
  64. 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 CrossRefGoogle Scholar
  65. 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):1133–1139Google Scholar
  66. 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 CrossRefGoogle Scholar
  67. 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 CrossRefGoogle Scholar
  68. 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 CrossRefGoogle Scholar
  69. 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 CrossRefGoogle Scholar
  70. 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 CrossRefGoogle Scholar
  71. 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 141:20–31CrossRefGoogle Scholar
  72. 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 CrossRefGoogle Scholar
  73. 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 CrossRefGoogle Scholar
  74. Suwalsky M, Mennickent S, Norris B, Cardenas H (2006) The antiepileptic drug carbamazepine affects sodium transport in toad epithelium. Toxicol in Vitro 20(6):891–898CrossRefGoogle Scholar
  75. 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 CrossRefGoogle Scholar
  76. 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 CrossRefGoogle Scholar
  77. 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 CrossRefGoogle Scholar
  78. 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):1969–1978CrossRefGoogle Scholar
  79. 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 CrossRefGoogle Scholar
  80. 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 CrossRefGoogle Scholar
  81. 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 CrossRefGoogle Scholar
  82. 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 SpanishCrossRefGoogle Scholar
  83. 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 CrossRefGoogle Scholar
  84. 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 CrossRefGoogle Scholar
  85. 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 CrossRefGoogle Scholar
  86. 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 CrossRefGoogle Scholar
  87. 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 CrossRefGoogle Scholar
  88. 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 CrossRefGoogle Scholar
  89. 19th WHO Model List of Essential Medicines April 2015. http://www.who.int/medicines/publications/essentialmedicines/EML2015_8-May-15.pdf

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Departamento Biología Funcional y Antropología FísicaUniversitat de ValènciaBurjassotSpain
  2. 2.Instituto de Acuicultura Torre de la Sal (IATS-CSIC)Ribera de CabanesSpain
  3. 3.Institut de Ciencies del Mar (ICM-CSIC)BarcelonaSpain

Personalised recommendations