Carbamazepine-mediated pro-oxidant effects on the unicellular marine algal species Dunaliella tertiolecta and the hemocytes of mussel Mytilus galloprovincialis

Ecotoxicology

Volumn 22, Issue 8, 2013, Pages 1208-1220

  Tsiaka, Pinelopi ^a   Tsarpali, Vasiliki ^a   Ntaikou, Ioanna ^b   Kostopoulou, Maria N ^c   Lyberatos, Gerasimos ^d   Dailianis, Stefanos ^a  

^a UNIVERSITY OF PATRAS   (Greece)

^b INSTITUTE OF CHEMICAL ENGINEERING SCIENCES   (Greece)

^c UNIVERSITY OF THE AEGEAN   (Greece)

^d NATIONAL TECHNICAL UNIVERSITY OF ATHENS   (Greece)

Author keywords

Carbamazepine; Dunaliella; Hemocytes; Lipid peroxidation; Oxidative stress related effects; Toxicity

Indexed keywords

CARBAMAZEPINE; CAROTENOID; CHLOROPHYLL A; NITRIC OXIDE; NITRITE; SUPEROXIDE;

ALGA; BIOASSAY; BIVALVE; CHEMICAL POLLUTANT; ECOTOXICOLOGY; ENVIRONMENTAL FACTOR; ENVIRONMENTAL FATE; GROWTH RATE; GROWTH RESPONSE; LIPID; PHYTOTOXICITY;

ALGAL GROWTH; ANIMAL CELL; ARTICLE; BIOASSAY; BLOOD CELL; CELL DEATH; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG EFFECT; DRUG EXPOSURE; DUNALIELLA TERTIOLECTA; MYTILUS GALLOPROVINCIALIS; NONHUMAN; OXIDATIVE STRESS; PHYTOTOXICITY; PRIORITY JOURNAL;

ALGAE; DUNALIELLA; DUNALIELLA TERTIOLECTA; MYTILUS GALLOPROVINCIALIS;

ANIMALS; ANTICONVULSANTS; CARBAMAZEPINE; CAROTENOIDS; CHLOROPHYLL; CHLOROPHYTA; HEMOCYTES; LIPID PEROXIDATION; MALONDIALDEHYDE; MYTILUS; NITRIC OXIDE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SUPEROXIDES; WATER POLLUTANTS, CHEMICAL;

EID: 84885431605     PISSN: 09639292     EISSN: 15733017     Source Type: Journal    
DOI: 10.1007/s10646-013-1108-3     Document Type: Article

References (78)

1. Al Aukidy Μ, Verlicchi P, Jelic A, Petrovic M, Barcelò D (2012) Monitoring release of pharmaceutical compounds: occurrence and environmental risk assessment of two WWTP effluents and their receiving bodies in the Po Valley, Italy. Sci Total Environ 438:15-25
2. Aminot A, Ray F (2000) Standard procedures for the determination of chlorophyll a by spectroscopic methods. ICES Tech Marine Environ Sci 30:1-18
3. Andreozzi R, Marotta R, Pinto G, Pollio A (2002) Carbamazepine in water: persistence in the environment, ozonation treatment and preliminary assessment on algal toxicity. Water Res 36:2869-2877
4. APHA, Awwa, WEF (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, Washington
5. Arumugam M, Romestand B, Torreilles J, Roch P (2000) In vitro production of superoxide and nitric oxide (as nitrite and nitrate) by Mytilus galloprovincialis haemocytes upon incubation with PMA or laminarin or during yeast phagocytosis. Eur J Cell Biol 79:513-519
6. + exchanger and respiratory burst enzymes NADPH oxidase and NO synthase, in Cd-induced lipid peroxidation and DNA damage in haemocytes of mussels. Comp Biochem Physiol C 152:346-352
7. Borenfreund E, Puerner JA (1985) Toxicity determined in vitro by morphological alterations and neutral red absorption. Toxicol Lett 24:119-124
8. Bouki E, Dimitriadis VK, Kaloyianni M, Dailianis S (2013) Antioxidant and pro-oxidant challenge of tannic acid in mussel hemocytes exposed to cadmium. Mar Environ Res 85:13-20
9. Canesi L, Lorusso LC, Ciacci C, Betti M, Regoli F, Poiana G, Gallo G, Marcomini A (2007) Effects of blood lipid lowering pharmaceuticals (bezafibrate and gemfibrozil) on immune and digestive gland functions of the bivalve mollusc, Mytilus galloprovincialis. Chemosphere 69:994-1002
10. Cao A, Mercado L, Ramos-Martinez JI, Barcia R (2003) Primary cultures of haemocytes from Mytilus galloprovincialis Lmk: expression of IL-2Rα. Aquaculture 216:1-8
11. Carballal MJ, Lopez MC, Azebedo C, Villalba A (1997) In vitro study of phagocytic ability of Mytilus galloprovincialis Lmk. haemocytes. Fish Shellfish Immunol 7:403-416
12. Chatziargyriou V, Dailianis S (2010) The role of selenium-dependent glutathione peroxidase (Se-GPx) against oxidative and genotoxic effects of mercury in haemocytes of mussel Mytilus galloprovincialis (Lmk.). Toxicol In Vitro 24:1363-1372
13. Chen M, Ohman K, Metcalfe C, Ikonomou MG, Amatya PL, Wilson J (2006) Pharmaceuticals and endocrine disruptors in wastewater treatment effluents and in the water supply system of Calgary, Alberta, Canada. Water Qual Res J Can 41:351-364
14. Clara M, Strenn B, Kreuzinger N (2004) Carbamazepine as a possible anthropogenic marker in the aquatic environment: investigations on the behaviour of carbamazepine in wastewater treatment and during groundwater infiltration. Water Res 38:947-954
15. 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 105:428-437
16. + exchanger in the induction of cadmium toxic effects. Fish Shellfish Immunol 27:446-453
17. Del Campo JA, Garcia-Gonzalez M, Guerrero MG (2007) Outdoor cultivation of microalgae for carotenoid production: current state and perspectives. Appl Microbiol Biotechnol 74:1163-1174
18. DeLorenzo ME, Flemming J (2008) Individual and mixture effects of selected pharmaceuticals and personal care products on the marine phytoplankton species Dunaliella tertiolecta. Arch Environ Contam Toxicol 54:203-210
19. Dietrich DR, Webb SF, Petry T (2002) Hot spot pollutants: pharmaceuticals in the environment. Toxicol Lett 131:1-3
20. El-Sheekh MM, El-Naggar AH, Osman MEH, El-Mazaly E (2003) Effect of cobalt on growth, pigments and the photosynthetic electron transport in Monoraphidium minutum and Nitzchia perminuta. Braz J Plant Physiol 15:159-166
21. Fent K, Weston AA, Caminada D (2006) Ecotoxicology of human pharmaceuticals. Aquat Toxicol 76:22-159
22. Ferrari B, Raxeus 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 55:359-370
23. Gagne F, Blaise C, Andre C (2006a) Occurrence of pharmaceutical products in a municipal effluent and toxicity to rainbow trout (Oncorhynchus mykiss) hepatocytes. Ecotoxicol Environ Saf 64:329-336
24. Gagne F, Blaise C, Fournier M, Hansen PD (2006b) Effects of selected pharmaceutical products on phagocytic activity in Elliptio complanata mussels. Comp Biochem Physiol C 143:179-186
25. Garcia-Gonzalez M, Moreno J, Manzano JC, Florencio FJ, Guerrero MG (2005) Production of Dunaliella salina biomass rich in 9-cis-β-carotene and lutein in a closed tubular photobioreactor. J Biotechnol 115:81-90
26. Garcia-Morales I, Rieger JS, Gil-Nagel A, Fernandez JLH (2007) Antiepileptic drugs: from a scientific evidence to clinical practice. Neurologist 13:S20-S28
27. Georgiou DC, Grintzalis K, Zervoudakis G, Papapostolou I (2008) Mechanism of Coomassie brilliant blue G-250 binding to proteins: a hydrophobic assay for nanogram quantities of proteins. Anal Bioanal Chem 391:391-403
28. 15N) nitrate in biological fluids. Anal Biochem 126:131-138
29. Grintzalis K, Georgiou CD, Dailianis S (2012) Total thiol redox status as a potent biomarker of PAH-mediated effects on mussels. Mar Environ Res 81:26-34
30. Gust M, Gelinas M, Fortier M, Fournier M, Gagne F (2012) In vitro immunotoxicity of environmentally representative antibiotics to the freshwater mussel Elliptio complanata. Environ Pollut 169:50-58
31. Gust M, Fortier M, Garric J, Fournier M, Gagne F (2013) Effects of short-term exposure to environmentally relevant concentrations of different pharmaceutical mixtures on the immune response of the pond snail Lymnaea stagnalis. Sci Total Environ 445-446:210-218
32. Heberer T, Reddersen K, Mechlinski A (2002) From municipal sewage to drinking water: fate and removal of pharmaceutical residues in the aquatic environment in urban areas. Water Sci Technol 46:81-88
33. Hermes-Lima M, Storey JM, Storey KB (2001) Antioxidant defenses and animal adaptation to oxygen availability during environmental stress. In: Storey KB, Storey JM (eds) Protein adaptation and signal transduction. Elsevier, Amsterdam, pp 263-287
34. Huerta B, Rodríguez-Mozaz S, Barceló D (2012) Pharmaceuticals in biota in the aquatic environment: analytical methods and environmental implications. Anal Bioanal Chem 404:2611-2624
35. Jones OAH, Volvoulis N, Lester JN (2002) Aquatic environmental assessment of the top 25 English prescription pharmaceuticals. Water Res 36:5013-5022
36. Jos A, Repetto G, Rios JC et al (2003) Ecotoxicological evaluation of carbamazepine using six different model systems with eighteen endpoints. Toxicol In Vitro 17:525-532
37. Kim Y, Choi K, Jung J, Park S, Kim PG, Park J (2007) Aquatic toxicity of acetaminophen, carbamazepine, cimetidine, diltiazem and six major sulfonamides, and their potential ecological risks in Korea. Environ Int 33:370-375
38. Kosma CI, Lambropoulou DA, Albanis TA (2010) Occurrence and removal of PPCPs in municipal and hospital wastewaters in Greece. J Hazard Mater 179:804-817
39. Kramer NI, Krismartina M, Rico-Rico A, Blaauboer BJ, Hermens JLM (2012) Quantifying processes determining the free concentration of phenanthrene in basal cytotoxicity assays. Chem Res Toxicol 25:436-445
40. Li ZH, Velisek J, Zlabek V, Grabic R, Machova J, Kolarova J, Randak T (2010) Hepatic antioxidant status and hematological parameters in rainbow trout, Oncorhynchus mykiss, after chronic exposure to carbamazepine. Chem-Biol Interact 183:98-104
41. Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656-666
42. 2+ on early stages of chlorophyll biosynthesis and pheophytinization in Euglena gracilis. Russ J Plant Physiol 50:390-394
43. Martin-Diaz L, Franzellitti S, Buratti S, Valbonesi P, Capuzzo A, Fabbri E (2009) Effects of environmental concentrations of the antiepileptic drug carbamazepine on biomarkers and cAMP-mediated cell signaling in the mussel Mytilus galloprovincialis. Aquat Toxicol 94:177-185
44. Montezinho LP, Mork A, Duarte CB, Penschuck S, Geraldes CF, Castro MM (2007) Effects of mood stabilizers on the inhibition of adenylate cyclase via dopamine D(2)-like receptors. Bipolar Disord 9:290-297
45. Nalecz-Jawecki G, Persoone G (2006) Toxicity of selected pharmaceuticals to the anostracan crustacean Thamnocephalus platyurus: comparison of sublethal and lethal effect levels with the 1 h Rapidtoxkit and the 24 h Thamnotoxkit microbiotests. Environ Sci Pollut Res 13:22-27
46. Nikookar K, Moradshahi A, Hosseini L (2005) Physiological responses of Dunaliella salina and Dunaliella tertiolecta to copper toxicity. Biomol Eng 22:141-146
47. NIWA (1998) Marine Algae Dunaliella tertiolecta Chronic Toxicity Test Protocol (MFE 80205: Appendix 1). Ecotoxicology Lab, New Zealand
48. OECD (1984) Alga, growth inhibition test (201) OECD Guideline for Testing of Chemicals. Organisation for Economic Co-Operation and Development, Paris
49. Olabarrieta I, L'Azou B, Yuric S, Cambar J, Cajaraville MP (2001) In vitro effects of cadmium on two different animal cell models. Toxicol In Vitro 15:511-517
50. Parolini M, Quinn B, Binelli A, Provini A (2011) Cytotoxicity assessment of four pharmaceutical compounds on the zebra mussel (Dreissena polymorpha) haemocytes, gill and digestive gland primary cell cultures. Chemosphere 84:91-100
51. Paxéus N (2004) Removal of selected non-steroidal anti-inflammatory drugs (NSAIDs), gemfibrozil, carbamazepine, b-blockers, trimethoprim and Triclosan in conventional wastewater treatment plants in five EU countries and their discharge to the aquatic environment. Water Sci Technol 50:253-260
52. Pipe RK, Jackie AC, Farley SR (1995) Assays for measuring immune response in the mussel Mytilus edulis. In: Stolen JS, Fletcher TC, Smith SA, Zelikoff JT, Kaattari SL, Anderson RS, Soderhall K, Weeks-Perkins BA (eds) Immunology and pathology of aquatic invertebrates: Techniques in Fish Immunology. Fair Haven SOS Publications, New Jersey, pp 93-99
53. Quinn B, Gagne F, Blaise C (2004) Oxidative metabolism activity in Hydra attenuate exposed to carbamazepine. Fresen Environ Bull 13:1-6
54. Quinn B, Gagne 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 attenuate. Sci Total Environ 389:306-314
55. Reish DJ, Lemay JA (2008) Bioassay manual for dredged materials. Technical Report, DACW-09-83R-005, US Army Crops of Engineers, Los Angeles District, Los Angeles, CA
56. Richardson SD, Ternes TA (2011) Water Analysis: emerging contaminants and current issues. Anal Chem 83:4614-4648
57. Rizzo L, Meric S, Guida M, Kassinos M, Belgiorno V (2010) Heterogenous photocatalytic degradation kinetics and detoxification of an urban wastewater treatment plant effluent contaminated with pharmaceuticals. Water Res 43:4070-4078
58. RxList (2006) The Internet Drug Index. http://www.rxlist.com
59. Sacan MT, Balcioglu IA (2006) A case study on algal response to raw and treated effluents from an aluminum plating plant and a pharmaceutical plant. Ecotox Environ Saf 64:234-243
60. Salguero A, De la Morena B, Vigara J, Vega JM, Vilchez C, Leon R (2003) Carotenoids as protective response against oxidative damage in Dunaliella bardawil. Biomol Eng 20:249-253
61. 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 62:1389-1395
62. Shaish A, Ben-Amotz A, Avron M (1992) Biosynthesis of b-carotene in Dunaliella. Method Enzymol 213:439-444
63. Stamatelatou K, Frouda C, Fountoulakis MS, Drillia P, Kornaros M, Lyberatos G (2003) Pharmaceuticals and health care products in wastewater effluents: the example of carbamazepine. Water Sci Technol: Water Supply 3:131-137
64. Tafalla C, Novoa B, Figueras A (2002) Production of nitric oxide by mussel (Mytilus galloprovincialis) hemocytes and effect of exogenous nitric oxide on phagocytic functions. Comp Biochem Physiol B 132:423-431
65. Telfer A (2002) What is β-carotene doing in the photosystem II reaction centre? Philos Trans R Soc B-Biol Sci 357:1431-1439
66. Ternes TA (1998) Occurrence of drugs in German sewage treatment plants and rivers. Water Res 32:3245-3260
67. Toufexi E, Tsarpali V, Efthimiou I, Vidali M-S, Vlastos D, Dailianis S (2013) Environmental and human risk assessment of landfill leachate: an integrated approach with the use of cytotoxic and genotoxic stress indices in mussel and human cells. J Hazard Mater 260:593-601
68. Vannini C, Domingo G, Marsoni M et al (2011) Effects of a complex mixture of therapeutic drugs on unicellular algae Pseudokirchneriella subcapitata. Aquat Toxicol 101:459-465
69. Vernouillet G, Eullaffroy P, Lajeunesse A, Blaise C, Gagne F, Juneau P (2010) Toxic effects and bioaccumulation of carbamazepine evaluated by biomarkers measured in organisms of different trophic levels. Chemosphere 80:1062-1068
70. Vouras Ch, Dailianis S (2012) Evidence for phosphatidylinositol-3-OH- kinase (PI3-kinase) involvement in Cd-mediated oxidative effects on haemocytes of mussels. Comp Biochem Physiol C 155:587-593
71. Wang W, Freemark K (1995) The use of plants for environmental monitoring and assessment. Ecotoxicol Environ Saf 30:289-301
72. Wills ED (1969) Lipid peroxide formation in microsomes. Biochem J 113:315-324
73. Winston GW, Moore MN, Straatsburg I, Kirchin M (1991) Lysosomal stability in Mytilus edulis L.: potential as a biomarker of oxidative stress related to environmental contamination. Arch Environ Contam Toxicol 21:401-408
74. Xia Y, Zweier JL (1997) Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages. Proc Natl Acad Sci USA 94:6954-6958
75. Zhang Y, Geißen S-U, Gal C (2008) Carbamazepine and diclofenac: removal in wastewater treatment plants and occurrence in water bodies. Chemosphere 73:1151-1161
76. Zhang W, Zhang M, Lin K, Sun W, Xiong B, Guo M, Cui X, Fu R (2012) Eco-toxicological effect of Carbamazepine on Scenedesmus obliquus and Chlorella pyrenoidosa. Environ Toxicol Pharmacol 33:344-352
77. Zhou JL, Zhang ZL, Banks E, Grover D, Jiang JQ (2009) Pharmaceutical residues in wastewater treatment works effluents and their impact on receiving river water. J Hazard Mater 166:655-661
78. Zuccato E, Calamari D, Natangelo M, Fanelli R (2000) Presence of therapeutic drugs in the environment. Lancet 355:1789-1790