Abstract
The nonsteroidal anti-inflammatory naproxen sodium is among the most commonly used pharmaceuticals in Mexico. Nevertheless, there is no adequate regulation to control its sale, use, and disposal. This agent can enter water bodies by diverse pathways, attaining significant concentrations, especially in sediments since they are the final reservoir of many organic contaminants, and may induce damage on hydrobionts. Naproxen sodium is water-soluble, shows stability in aquatic ecosystems, and can form reactive products when oxidized. The aim of this study was to evaluate the oxidative stress and consequent damage to genetic material induced by naproxen sodium in sediments on Hyalella azteca. After 48 h of exposure to artificial sediments enriched with 76.6 and 339.2 mg kg−1 (equivalent to 1/10 of the LC50 and the NOAEL obtained in an earlier 48-h acute toxicity assay), the following biomarkers were evaluated: lipid peroxidation level, protein carbonyl content, activity of the antioxidant enzymes, and DNA damage. Results show that naproxen sodium induces oxidative stress (increased lipid and protein oxidation, as well as superoxide dismutase and catalase activity and decrease of glutathione peroxidase activity) and genotoxicity (increased oxidative damage of DNA) at sublethal concentrations on H. azteca, being the damage, concentration dependent.
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References
Boelsterli, U. A. (2007). Mechanistic toxicology: The molecular basis of how chemicals disrupt biological targets. Boca Raton: CRC Press.
Borgmann, U., Bennie, D. T., Ball, A. L., & Palabrica, V. (2007). Effect of a mixture of seven pharmaceuticals on Hyalella azteca over multiple generations. Chemosphere, 66, 1278–1283.
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, 248–254.
Büege, J. A., & Aust, S. D. (1978). Microsomal lipid peroxidation. Methods in Enzymology, 52, 302–310.
Chandran, R., Sivakumar, A. A., Mohandass, S., & Aruchami, M. (2005). Effect of cadmium and zinc on antioxidant enzyme activity in the gastropod Achatina fulica. Comparative Biochemistry and Physiology C Pharmacology Toxicology and Endocrinology, 140, 422–426.
Dobor, J., Varga, M., & Záray, G. (2012). Biofilm controlled sorption of selected acidic drugs on river sediments characterized by different organic carbon content. Chemosphere, 87, 105–110.
Fazio, F., Cecchini, S., Faggio, C., Caputo, A. R., & Piccione, G. (2014). Stability of oxidative stress biomarkers in flathead mullet, Mugil caphalus, serum during short-term storage. Ecological Indicators, 46, 188–192.
Fent, K., Weston, A. A., & Caminada, D. (2006). Ecotoxicology of human pharmaceuticals. Aquatic Toxicology, 76, 122–159.
Gagné, F., Blaise, C., & André, C. (2006). Ocurrence of pharmaceutical products in a municipal effluent and toxicity to rainbow trout (Oncorhynchus mykiss) hepatocytes. Ecotoxicology and Environmental Safety, 64, 329–336.
Galati, G., Tafazoli, S., Sabzevari, O., Chan, T. S., & O’Brien, P. J. (2002). Idiosyncratic NSAID drug induced oxidative stress. Chemico-Biological Interactions, 142, 25–41.
Gibson, R., Durán-Álvarez, J. C., León, E. K., Chávez, A., & Jiménez, C. B. (2010). Accumulation and leaching potential of some pharmaceuticals and potential endocrine disruptors in soils irrigated with wastewater in the Tula Valley, Mexico. Chemosphere, 81, 1437–1445.
Gilroy, A. M. E., Balakrishnan, K. V., Solomon, R. K., Sverko, E., & Sibley, K. P. (2012). Behaviour of pharmaceuticals in spiked lake sediments – Effects and interactions with benthic invertebrates. Chemosphere, 86, 578–584.
Gómez-Oliván, L. M., Galar-Martínez, M., Téllez, L. A. M., Carmona, Z. F. A., & Amaya-Chávez, A. (2009). Estudio de automedicación en una farmacia comunitaria de la ciudad de Toluca. Revista Mexicana de Ciencias Farmaceuticas, 40, 5–11.
Gómez-Oliván, L. M., Neri-Cruz, N., Galar-Martínez, M., Vieyra-Reyes, P., & García-Medina, S. (2012). Assessing the oxidative stress induced by paracetamol spiked in artificial sediment on Hyalella azteca. Water, Air, and Soil Pollution, 223(8), 5097–5104.
Hautaniemi, T., Petrenko, N., Skorinkin, A., & Giniatullin, R. (2012). The inhibitory action of the antimigraine nonsteroidal anti-inflammatory drug naproxen on P2X3 receptor-mediated responses in rat trigeminal neurons. Neuroscience, 209, 32–38.
Huang, D. J., Zhang, Y. M., Song, G., Long, J., Liu, J. H., & Ji, W. H. (2007). Contaminants-induced oxidative damage on the carp Cyprinus carpio collected from the Upper Yellow River, China. Environmental Monitoting and Assessment, 128, 483–488.
Huq, F. (2006). Molecular modeling analysis of the metabolism of naproxen. Journal of Pharmacology and Toxicology, 1, 346–353.
Isidori, M., Lavorgna, M., Nardelli, A., Parrella, A., Previtera, L., & Rubino, M. (2005). Ecotoxicity of naproxen and its phototransformation products. Science of the Total Environment, 348, 93–101.
Lal, N., Kumar, J., Erdhal, W. E., Pfeiffer, D. R., Gadd, M. E., Graff, G., & Yanni, J. M. (2009). Differential effects of non-steroidal anti-inflammatory drugs on mithocondrial dysfunction during oxidative stress. Archives of Biochemistry and Biophysics, 490, 1–8.
Lankoff, A., Banasik, A., Duma, A., Ochniak, E., Lisowska, H., Kuszewski, T., Gozdz, S., & Wojcik, A. (2006). A comet assay study reveals that aluminium induces DNA damage and inhibits the repair of radiation-induced lesions in human peripheral blood lymphocytes. Toxicology Letters, 161, 27–36.
Larsen, T. A., Lienert, J., Joss, A., & Siegrist, H. (2004). How to avoid pharmaceuticals in the environment. Journal of Biotechnology, 113, 295–304.
Legeay, A., Achard-Joris, M., Baudrimont, M., Massabuau, J., & Bourdineaud, J. (2005). Impact of cadmium contamination and oxygenation levels on biochemical responses in the Asiatic clam Corbicula fluminea. Aquatic Toxicology, 74, 242–253.
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.
Misra, P., & Fridovich, I. (1972). The role of superoxide anion in the autoxidation of epinephrine and simple assay for superoxide dismutase. The Journal of Biological Chemistry, 247, 3170–3175.
Oviedo-Gómez, D., Galar-Martínez, M., García-Medina, S., Razo-Estrada, C., & Gómez-Oliván, L. (2010). Diclofenac-enriched artificial sediment induces oxidative stress in Hyalella azteca. Environmental Toxicology and Pharmacology, 29, 39–43.
Paglia, D. E., & Valentine, W. N. (1967). Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. The Journal of Laboratory and Clinical Medicine, 70, 158–169.
Poplawski, T., Pawlowska, E., Wisniewska-Jarosinska, M., Ksiazek, D., Wozniak, K., Szczepanska, J., & Blasiak, J. (2009). Cytotoxicity and genotoxicity of glycidyl methacrylate. Chemico-Biological Interactions, 180, 69–78.
Quinn, B., Gagné, F., & Blaise, C. (2008). The effects of pharmaceuticals on the regeneration of the cnidarian Hydra attenuata. The Science of the Total Environment, 402, 62–69.
Radi, R., Turrens, J., Chang, Y., Bush, M., Capro, D., & Freeman, A. (1991). Detection of catalase in rat heart mitochondria. Journal of Biological Chemistry, 266(32), 20028–22034.
Salgueiro-Pagadigorria, C., Kelmer-Bracht, A., Bracht, A., & Ishii-Iwamoto, E. (2004). Naproxen affects Ca2+ fluxes in mitochondria, microsomes and plasma membrane vesicles. Chemico-Biological Interactions, 147, 49–63.
Santos, L. H. M. L. M., 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, 45–95.
Siemens, J., Huscheka, G., Siebeb, 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, 2124–2134.
Tice, R., Anderson, D., Burlinson, D., Hartmann, A., Kobayashi, H., Miyamae, Y., Rojas, E., Ryu, J. C., & Sasaki, Y. F. (2000). The single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environmental and Molecular Mutagenesis, 35, 206–221.
Tracy, T. S., Marra, C., Wrighton, S. A., Gonzalez, F. J., & Korzekwa, K. R. (1997). Involvement of multiple cytochrome P450 isoforms in naproxen O-demethylation. European Journal of Clinical Pharmacology, 52, 293–298.
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, 178–189.
Vlahogianni, T., Dassenakis, M., Scoullos, M., & Valavanidis, A. (2007). Integreated use of biomarkers (superoxide dismutase, catalase and lipid peroxidation) in mussels Mytilis galloprovincialis for assessing heavy metals pollution in coastal areas from the Saronikos Gulf of Greece. Marine Pollution Bulletin, 54, 1361–1371.
Xing, H., Li, S., Wang, Z., Gao, X., Xu, S., & Wang, X. (2012a). Oxidative stress response and histopathological changes due to atrazine and chlorpyrifos exposure in common carp. Pesticide Biochemistry and Physiology, 103, 74–80.
Xing, H., Li, S., Wang, Z., Gao, X., Xu, S., & Wang, X. (2012b). Histopathological changes and antioxidant response in brain and kidney of common carp exposed to atrazine and chlorpyrifos. Chemosphere, 88, 377–383.
Acknowledgments
This study was made possible through support provided by the Research and Postgraduate Division of the National Polytechnic Institute (Secretaría de Investigación y Posgrado del Instituto Politécnico Nacional; SIP-IPN, Project 20080526), Mexico.
Conflict of Interests
The authors state that the results contained in this document do not present any conflict of interest.
Ethical Approval
All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures performed were in accordance with the ethical standards of the institution at which the studies were conducted.
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Lucero, GM.A., Marcela, GM., Sandra, GM. et al. Naproxen-Enriched Artificial Sediment Induces Oxidative Stress and Genotoxicity in Hyalella azteca . Water Air Soil Pollut 226, 195 (2015). https://doi.org/10.1007/s11270-015-2454-y
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DOI: https://doi.org/10.1007/s11270-015-2454-y