Identification of biomarkers responsive to chronic exposure to pharmaceuticals in target tissues of Carcinus maenas

Marine Environmental Research

Volumn 87-88, Issue , 2013, Pages 1-11

  Aguirre Martinez G V ^a,b   Del Valls, T A ^a   Martin Diaz M L ^a,b  

^a UNIVERSITY OF CÁDIZ   (Spain)

^b Campus Universitario de Puerto Real   (Spain)

Author keywords

Bioassay; Biochemical responses; Crabs; Emergent contaminants; Hepatopancreas

Indexed keywords

BIOCHEMICAL RESPONSE; CRABS; ENVIRONMENTAL CONCENTRATION; GLUTATHIONE PEROXIDASE; GLUTATHIONE-S-TRANSFERASE; HEPATOPANCREAS; LYSOSOMAL MEMBRANE STABILITIES; MARINE ENVIRONMENT;

BIOASSAY; CAFFEINE; MUSCLE; SHELLFISH; TOXICITY;

HISTOLOGY;

BIOLOGICAL MARKER; CAFFEINE; DIBENZYLFLUORESCEIN DEALKYLASE; ENZYME; ETHOXYRESORUFIN DEETHYLASE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; IBUPROFEN; SEA WATER; UNCLASSIFIED DRUG;

BIOASSAY; BIOCHEMISTRY; BIOMARKER; CRAB; DRUG; MARINE POLLUTION; POLLUTION EXPOSURE; TOXICITY;

ANIMAL TISSUE; ARTICLE; BIOASSAY; CARCINUS MAENAS; CONTROLLED STUDY; CRAB; DNA DAMAGE; ECOTOXICITY; ENZYME ACTIVITY; GILL; GONAD; HEMOLYMPH; HEPATOPANCREAS; LIPID PEROXIDATION; LONG TERM EXPOSURE; LYSOSOME MEMBRANE; MARINE ENVIRONMENT; MUSCLE TISSUE; NONHUMAN; WATER POLLUTION INDICATOR;

ANIMALS; BIOLOGICAL AVAILABILITY; BIOLOGICAL MARKERS; BRACHYURA; CAFFEINE; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; FEMALE; IBUPROFEN; SPAIN; TISSUE DISTRIBUTION; WATER POLLUTANTS, CHEMICAL;

CARCINUS MAENAS; DECAPODA (CRUSTACEA);

EID: 84878390943     PISSN: 01411136     EISSN: 18790291     Source Type: Journal    
DOI: 10.1016/j.marenvres.2013.02.011     Document Type: Article

References (91)

1. Aguirre-Martínez G.V., Burattis S., Fabbri E., Del Valls T.A., Martín-Díaz M.L. Stability of lysosomal membrane in Carcinus maenas acts as a biomarker of exposure to pharmaceuticals. Environmental Monitoring and Assessment 2012, 10.1007/s10661-012-2827-2.
2. Aguirre-Martínez G.V., Salamanca M.J., Del Valls T.A., Martín-Díaz M.L. Biological and biochemical responses of Carcinus maenas: a consequence of pharmaceutical exposure. Abstracts/Comparative Biochemistry and Physiology A 2010, 157:S16-S17.
3. Andreozzi R., Marottaa R., Pinto G., Pollio A. Carbamazepine in water: persistence in the environment, ozonation treatment and preliminary assessment on algal toxicity. Water Research 2002, 36:2869-2877.
4. Ashton D., Hilton M., Thomas K.V. Investigating the environmental transport of human pharmaceuticals to streams in the United Kingdom. Science of the Total Environment 2004, 333(1-3):167-184.
5. Astley K.N., Meigh H.C., Glegg G.A., Braven J., Depledge M.H. Multi-variate analysis of biomarker responses in Mytilus edulis and Carcinus maenas from the Tees Estuary (UK). Marine Pollution Bulletin 1999, 39(1-2):145-154.
6. Bamber S.D., Depledge M.H. Responses of shore crabs to physiological challenges following exposure to selected environmental contaminants. Aquatic Toxicology 1997, 40:79-92.
7. Bebianno M.J., Lopes B., Guerra L., Hoarau P., Ferreira A.M. Glutathione S-tranferases and cytochrome P450 activities in Mytilus galloprovincialis from the South coast of Portugal: effect of abiotic factors. Environment International 2007, 33:550-558.
8. Beijer K., Abrahamson A., Brandt I. CYP1A inhibition in fish gill filaments: a novel assay applied on pharmaceuticals and other chemicals. Aquatic Toxicology 2010, 96:145-150.
9. Boryslawskyj M., Garrood A.C., Pearson J.T. Elevation of glutathione-S-transferase activity as a stress response to organochlorine compounds, in the freshwater mussel, Sphaerium corneum. Marine Environmental Research 1998, 23:101-104.
10. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:24-254.
11. Buratti S., Fabbri E., Pereira C.D.S., Ramos-Gómez J., Del Valls T.A., Martín-Díaz M.L. Application of neutral red retention assay in the clam Ruditapes philippinarum and the crab Carcinus maenas as a screening tool for sediment quality assessment in marine environment. Abstracts/Comparative Biochemistry and Physiology A 2010, 157:S22-S28.
12. Buser H.R., Poiger T., Muller M.D. Occurrence and environmental behavior of the chiral pharmaceutical drug ibuprofen in surface waters and in wastewater. Environmental Science & Technology 1999, 33:2529-2535.
13. Cajaraville M.P., Bebianno M.J., Blasco J., Porte C., Sarasquete C., Viarengo A. The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Science of the Total Environment 2000, 247:295-311.
14. Carballa M., Omil F., Lema J.M., Llompart M., García-Jares C., Rodríguez I., Gómez M., Ternes T. Behaviour of pharmaceuticals, cosmetics and hormones in a sewage treatment plant. Water Research 2004, 38(12):2918-2926.
15. Carlsson C., Johansson A.K., Alvan G., Bergman K., Kühler T. Are pharmaceuticals potent environmental pollutants? Part I: environmental risk assessment of selected active pharmaceutical ingredients. Science of the Total Environment 2006, 364:67-87.
16. Cheung C.C.C., Zheng G.J., Li A.M.Y., Richardson B.J., Lam P.K.S. Relationships between tissue concentrations of poly-cyclic aromatic hydrocarbons and antioxidative responses of marine mussels, Perna viridis. Aquatic Toxicology 2001, 52:189-203.
17. 2 and Si/BDD electrodes. Electrochimica Acta 2009, 54(5):1464-1472.
18. Cossu C., Doyotte A., Jacquin M.C., Babut M., Extinger A., Vasseur P. Glutathione reductase, selenium-dependent glutathione peroxidase, glutathione levels, and lipid peroxidation in fresh water bivalves, Unio tumidus, as biomarkers of aquatic contamination in field studies. Ecotoxicology and Environmental Safety 1997, 38:122-131.
19. Crane M., Watts C., Boucard T. Chronic aquatic environmental risks from exposure to human pharmaceuticals. Science of the Total Environment 2006, 367:23-41.
20. Dailianis S., Domouhtsidou G.P., Raftopoulou E., Kaloyianni M., Dimitriadis V.K. Evaluation of neutral red retention assay, micronucleus test, acetylcholinesterase activity and a signal transduction molecule (cAMP) in tissues of Mytilus galloprovincialis (L.), in pollution monitoring. Marine Environmental Research 2003, 56:443-470.
21. Di Giulio R.T., Washburn P.C., Wenning R.J., Winston G.W., Jewel C.S. Biochemical responses in aquatic animals: a review of determinants of oxidative stress. Environmental Toxicology and Chemistry 1989, 8:1103-1123.
22. Doyotte A., Cossu C., Jacquin M.C., Babut M., Vaseur P. Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or field exposure in the gills and the digestive gland of the freshwater bivalve Unio tumidus. Aquatic Toxicology 1997, 39:93-110.
23. Eades C., Waring C.P. The effects of diclofenac on the physiology of the green shore crab Carcinus maenas. Aquatic Toxicology 2010, 69:46-48.
24. Fent K., Weston A.A., Caminada D. Ecotoxicology of human pharmaceuticals. Aquatic Toxicology 2006, 76:122-159.
25. Ferrari B., Paxéus N., Lo Guiudice R., Pollio A., Garric J. Ecotoxicological impact of pharmaceuticals found in treated wastewaters: study of carbamazepine, clorifibric acid, and diclofenac. Ecotoxicology and Environmental Safety 2003, 55:359-370.
26. Gagné F., Blaise C. Hepatic metallothionein level and mixed function oxidase activity in fingerling rainbow trout (Oncorhynchus mykiss) after acute exposure to pulp and paper mill effluents. Water Research 1993, 27:1669-1682.
27. Gagné F., Blaise C., Hellou J. Endocrine disruption and health effects of caged mussels, Elliptio complanata, placed downstream from a primary-treated municipal effluent plume for 1 year. Comparative Biochemistry and Physiology C 2004, 138:33-44.
28. Gagné F., Bérubé E., Fournier M., Blaise C. Inflammatory properties of municipal effluents to Elliptio complanata mussels: lack of effects from anti-inflammatory drugs. Comparative Biochemistry and Physiology C 2005, 141:332-337.
29. Gagné F., Blaise C., André C. Occurrence of pharmaceuticals products in a municipal effluent and toxicity to rainbow trout (Oncorhynchus mykiss) hepatocytes. Ecotoxicology and Environmental Safety 2006, 64:329-336.
30. Gerhardt A., Janssens de Bisthoven L., MO Z., Wang C., Yang M., Wang Z. Short-term responses of Oryzias latipes (Pisces: Adrianichthyidae) and Macrobrachium nipponense (Crustacea: Palaemonidae) to municipal and pharmaceutical waste water Beijing, China: survival, behavior, biochemical biomarkers. Chemosphere 2002, 47:35-47.
31. Gibson A.M., Morgan R.M., MacDonald N., Nikitin A.G. Possible effects of the presence of common household chemicals in the environment: the growth of an aquatic bacterial species on high concentrations of caffeine. Journal of Biotech Research 2012, 4:72-79.
32. Gómez M.J., Martínez-Bueno M.J., Lacorte S., Fernández-Alba A.R., Agüera A. Pilot survey monitoring pharmaceuticals and related compounds in a sewage treatment plant located on the Mediterranean Coast. Chemosphere 2007, 66(6):993-1002.
33. Gros M., Petrović M., Barceló D. Development of a multi-residue analytical methodology based on liquid chromatography-tandem mass spectrometry (LC-MS/MS) for screening and trace level determination of pharmaceuticals in surface and wastewaters. Talanta 2006, 70:678-690.
34. Grung M., Källsqvist T., Sakshaug S., Skurtveit S., Thomas K.V. Environmental assessment of Norwegian priority pharmaceuticals based on the EMEA guideline. Ecotoxicology and Environmental Safety 2007, 71:328-340.
35. Halling-Sørensen B., Nors Nielsen S., Lanzky P.F., Ingerslev F., Holten Lützheft H.C., Jørgensen S.E. Occurrence, fate and effects of pharmaceuticals substances in the environment - a review. Chemosphere 1998, 36(2):357-393.
36. Heckmann L.H., Callaghan A., Hooper H.L., Connon R., Hutchinson T.H., Maund S.J. Chronic toxicity of ibuprofen to Daphnia magna: effects on life history traits and population dynamic. Toxicology Letters 2007, 172:137-145.
37. Irato P., Piccinni E., Cassini A., Santovito G. Antioxidant responses to variations in dissolved oxygen of Scapharca inaequivalvis and Tapes philippinarum, two bivalve species from the lagoon of Venice. Marine Pollution Bulletin 2007, 54:1020-1030.
38. Isidori M., Nardelli A., Parrella A., Pascarella L., Previtera L. A multispecies study to assess the toxic and genotoxic effect of pharmaceuticals: furosemide and its photoproduct. Chemosphere 2006, 63:785-793.
39. James M.O., Boyle S.M. Cytochromes P450 in crustacea. Comparative Biochemistry and Physiology C 1998, 121:157-172.
40. Khoshayand M.R., Abdollahi H., Shariatpanahi M., Saadatfard A., Mohammadi A. Simultaneous spectrophotometric determination of paracetamol, ibuprofen and caffeine in pharmaceuticals by chemometric methods. Spectrochimica Acta A 2008, 70(3):491-499.
41. Köhler A., Pluta H.J. Lysosomal injury and MFO activity in the liver of flounder (Platichthys flesus L.) in relation to histopathology of hepatic degeneration and carcinogenesis. Carcinogenesis 1995, 39:255-260.
42. Kolpin D.W., Furlong E.T., Meyer M.T., Thurman E.M., Zaugg S.D., Barber L.B., Buxton H.T. Pharmaceuticals, hormones and other organic wastewater in the US streams, 1999-2000: a national reconnaissance. Environmental Science & Technology 2002, 36:1202-1211.
43. Kosma C.I., Lambropoulou D.A., Albanis T.A. Occurrence and removal of PPCPs in municipal and hospital wastewaters in Greece. Journal of Hazardous Materials 2010, 179:804-817.
44. Laville N., Aït-Aïssa S., Gomez E., Casellas C., Porcher J.M. Effects of human pharmaceuticals on cytotoxicity, EROD activity and ROS production in fish hepatocytes. Toxicology 2004, 196:41-55.
45. Lafontaine Y., Gagné F., Blaise C., Costan G., Gagnon P., Chan H.M. Biomarkers in Zebra mussels (Dreissena polymorpha) for the assessment and monitoring of water quality of the St. Lawrence River (Canada). Aquatic Toxicology 2000, 50:51-70.
46. Livingstone D.R., Lips F., Garcia M.P., Pipe R.K. Antioxidant enzymes in the digestive gland of the common mussel Mytilus edulis. Marine Biology 1992, 112:265-276.
47. Livingstone D.R., Hill C., Giulio D. Contaminant stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Marine Pollution Bulletin 2001, 42(8):656-666.
48. Lowe D.M., Soverchia C., Moore M.N. Lysosomal membrane responses in the blood and digestive cells of mussels experimentally exposed to fluoranthene. Aquatic Toxicology 1995, 33:105-112.
49. Lyons B.P., Thain J.E., Stentiford G.D., Hylland K., Davies I.M., Vethaak A.D. Using biological effects tools to define good environmental status under the European Union marine strategy framework directive. Marine Pollution Bulletin 2010, 60:1647-1651.
50. Martín-Díaz M.L., Gagné F., Blaise C. The use of biochemical responses to assess ecotoxicological effects of pharmaceuticals and personal care products (PPCPs) after injection in the mussel Elliptio complanata. Environmental Toxicology and Pharmacology 2009, 28:237-242.
51. Martín-Díaz M.L., Franzellitti S., Buratti S., Valbonesi P., Capuzzo A., Fabbri E. Effects of environmental concentrations of the antiepilectic drug carbamazepine on biomarkers and cAMP-mediated cell signaling in the mussel Mytilus galloprovincialis. Aquatic Toxicology 2009, 94:177-185.
52. Martínez-Gómez C., Benedicto J., Campilloa J.A., Moore M. Application and evaluation of the neutral red retention (NRR) assay for lysosomal stability in mussel populations along the Iberian Mediterranean coast. Journal of Environmental Monitoring 2008, 10:490-499.
53. McFarland V.A., Inouye S.L., Lutz C.H., Jarvis A.S., Clarke J.U., McCant D.D. Biomarkers of oxidative stress and genotoxicity in livers of field collected brown bullhead, Ameiurus nebulosus. Archives of Environmental Contamination and Toxicology 1999, 37:236-241.
54. Miège C., Choubert J.M., Ribeiro L., Eusèbe M., Coquery M. Fate of pharmaceuticals and personal care products in wastewater treatment plants - conception of a database and first results. Environmental Pollution 2009, 157:1721-1726.
55. Monari M., Cattani O., Serrazanetti G.P., Selli A., Pagliuca G., Zironi E., O'Hara S.C., Livingstone D.R. Effect of exposure to benzo[a]pyrene on SODs, CYP1A1/1A2- and CYP2E1 immunopositive proteins in the blood clam Scapharca inaequivalvis. Marine Environmental Research 2007, 63(3):200-218.
56. Moore N.N., Pip R.K., Farrar S.V. Lysosomal and microsomal responses to environmental factors in Littorina littorea, from Sullom Voe. Marine Pollution Bulletin 1982, 13:340-345.
57. Nakada N., Tanishima T., Shinohara H., Kiri K., Takada H. Pharmaceutical chemicals and endocrine disrupters in municipal wastewater in Tokyo and their removal during activated sludge treatment. Water Research 2006, 40:3297-3303.
58. Newman M.C., Unger M.A. Fundamentals of Ecotoxicology 2003, Lewis Publishers, United States of America, p. 458. second ed.
59. Nikolau A., Meric S., Fatta D. Occurrence patterns of pharmaceuticals in water and wastewater environments. Analytical and Bioanalytical Chemistry 2007, 387:1225-1234.
60. Olive O.P. DNA precipitation assay: a rapid and simple method for detecting DNA damage in mammalian cells. Environmental and Molecular Mutagenesis 1988, 11:487-495.
61. Palo A.K., Choudhury R.C. Modulation of methotrexate-induced cytogenotoxicity in mouse spermatogonia and its transmission in the male germline by caffeine. Environmental Toxicology and Pharmacology 2006, 21:254-259.
62. Pomati F., Castiglioni S., Zucatto E., Fanelli R., Evigetti D., Rossetti C., Calamari D. Effects of a complex mixture of therapeutic drugs at environmental levels on human embryonic cells. Environmental Science & Technology 2006, 40:2442-2447.
63. Quinn B., Gagné F., Blaise C. Oxidative metabolism activity in Hydra attenuata exposed to carbamazepine. Fresenius Environmental Bulletin 2004, 13(8):783-788.
64. Quinn B., Gagné F., Blaise C. The effects of pharmaceuticals on the regeneration of the cnidarian, Hydra attenuata. Science of the Total Environment 2008, 402:62-69.
65. Quinn B., Gagné F., Blaise C. An investigation into the acute and chronic toxicity of eleven pharmaceuticals (and their solvents) found in waste water effluent on the cnidarian, Hydra attenuata. Science of the Total Environment 2008, 389:306-314.
66. Ramšak A., Stopar K., Sepčić K., Berden-Zrimec M., Bajt O., Malej A. Reflection of hydrocarbon pollution on hepatic EROD activity in the black Goby (Gobius níger). Environmental Toxicology and Pharmacology 2007, 24:304-310.
67. Regoli F., Giuliani M.E., Benedetti M., Arukwe A. Molecular and biochemical biomarkers in environmental monitoring: a comparison of biotransformation and antioxidant defence systems in multiple tissues. Aquatic Toxicology 2011, 105(3-4 Suppl.):56-66.
68. Rewitz K.F., Styrishave B., Løbner-Olesen A., Andersen O. Marine invertebrate cytochrome P450: emerging insights from vertebrate and insect analogies. Comparative Biochemistry and Physiology Part C 2006, 143:363-381.
69. Ringwood A.H., Hoguet J., Keppler C.J., Gielazyn M.L., Ward B.P., Rourk A.R. Cellular Biomarkers (Lysosomal Destabilization, Glutathione and Lipid Peroxidation) in Three Common Estuarine Species: a Methods Handbook 2003, Marine Resources Research Institute, South Carolina Department of Natural Resources, USA, 46pp.
70. Roberts P.H., Thomas K.V. The occurrence of selected pharmaceuticals in wastewaters effluent and surface waters of lower Tyne catchment. Science of the Total Environment 2006, 356:143-153.
71. Santos J.L., Aparicio I., Alonso E., Callejón M. Simultaneous determination of pharmaceutically active compounds in waste water samples by solid phase extraction and high-performance liquid chromatography with diode array and fluorescence detectors. Analytica Chimica Acta 2005, 550:116-122.
72. Sedlak D.L., Gray J.L., Pinkston K.E. Understanding microcontaminants in recycled water. Environmental Science & Technology 2000, 34:508A-515A.
73. Seiler R.L., Zaugg S.D., Thomas J.M., Howcroft D.L. Caffeine and pharmaceuticals as indicators of waste water contamination in wells. Ground Water 2005, 37(3):405-410.
74. Snyder M.J. Cytochrome P450 enzymes in aquatic invertebrates: recent advances and future directions. Aquatic Toxicology 2000, 48:529-547.
75. Soares S.S., Martins H., Gutierrez-Merino C., Aureliano M. Vanadium and cadmium in vivo effects in teleost cardiac muscle: metal accumulation and oxidative stress markers. Comparative Biochemistry and Physiology C 2008, 147:168-178.
76. Söderhall K., Smith V.J. Separation of the haemocyte populations of Carcinus maenas and other marine decapods and prophenoloxidase distribution. Developmental and Comparative Immunology 1983, 7:229-239.
77. Ternes T., Hirsch R., Mueller J., Haberer K. Methods for the determination of neutral drugs as well as betablockers and alpha2-sympathomimetics in aqueous matrices using GC/MS and LC/MS/MS. Fresenius Journal of Analytical Chemistry 1998, 362(3):329-340.
78. Thibaut R., Porte C. Effects of fibrates, anti-inflammatory drugs antidepressants in the fish hepatoma cell line PHLC-1: cytotoxicity and interactions with cytochrome P450 1A. Toxicology in Vitro 2008, 22:1128-1135.
79. Thomas P.M., Foster G.D. Determination of nonsteroidal anti-inflammatory drugs, caffeine, and triclosan in wastewater by gas chromatography-mass spectrometry. Journal of Environmental Science and Health A 2004, 39(8):1969-1978.
80. Tixier C., Singer H.P., Ollers S., Muller S.R. Occurrence and fate of carbamazepine, clorifibric acid, diclofenac, ibuprofen, ketoprofen, and naproxen in surface waters. Environmental Science & Technology 2003, 37:1061-1068.
81. Van der Oost R., Beyer J., Vermeulen N.P.E. Fish bioaccumulation and biomarkers in environmental risk assessment. Environmental Toxicology and Pharmacology 2003, 13:57-149.
82. Viarengo A., Lowe D., Bolognesi C., Fabbri E., Koehler A. The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comparative Biochemistry and Physiology C 2007, 146:281-300.
83. Wedderburn J., Cheung V., Bamber S., Bloxham M., Depledge M.H. Biomarkers of biochemical and cellular stress in Carcinus maenas: an in situ field study. Marine Environmental Research 1998, 46(1-5):321-324.
84. Weigel S., Kuhlmann J., Hühnerfuss H. Drugs and personal care products as ubiquitous pollutants: occurrence and distribution of clofibric acid, caffeine and DEET in the North Sea. Science of the Total Environment 2002, 295:131-141.
85. Weigel S., Berguer U., Jensen E., Kallenborn R., Thorensen H., Hühnerfuss H. Determination of selected pharmaceuticals and caffeine in sewage and seawater from Tromsø/Norway with emphasis on ibuprofen and its metabolites. Chemosphere 2004, 56:583-592.
86. Weigel S., Aulinger A., Brockmeyer R., Harms H., Löffler J., Reincke H., Schmidt R., Stachel B., von Tümpling W., Wanke A. Pharmaceuticals in the river Elbe and its tributaries. Chemosphere 2004, 57:107-126.
87. Wills E.D. Evaluation of lipid peroxidation in lipids and biological membranes. Biochemical Toxicology: a Practical Approach 1987, 127-152. IRL Press, Oxford. K. Snell, B. Mullack (Eds.).
88. Winston G.W., Di Giulio R.T. Prooxidant and antioxidant mechanisms in aquatic organisms. Aquatic Toxicology 1991, 19:137-161.
89. Wright D.A., Welbourn P. Environmental toxicology. Cambridge Environmental Chemistry Series 2002, vol. 11. Cambridge University Press, United Kingdom, p. 630.
90. Yoon Y., Ryu J., Oh J., Choi B.G., Snyder S.A. Occurrence of endocrine disrupting compounds, pharmaceuticals, and personal care products in the Han River (Seoul, South Korea). Science of the Total Environment 2010, 408:636-643.
91. Zuccato E., Calamari D., Natangelo M., Fanelli R. Presence of therapeutic drugs in the environment. The Lancet 2000, 335:1789-1790.