Effluent from an NSAID-manufacturing plant in Mexico induces oxidative stress on Cyprinus Carpio

Water, Air, and Soil Pollution

Volumn 224, Issue 9, 2013, Pages

  Sanjuan Reyes, Nely ^a   Gómez Oliván, Leobardo Manuel ^a   Galar Martínez, Marcela ^b   Vieyra Reyes, Patricia ^a   García Medina, Sandra ^b   Islas Flores, Hariz ^a   Neri Cruz, Nadia ^a  

^a UNIVERSIDAD AUTÓNOMA DEL ESTADO DE MÉXICO   (Mexico)

^b INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

Author keywords

Cyprinus carpio; Nonsteroidal anti inflammatory; Oxidative stress

Indexed keywords

BIOMARKERS; BRAIN; CONTROLLED DRUG DELIVERY; DRUG PRODUCTS; ENZYMES; OXIDATIVE STRESS; SEWAGE; SOAPS (DETERGENTS);

ANTI-INFLAMMATORIES; CYPRINUS CARPIO; GLUTATHIONE PEROXIDASE; INDUSTRIAL ACTIVITIES; MEDIAN LETHAL CONCENTRATION; NON-STEROIDAL ANTI-INFLAMMATORY DRUGS; PHARMACEUTICAL PRODUCTS; PROTEIN CARBONYL CONTENT;

EFFLUENTS;

CARBONYL DERIVATIVE; CATALASE; GLUTATHIONE PEROXIDASE; HYDROPEROXIDE; NONSTEROID ANTIINFLAMMATORY AGENT; SUPEROXIDE DISMUTASE;

BIOMARKER; CHEMICAL POLLUTANT; CYPRINID; DRUG; EFFLUENT; INDUSTRIAL WASTE; MANUFACTURING; POLLUTION EFFECT;

ANIMAL TISSUE; ARTICLE; BLOOD ANALYSIS; BRAIN TISSUE; CARP; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG INDUSTRY; EFFLUENT; ENZYME ACTIVITY; GILL; LIPID PEROXIDATION; LIVER PARENCHYMA; MEXICO; NONHUMAN; OXIDATIVE STRESS; WASTE WATER;

MEXICO [NORTH AMERICA];

CYPRINIDAE; CYPRINUS CARPIO;

EID: 84884214611     PISSN: 00496979     EISSN: 15732932     Source Type: Journal    
DOI: 10.1007/s11270-013-1689-8     Document Type: Article

References (90)

1. Ajmone-Cat, M. A., Bernardo, A., Greco, A., & Minghetti, L. (2010). Non-steroidal anti-inflammatory drugs and brain inflammation: effects on microglial functions. Pharmaceuticals, 3(6), 1949-1965.
2. Ashton, D., Hilton, M., & Thomas, K. V. (2004). Investigating the environmental transport of human pharmaceuticals to streams in the United Kingdom. Science of the Total Environment, 333(1), 167-184.
3. Azzi, A., Davies, K. J., & Kelly, F. (2004). Free radical biology-terminology and critical thinking. FEBS Letters, 558(1), 3-6.
4. Baillie, T. A. (2006). Future of toxicology metabolic activation and drug design: challenges and opportunities in chemical toxicology. Chemical Research in Toxicology, 19(7), 889-893.
5. 2 processes. Chemosphere, 50(1), 85-95.
6. Barata, C., Varo, I., Navarro, J. C., Arun, S., & Porte, C. (2005). Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds. Comparative Biochemistry and Physiology, Part C: Toxicology & Pharmacology, 140(2), 175-186.
7. Bebianno, M. J., Serafim, A., Camus, L., Cosson, R. P., & Fiala-Médoni, A. (2005). Antioxidant systems and lipid peroxidation in Bathymodiolus azoricus from Mid-Atlantic Ridge hydrothermal vent fields. Aquatic Toxicology, 75(4), 354-373.
8. Bedner, M., & MacCrehan, W. A. (2006). Transformation of acetaminophen by chlorination produces the toxicants 1, 4-benzoquinone and N-acetyl-p-benzoquinone imine. Environmental Science & Technology, 40(2), 516-522.
9. Bilotta, J., Barnett, J. A., Hancock, L., & Saszik, S. (2004). Ethanol exposure alters zebrafish development: a novel model of fetal alcohol syndrome. Neurotoxicology and Teratology, 26(6), 737-743.
10. Blanco, G., Martínez, C., García-Martín, E., & Agúndez, J. A. (2005). Cytochrome P450 gene polymorphisms and variability in response to NSAIDs. Clinical Research and Regulatory Affairs, 22(2), 57-81.
11. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1), 248-254.
12. Bruner, S. D., Norman, D. P., & Verdine, G. L. (2000). Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA. Nature, 403(6772), 859-866.
13. Büege, J. A., & Aust, S. D. (1978). Microsomal lipid peroxidation. Methods in Enzymology, 52, 302-310.
14. Burcham, P. C. (2007). Modified protein carbonyl assay detects oxidised membrane proteins: a new tool for assessing drug- and chemically-induced oxidative cell injury. Journal of Pharmacological and Toxicological Methods, 56(1), 18-22.
15. Cabiscol, E., Tamarit, J., & Ros, J. (2010). Oxidative stress in bacteria and protein damage by reactive oxygen species. International Microbiology, 3(1), 3-8.
16. Carlsson, G., Örn, S., & Larsson, D. G. (2010). Effluent from bulk drug production is toxic to aquatic vertebrates. Environmental Toxicology and Chemistry, 28(12), 2656-2662.
17. Cengiz, E. I., & Unlu, E. (2006). Sublethal effects of commercial deltamethrin on the structure of the gill, liver and gut tissues of mosquitofish, Gambusia affinis: a microscopic study. Environmental Toxicology and Pharmacology, 21(3), 246-253.
18. Comeau, F., Surette, C., Brun, G. L., & Losier, R. (2008). The occurrence of acidic drugs and caffeine in sewage effluents and receiving waters from three coastal watersheds in Atlantic Canada. Science of the Total Environment, 396(2), 132-146.
19. Correa, M., Arizzi, M. N., Betz, A., Mingote, S., & Salamone, J. D. (2003). Open field locomotor effects in rats after intraventricular injections of ethanol and the ethanol metabolites acetaldehyde and acetate. Brain Research Bulletin, 62(3), 197-202.
20. Cserhati, T., Forgács, E., & Oros, G. (2002). Biological activity and environmental impact of anionic surfactants. Environment International, 28(5), 337-348.
21. Dalzell, D. J. B., & Macfarlane, N. A. A. (1999). The toxicity of iron to brown trout and effects on the gills: a comparison of two grades of iron sulphate. Journal of Fish Biology, 55(2), 301-315.
22. Deng, A., Himmelsbach, M., Zhu, Q. Z., Frey, S., Sengl, M., Buchberger, W., et al. (2003). Residue analysis of the pharmaceutical diclofenac in different water types using ELISA and GC-MS. Environmental Science & Technology, 37(15), 3422-3429.
23. Doi, H., Iwasaki, H., Masubuchi, Y., Nishigaki, R., & Horie, T. (2002). Chemiluminescence associated with the oxidative metabolism of salicylic acid in rat liver microsomes. Chemico-Biological Interactions, 140(2), 109-119.
24. Eaton, P. (2006). Protein thiol oxidation in health and disease: techniques for measuring disulfides and related modifications in complex protein mixtures. Free Radical Biology and Medicine, 40(11), 1889-1899.
25. Evans, D. H., Piermarini, P. M., & Choe, K. P. (2005). The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiological Reviews, 85(1), 97-177.
26. Fent, K., Weston, A. A., & Caminada, D. (2006). Ecotoxicology of human pharmaceuticals. Aquatic Toxicology, 76(2), 122-159.
27. Firth, C. A., Yang, Y. T., & Gieseg, S. P. (2007). Lipid oxidation predominates over protein hydroperoxide formation in human monocyte-derived macrophages exposed to aqueous peroxyl radicals. Free Radical Research, 41(7), 839-848.
28. Gagné, F., Blaise, C., & André, C. (2006). Occurrence of pharmaceutical products in a municipal effluent and toxicity to rainbow trout (Oncorhynchus mykiss) hepatocytes. Ecotoxicology and Environmental Safety, 64(3), 329-336.
29. Glusczak, L., Miron, D. D. S., Moraes, B. S., Simões, R. R., Schetinger, M. R. C., Morsch, V. M., et al. (2007). Acute effects of glyphosate herbicide on metabolic and enzymatic parameters of silver catfish (Rhamdia quelen). Comparative Biochemistry and Physiology, Part C: Toxicology & Pharmacology, 146(4), 519-524.
30. Gómez-Oliván, L., Carmona-Zepeda, F., Galar- Martínez, M., Téllez-López, A., & Amaya-Chávez, A. (2009). Estudio de automedicación en una farmacia comunitaria de la ciudad de Toluca. Revista Mexicana de Ciencias Farmacéuticas, 40(1), 5-11.
31. Gómez-Oliván, L. M., Neri-Cruz, N., Galar-Martínez, M., Vieyra-Reyes, P., García-Medina, S., Razo-Estrada, C., et al. (2012). Assessing the oxidative stress induced by paracetamol spiked in artificial sediment on Hyalella azteca. Water, Air, & Soil Pollution, 223(1), 5097-5104.
32. Gonzalez-Rey, M., & Bebianno, M. J. (2011). Non-steroidal anti-inflammatory drug (NSAID) ibuprofen distresses antioxidant defense system in mussel Mytilus galloprovincialis gills. Aquatic Toxicology, 105(3), 264-269.
33. Graham, G. G., & Williams, K. M. (2004). Metabolism and pharmacokinetics of ibuprofen. Aspirin and Related Drugs, 195.
34. Grillo, M. P., Hua, F., Knutson, C. G., Joseph, A., & Li, C. (2003). Mechanistic studies on the bioactivation of diclofenac: identification of diclofenac-S-acyl-glutathione in vitro in incubations with rat and human hepatocytes. Chemical Research in Toxicology, 16(11), 1410-1417.
35. Gunzler, W., & Flohe-Clairborne, A. (1985). Glutathione peroxidase. In R. A. Green-Wald (Ed.), Handbook of methods for oxygen radical research (pp. 285-290). Boca Raton: CRC Press.
36. Halliwell, B. (1997). Antioxidants and human disease: a general introduction. Nutrition Reviews, 55(1), S44-S49.
37. Halliwell, B. (2006). Oxidative stress and neurodegeneration: where are we now? Journal of Neurochemistry, 97(6), 1634-1658.
38. Halliwell, B., & Gutteridge, J. M. C. (1999). Free radicals in biology and medicine. Oxford: Oxford University Press.
39. Hoeger, B., Köllner, B., Dietrich, D. R., & Hitzfeld, B. (2005). Water-borne diclofenac affects kidney and gill integrity and selected immune parameters in brown trout (Salmo trutta f. fario). Aquatic Toxicology, 75(1), 53-64.
40. Islas-Flores, H., Gómez-Oliván, L. M., 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). Ecotoxicology and Environmental Safety. doi: 10.1016/j.ecoenv.2013.01.025.
41. Jiang, Z. Y., Hunt, J. V., & Wolff, S. P. (1992). Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein. Analytical Biochemistry, 202(2), 384-389.
42. Jifa, W., Yu, Z., Xiuxian, S., & You, W. (2006). Response of integrated biomarkers of fish (Lateolabrax japonicus) exposed to benzo [a] pyrene and sodium dodecylbenzene sulfonate. Ecotoxicology and Environmental Safety, 65(2), 230-236.
43. Karan, V., Vitorović, S., Tutundžić, V., & Poleksić, V. (1998). Functional enzymes activity and gill histology of carp after copper sulfate exposure and recovery. Ecotoxicology and Environmental Safety, 40(1), 49-55.
44. Lam, M. W., Young, C. J., Brain, R. A., Johnson, D. J., Hanson, M. A., Wilson, C. J., et al. (2009). Aquatic persistence of eight pharmaceuticals in a microcosm study. Environmental Toxicology and Chemistry, 23(6), 1431-1440.
45. Levine, R. L., Williams, J. A., Stadtman, E. R., & Shacter, E. (1994). Carbonyl assays for determination of oxidatively modified proteins. Methods in Enzymology, 233, 346-357.
46. Livingstone, D. R. (2003). Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Revue de Médecine Vétérinaire, Toulouse, 154(6), 427-430.
47. Lushchak, V. I. (2011). Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicology, 101(1), 13-30.
48. Mehinto, A. C., Hill, E. M., & Tyler, C. R. (2010). Uptake and biological effects of environmentally relevant concentrations of the nonsteroidal anti-inflammatory pharmaceutical diclofenac in rainbow trout (Oncorhynchus mykiss). Environmental Science & Technology, 44(6), 2176-2182.
49. Miller, H., Prasad, R., Wilson, S. H., Johnson, F., & Grollman, A. P. (2000). 8-oxodGTP incorporation by DNA polymerase beta is modified by active-site residue Asn279. Biochemistry, 39, 1029-1033.
50. Miranda, M. A., Morera, I., Vargas, F., Gómez-Lechón, M. J., & Castell, J. V. (1991). In vitro assessment of the phototoxicity of anti-inflammatory 2-arylpropionic acids. Toxicology in Vitro, 5(5), 451-455.
51. Misra, H. P., & Fridovich, I. (1972). The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Journal of Biological Chemistry, 247(10), 3170-3175.
52. Montague, P. (2006). Drugs in the water. Rachel's Environmental Health Weekly, 614(1), 15-22.
53. Mycek, M. J., Harvey, R. A., & Champe, P. C. (2004). Farmacología. Mexico, DF: McGraw-Hill.
54. Negre-Salvayre, A., Auge, N., Ayala, V., Basaga, H., Boada, J., Brenke, R., et al. (2010). Pathological aspects of lipid peroxidation. Free Radical Research, 44(10), 1125-1171.
55. Nunes, B., Gaio, A. R., Carvalho, F., & Guilhermino, L. (2008). Behaviour and biomarkers of oxidative stress in Gambusia holbrooki after acute exposure to widely used pharmaceuticals and a detergent. Ecotoxicology and Environmental Safety, 71(2), 341-354.
56. Oviedo-Gómez, D. G. C., Galar-Martínez, M., García-Medina, S., Razo-Estrada, C., & Gómez-Oliván, L. M. (2010). Diclofenac-enriched artificial sediment induces oxidative stress in Hyalella azteca. Environmental Toxicology and Pharmacology, 29(1), 39-43.
57. Parvez, S., & Raisuddin, S. (2005). Protein carbonyls: novel biomarkers of exposure to oxidative stress-inducing pesticides in freshwater fish Channa punctata (Bloch). Environmental Toxicology and Pharmacology, 20(1), 112-117.
58. Radi, R., Turrens, J. F., Chang, L. Y., Bush, K. M., Crapo, J. D., & Freeman, B. A. (1991). Detection of catalase in rat heart mitochondria. Journal of Biological Chemistry, 266(32), 22028-22034.
59. Reed, D. J. (1995). Toxicity of oxygen. In F. DeMatters & L. L. Smith (Eds.), Molecular and cellular mechanisms of toxicity (pp. 35-68). Boca Raton: CRC Press.
60. Richardson, S. D. (2009). Water analysis: emerging contaminants and current issues. Analytical Chemistry, 81(12), 4645-4677.
61. Ruas, C. B. G., Carvalho, C. D. S., de Araújo, H. S. S., Espíndola, E. L. G., & Fernandes, M. N. (2008). Oxidative stress biomarkers of exposure in the blood of cichlid species from a metal-contaminated river. Ecotoxicology and Environmental Safety, 71(1), 86-93.
62. Sali, T. (2005). Prostaglandins. In H. W. Vohr (Ed.), Encyclopedic reference of immunotoxicology (pp. 537-540). Heidelberg: Springer.
63. Santos, L. H., Araújo, A. N., Fachini, A., Pena, A., Delerue-Matos, C., & Montenegro, M. C. B. S. M. (2010). Ecotoxicological aspects related to the presence of pharmaceuticals in the aquatic environment. Journal of Hazardous Materials, 175(1), 45-95.
64. Sarasquete, C., & Segner, H. (2000). Cytochrome P4501A (CYP1A) in teleostean fishes. A review of immunohistochemical studies. Science of the Total Environment, 247(2), 313-332.
65. Schwaiger, J., Ferling, H., Mallow, U., Wintermayr, H., & Negele, R. D. (2004). Toxic effects of the non-steroidal anti-inflammatory drug diclofenac: Part I: histopathological alterations and bioaccumulation in rainbow trout. Aquatic Toxicology, 68(2), 141-150.
66. Sevcikova, M., Modra, H., Slaninova, A., & Svobodova, Z. (2011). Metals as a cause of oxidative stress in fish: a review. Veterinary Medicine, 56, 537-546.
67. 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 Research, 42(8), 2124-2134.
68. Sirisattha, S., Momose, Y., Kitagawa, E., & Iwahashi, H. (2004). Toxicity of anionic detergents determined by Saccharomyces cerevisiae microarray analysis. Water Research, 38(1), 61-70.
69. Stegeman, J. J., & Livingstone, D. R. (1998). Forms and functions of cytochrome P450. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology & Endocrinology, 121, 1-3.
70. Stephensen, E., Svavarsson, J., Sturve, J., Ericson, G., Adolfsson-Erici, M., & Förlin, L. (2000). Biochemical indicators of pollution exposure in shorthorn sculpin (Myoxocephalus scorpius), caught in four harbours on the southwest coast of Iceland. Aquatic Toxicology, 48(4), 431-442.
71. Stülten, D., Zühlke, S., Lamshöft, M., & Spiteller, M. (2008). Occurrence of diclofenac and selected metabolites in sewage effluents. Science of the Total Environment, 405(1), 310-316.
72. Sui, Q., Huang, J., Deng, S., Yu, G., & Fan, Q. (2010). Occurrence and removal of pharmaceuticals, caffeine and DEET in wastewater treatment plants of Beijing, China. Water Research, 44(2), 417-426.
73. Tauxe-Wuersch, A., De Alencastro, L. F., Grandjean, D., & Tarradellas, J. (2005). Occurrence of several acidic drugs in sewage treatment plants in Switzerland and risk assessment. Water Research, 39(9), 1761-1772.
74. Ternes, T. A., Joss, A., & Siegrist, H. (2004). Peer reviewed: scrutinizing pharmaceuticals and personal care products in wastewater treatment. Environmental Science & Technology, 38(20), 392A-399A.
75. Tixier, C., Singer, H. P., Oellers, S., & Müller, S. R. (2003). Occurrence and fate of carbamazepine, clofibric acid, diclofenac, ibuprofen, ketoprofen, and naproxen in surface waters. Environmental Science & Technology, 37(6), 1061-1068.
76. Valavanidis, A., Vlahogianni, T., Dassenakis, M., & Scoullos, M. (2006). Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicology and Environmental Safety, 64(2), 178-189.
77. Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T., Mazur, M., & Telser, J. (2007). Free radicals and antioxidants in normal physiological functions and human disease. International Journal of Biochemistry and Cell Biology, 39(1), 44-84.
78. Van der Oost, R., Beyer, J., & Vermeulen, N. P. (2003). Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology, 13(2), 57-149.
79. Vlahogianni, T., Dassenakis, M., Scoullos, M. J., & Valavanidis, A. (2007). Integrated use of biomarkers (superoxide dismutase, catalase and lipid peroxidation) in mussels Mytilus galloprovincialis for assessing heavy metals' pollution in coastal areas from the Saronikos Gulf of Greece. Marine Pollution Bulletin, 54(9), 1361-1371.
80. Vree, T. B., Van Den Biggelaar-Martea, M., & Verwey-van Wissen, C. P. W. G. M. (1992). Determination of naproxen and its metabolite O-desmethylnaproxen with their acyl glucuronides in human plasma and urine by means of direct gradient high-performance liquid chromatography. Journal of Chromatography B: Biomedical Sciences and Applications, 578(2), 239-249.
81. Wilhelm Filho, D., Torres, M. A., Zaniboni-Filho, E., & Pedrosa, R. C. (2005). Effect of different oxygen tensions on weight gain, feed conversion, and antioxidant status in piapara, Leporinus elongates (Valenciennes, 1847). Aquaculture, 244(1), 349-357.
82. Wilhelm, E. A., Jesse, C. R., Leite, M. R., & Nogueira, C. W. (2009). Studies on preventive effects of diphenyl diselenide on acetaminophen-induced hepatotoxicity in rats. Pathophysiology, 16(1), 31-37.
83. Wu, D., & Cederbaum, A. I. (2005). Oxidative stress mediated toxicity exerted by ethanol-inducible CYP2E1. Toxicology and Applied Pharmacology, 207(2), 70-76.
84. Wu, M., Chaudhary, A., Khan, I. A., & Dasmahapatra, A. K. (2008). Ethanol teratogenesis in Japanese medaka: effects at the cellular level. Comparative Biochemistry and Physiology Part B, Biochemistry & Molecular Biology, 149(1), 191-201.
85. Yamanaka, H., Sogabe, A., Handoh, I. C., & Kawabata, Z. (2011). The effectiveness of clove oil as an anaesthetic on adult common carp, Cyprinus carpio L. Journal of Animal and Veterinary Advances, 10(2), 210-213.
86. 2 photocatalysis. Water Research, 42(13), 3480-3488.
87. Zanger, U. M., Turpeinen, M., Klein, K., & Schwab, M. (2008). Functional pharmacogenetics/genomics of human cytochromes P450 involved in drug biotransformation. Analytical and Bioanalytical Chemistry, 392(6), 1093-1108.
88. Zuccato, E., Calamari, M., Natangelo, R., & Fanelli, R. (2000). Presence of therapeutic drugs in the environment. Lancet, 355, 1789-1790.
89. Zuccato, E., Castiglioni, S., & Fanelli, R. (2005). Identification of the pharmaceuticals for human use contaminating the Italian aquatic environment. Journal of Hazardous Materials, 122(3), 205-209.
90. Zwiener, C., Seeger, S., Glauner, T., & Frimmel, F. (2002). Metabolites from the biodegradation of pharmaceutical residues of ibuprofen in biofilm reactors and batch experiments. Analytical and Bioanalytical Chemistry, 372(4), 569-575.