Skip to main content
SpringerLink
Log in

Metals and Nonsteroidal Anti-inflammatory Pharmaceuticals Drugs Present in Water from Madín Reservoir (Mexico) Induce Oxidative Stress in Gill, Blood, and Muscle of Common Carp (Cyprinus carpio)

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Many toxic xenobiotics that enter the aquatic environment exert their effects through redox cycling. Oxidative stress, which incorporates both oxidative damage and antioxidant defenses, is a common effect induced in organisms exposed to xenobiotics in their environment. The results of the present study aimed to determine the oxidative stress induced in the common carp Cyprinus carpio by contaminants [metals and nonsteroidal anti-inflammatory drugs (NSAIDs)] present in Madín Reservoir. Five sampling stations (SSs), considered to have the most problems due to discharges, were selected. Carp were exposed to water from each SS for 96 h, and the following biomarkers were evaluated in gill, blood, and muscle: hydroperoxide content, lipid peroxidation, protein carbonyl content, and the activity of antioxidant enzymes superoxide dismutase and catalase. Results show that contaminants (metals and NSAIDs) present in water from the different SSs induce oxidative stress. Thus, water in this reservoir is contaminated with xenobiotics that are hazardous to C. carpio, a species consumed by the local human population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abdollahi M, Mostafalou S, Pournourmohammadi S, Shadnia S (2004) Oxidative stress and cholinesterase inhibition in saliva and plasma of rats following subchronic exposure to malathion. Comp Biochem Physiol C 137:29–34

    Google Scholar 

  • Ahmad I, Hamid T, Fatima M, Chand HS, Jain SK, Athar M et al (2000) Induction of hepatic antioxidants in freshwater catfish (Channa punctatus Bloch) is a biomarker of paper mill effluent exposure. Biochim Biophys Acta 1523:37–48

    Article  CAS  Google Scholar 

  • Amador FC, Santos MS, Oliveira CR (2001) Lipid peroxidation and aluminium effects on the cholinergic system in nerve terminals. Neurotoxicol Res 3:223–233

    Article  CAS  Google Scholar 

  • American Public Health Association, American Water Works Association, Water Pollution Control Federation (1995) Standard methods. Examination of water and wastewater, 19th edn. APHA, AWWA, WPCF, Washington, DC

    Google Scholar 

  • Anand RJK, Arabi M, Rana KS, Kanwar U (2000) Role of vitamin C and E with GSH in checking the peroxidative damage to human ejaculated spermatozoa. Int J Urol 7:S1–S98

    Article  Google Scholar 

  • Ankley GT, Burkhard LP (1992) Identification of surfactants as toxicants in a primary effluent. Environ Toxicol Chem 11:1235–1248

    Article  CAS  Google Scholar 

  • Asensio C, Levoin N, Guillaume C, Guerquin MJ, Rouguieg K, Chrétien F et al (2007) Irreversible inhibition of glucose-6-phosphate dehydrogenase by the coenzyme A conjugate of ketoprofen: a key to oxidative stress induced by non-steroidal anti-inflammatory drugs? Biochem Pharmacol 73:405–416

    Article  CAS  Google Scholar 

  • Bagnyukova TV, Chahrak OI, Lushchak VI (2006) Coordinated response of goldfish antioxidant defenses to environmental stress. Aquat Toxicol 78:325–331

    Article  CAS  Google Scholar 

  • Baillie TA (2006) Future of toxicology-metabolic activation and drug design: challenges and opportunities in chemical toxicology. Chem Res Toxicol 19:889–893

    Article  CAS  Google Scholar 

  • Büege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    Article  Google Scholar 

  • Burcham PC (2007) Modified protein carbonyl assay detects oxidised membrane proteins: a new tool for assessing drug- and chemically-induced oxidative cell injury. J Pharmacol Toxicol Metab 56:18–22

    Article  CAS  Google Scholar 

  • Cabiscol E, Tamarit J, Ros J (2000) Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3:3–8

    CAS  Google Scholar 

  • Coz A, Andrés A, Irabien A (2004) Ecotoxicity assessment of stabilized/solidified foundry sludge. Environ Sci Technol 38:1897–1900

    Article  CAS  Google Scholar 

  • Deng A, Himmelsbach M, Zhu QZ, Frey S, Sengl M, Buchberger W et al (2003) Residue analysis of the pharmaceutical diclofenac in different water types using ELISA and GC–MS. Environ Sci Technol 37:3422–3429

    Article  CAS  Google Scholar 

  • Doi H, Iwasaki H, Masubuchi Y, Nishigaki R, Horie T (2002) Chemiluminescence associated with the oxidative metabolism of salicylic acid in rat liver microsomes. Chem Biol Interact 140:109–119

    Article  CAS  Google Scholar 

  • Dua R, Gill KD (2001) Aluminium phosphide exposure: implications on rat brain lipid peroxidation and antioxidant defence system. Pharmacol Toxicol 89:315–319

    Article  CAS  Google Scholar 

  • Eaton P (2006) Protein thiol oxidation in health and disease: techniques for measuring disulfides and related modifications in complex protein mixtures. Free Radic Biol Med 40:1889–1899

    Article  CAS  Google Scholar 

  • Eaton DA, Clesceri LS, Greenberg AE (eds) (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association, Washington, DC, pp 8–90

    Google Scholar 

  • Fent K, Weston AA, Caminada D (2006) Ecotoxicology of human pharmaceuticals. Aquat Toxicol 76:122–159

    Article  CAS  Google Scholar 

  • Galar-Martínez M, Gómez-Oliván LM, Amaya Chávez A, Razo-Estrada C, García-Medina S (2010) Oxidative stress induced on Cyprinus carpio by contaminants present in the water and sediment of Madín Reservoir. J Environ Sci Health A 45(2):155–160

    Article  Google Scholar 

  • García-Medina S, Razo-Estrada AC, Gómez-Oliván LM, Amaya-Chávez A, Madrigal-Bujaidar E, Galar-Martínez M (2010) Aluminum-induced oxidative stress in lymphocytes of common carp (Cyprinus carpio). Fish Physiol Biochem 36:875–882

    Article  Google Scholar 

  • Glusczak L, Miron DS, Morales BS, Simões RR, Schetinger MR, Morsch VM et al (2007) Acute effects of glyphosate herbicide on metabolic and enzymatic parameters of silver catfish (Rhamdia quelen). Comp Biochem Physiol C 146:519–524

    Google Scholar 

  • Gómez-Olivan LM, Galar-Martínez M, Téllez LA, Carmona-Zepeda F, Amaya-Chávez A (2009) Estudio de automedicación en una farmacia comunitaria de la ciudad de Toluca. Rev Mex Cienc Farm 40(1):5–11

    Google Scholar 

  • Gómez-Oliván LM, 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 Pollut 223:5097–5104

    Article  Google Scholar 

  • Gómez-Oliván LM, Galar-Martínez M, García-Medina S, Valdés-Alanís A, Islas-Flores H, Neri-Cruz N (7 June 2014) Genotoxic response and oxidative stress induced by diclofenac, ibuprofen and naproxen in Daphnia magna. Drug Chem Toxicol. doi:10.3109/01480545.2013.870191

  • Graham GG, Williams KM (2004) Metabolism and pharmacokinetics of ibuprofen. In: Rainsford KD (ed) Aspirin and related drugs. Taylor and Francis, London, pp 157–180

    Google Scholar 

  • Grillo MP, Hua F, Knutson CG, Ware JA, 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. Chem Res Toxicol 16:1410–1417

    Article  CAS  Google Scholar 

  • Grune T (2000) Oxidative stress, aging and the proteasomal system. Biogerontology 1:31–40

    Article  CAS  Google Scholar 

  • Guecheva T, Henriques JA, Erdtmann B (2001) Genotoxic effects of copper sulphate in freshwater planarian in vivo, studied with the single-cell gel test (comet assay). Mutat Res 497:19–27

    Article  CAS  Google Scholar 

  • Halliwell B (2006) Oxidative stress and neurodegeneration: where are we now? J Neurochem 97:1634–1658

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (eds) (1999) Free radicals in biology and medicine, 3rd edn. Oxford University Press, Oxford

    Google Scholar 

  • Hoeger B, Köllner B, Dietrich DR, Hitzfeld B (2005) Water-borne diclofenac affects kidney and gill integrity and selected immune parameters in brown trout (Salmo trutta f. fario). Aquat Toxicol 5:53–64

    Article  Google Scholar 

  • Hofer R, Jeney Z, Bucher F (1995) Chronic effects of linear alkylbenzene sulfonate (LAS) and ammonia on rainbow trout (Oncorhynchus mykiss) fry at water criteria limits. Water Res 29:2725–2729

    Article  CAS  Google Scholar 

  • Huie RE, Padmaja S (1993) The reaction of NO with superoxide. Free Radic Res Commun 18:195–199

    Article  CAS  Google Scholar 

  • Islas-Flores H, Gómez-Oliván LM, 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). Ecotoxicol Environ Saf 9:32–38

    Article  Google Scholar 

  • Jaeschke H, Knight TR, Bajt ML (2003) The role of oxidant stress and reactive nitrogen species in acetaminophen hepatotoxicity. Toxicol Lett 144:279–288

    Article  CAS  Google Scholar 

  • Jiang ZY, Hunt JV, Wolff SP (1992) Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein. Anal Biochem 202:384–389

    Article  CAS  Google Scholar 

  • Jifa W, Zhiming Y, Xiuxian S, You W, Xihua C (2005) Comparative researches on effects of sodium dodecylbenzene sulfonate and sodium dodecyl sulfate upon Lateolabrax japonicus biomarker system. Environ Toxicol Pharmacol 20:465–470

    Article  Google Scholar 

  • Kiss T, Hollósi M (2001) The interaction of aluminium with peptides and proteins. In: Exley C (ed) Aluminium and Alzheimer’s disease: the science that describes the link. Elsevier, Amsterdam, pp 361–392

    Chapter  Google Scholar 

  • Lam MW, Young CJ, Brain RA, Johnson DJ, Hanson MA, Wilson CJ et al (2004) Aquatic persistence of eight pharmaceuticals in a microcosm study. Environ Toxicol Chem 23:1431–1440

    Article  CAS  Google Scholar 

  • Levine RL, Williams JA, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357

    Article  CAS  Google Scholar 

  • Li MH (2008) Effects of nonionic and ionic surfactants on survival, oxidative stress, and cholinesterase activity of planarian. Chemosphere 70:1796–1803

    Article  CAS  Google Scholar 

  • Livingstone DR (2003) Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Rev Med Vet 154:427–430

    CAS  Google Scholar 

  • Mehinto AC, Hill EM, Tyler CR (2010) Uptake and biological effects of environmentally relevant concentrations of the nonsteroidal anti-inflammatory pharmaceutical diclofenac in rainbow trout (Oncorhynchus mykiss). Environ Sci Technol 44:2176–2182

    Article  CAS  Google Scholar 

  • Miranda MA, Morera I, Vargas F, Gómez-Lechón MJ, Castell JV (1991) In vitro assessment of the phototoxicity of anti-inflammatory 2-arylpropionic acids. Toxicol In Vitro 5:451–455

    Article  CAS  Google Scholar 

  • Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175

    CAS  Google Scholar 

  • Monteiro DA, de Almeida JA, Rantin FT, Kalinin AL (2006) Oxidative stress biomarkers in the freshwater characid fish, Brycon cephalus, exposed to organophosphorus insecticide Folisuper 600 (methyl parathion). Comp Biochem Physiol C 143:141–149

    Article  Google Scholar 

  • Monteiro DA, Rantin FT, Kalinin AL (2010) Inorganic mercury exposure: toxicological effects, oxidative stress biomarkers and bioaccumulation in the tropical freshwater fish matrinxã, Brycon amazonicus (Spix and Agassiz 1829). Ecotoxicology 19:105–123

    Article  CAS  Google Scholar 

  • Norma Mexicana (NMX-AA-003-1980) Aguas residuales, muestreo. Procuraduría Federal de Protección al Ambiente. Diario Oficial de la Federación 25-03-1980

  • Norma Oficial Mexicana (NOM-001-ECOL-1996) Que establece los limites maximos permisibles de contaminantes en las descargas residuales en aguas y bienes nacionales. Procuraduría Federal de Protección al Ambiente. Diario Oficial de la Federación 06-01-1997

  • Norma Oficial Mexicana (NOM-002-ECOL-1996) Que establece los límites máximos permisibles de contaminantes en las descargas de aguas residuales a los sistemas de alcantarillado urbano o municipal. Procuraduría Federal de Protección al Ambiente. Diario Oficial de la Federación 03-06-1998

  • Norma Oficial Mexicana (NOM-127-SSA1-1994) Que establece salud ambiental, agua para uso y consumo humano límites permisibles de calidad y tratamientos a que debe someterse el agua para su potabilizacion. Procuraduría Federal de Protección al Ambiente. Diario Oficial de la Federación 16-11-1999

  • Oruç EO, Uner N (2002) Marker enzyme assessment in the liver of Cyprinus carpio (L.) exposed to 2,4-D and azinphosmethyl. J Biochem Mol Toxicol 16:182–188

    Article  Google Scholar 

  • Oviedo-Gómez DG, Galar-Martínez M, García-Medina S, Razo-Estrada C, Gómez-Oliván LM (2010) Diclofenac-enriched artificial sediment induces oxidative stress in Hyalella azteca. Environ Toxicol Pharmacol 29:39–43

    Article  Google Scholar 

  • Pantke U, Volk T, Schmutzler M, Kox WJ, Sitte N, Grune T (1999) Oxidized proteins as a marker of oxidative stress during coronary heart surgery. Free Radic Biol Med 27:1080–1086

    Article  CAS  Google Scholar 

  • Parvez S, Raisuddin S (2005) Protein carbonyls: novel biomarkers of exposure to oxidative stress-inducing pesticides in freshwater fish Channa punctata (Bloch). Environ Toxicol Pharmacol 20:112–117

    Article  CAS  Google Scholar 

  • Paul-Clark MJ, Van Cao T, Moradi-Bidhendi N, Cooper D, Gilroy DW (2004) 15-Epi-lipoxin A4-mediated induction of nitric oxide explains how aspirin inhibits acute inflammation. J Exp Med 200:69–78

    Article  CAS  Google Scholar 

  • Radi R, Turrens JF, Chang LY, Bush KM, Crapo JD, Freeman BA (1991) Detection of catalase in rat heart mitochondria. J Biol Chem 266:22028–22034

    CAS  Google Scholar 

  • Requena JR, Levine RL, Stadtman ER (2003) Recent advances in the analysis of oxidized proteins. Amino Acids 25:221–226

    Article  CAS  Google Scholar 

  • Salgueiro-Pagadigorria CL, Kelmer-Bracht AM, Bracht A, Ishii-Iwamoto EL (2004) Naproxen affects Ca(2+) fluxes in mitochondria, microsomes and plasma membrane vesicles. Chem Biol Interact 147:49–63

    Article  CAS  Google Scholar 

  • Schwaiger J, Ferling H, Mallow U, Wintermayr H, Negele RD (2004) Toxic effects of the non-steroidal anti-inflammatory drug diclofenac. Part I: histopathological alterations and bioaccumulation in rainbow trout. Aquat Toxicol 68:141–150

    Article  CAS  Google Scholar 

  • Slaninova A, Smutna M, Modra H, Svobodova Z (2009) A review: oxidative stress in fish induced by pesticides. Neuroendocrinol Lett 30:2–12

    CAS  Google Scholar 

  • Stadtman ER, Oliver CN (1991) Metal-catalyzed oxidation of proteins. Physiological consequences. J Biol Chem 266:2005–2008

    CAS  Google Scholar 

  • Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336

    Article  CAS  Google Scholar 

  • Stülten D, Zühlke S, Lamshöft M, Spiteller M (2008) Occurrence of diclofenac and selected metabolites in sewage effluents. Sci Total Environ 405:310–316

    Article  Google Scholar 

  • Uner N, Oruç EÖ, Sevgiler Y, Sahin N, Durmaz H, Usta D (2006) Effects of diazinon on acetylcholinesterase activity and lipid peroxidation in the brain of Oreochromis niloticus. Environ Toxicol Pharmacol 21:241–245

    Article  Google Scholar 

  • Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf 64:178–189

    Article  CAS  Google Scholar 

  • Valko M, Morris H, Cronin MT (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208

    Article  CAS  Google Scholar 

  • van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

    Article  Google Scholar 

  • Vlahogianni T, Dassenakis M, Scoullos MJ, 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. Mar Pollut Bull 54:1361–1371

    Article  CAS  Google Scholar 

  • Vree TB, van den Biggelaar-Martea M, Verwey-van Wissen CP (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. J Chromatogr 578:239–249

    Article  CAS  Google Scholar 

  • Wilhelm EA, Jesse CR, Leite MR, Nogueira CW (2009) Studies on preventive effects of diphenyl diselenide on acetaminophen-induced hepatotoxicity in rats. Pathophysiology 16:31–37

    Article  CAS  Google Scholar 

  • Wilhelm Filho D (1996) Fish antioxidant defenses—a comparative approach. Braz J Med Biol Res 29:1735–1742

    CAS  Google Scholar 

  • Wilhelm Filho D, Torres MA, Zaniboni-Filho E, Pedrosa RC (2005) Effect of different oxygen tensions on weight gain, feed conversion, and antioxidant status in piapara, Leporinus elongatus (Valenciennes 1847). Aquaculture 244:349–357

    Article  Google Scholar 

  • Winston GW, Di Giulio RT (1991) Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat Toxicol 19:137–161

    Article  CAS  Google Scholar 

  • Winzer K, Becker W, Van Noorden CJ, Köhler A (2000) Short-time induction of oxidative stress in hepatocytes of the European flounder (Platichthys flesus). Mar Environ Res 50:495–501

    Article  CAS  Google Scholar 

  • Yamanaka H, Sogabe A, Handoh IC, Kawabata Z (2011) The effectiveness of clove oil as an anaesthetic on adult common carp, Cyprinus carpio L. J Anim Vet Adv 10:210–213

    Article  Google Scholar 

  • Yokel RA (2000) The toxicology of aluminum in the brain: a review. Neurotoxicology 21:813–828

    CAS  Google Scholar 

  • Yousef MI (2004) Aluminium-induced changes in hemato-biochemical parameters, lipid peroxidation and enzyme activities of male rabbits: protective role of ascorbic acid. Toxicology 199:47–57

    Article  CAS  Google Scholar 

  • Zwiener C, Seeger S, Glauner T, Frimmel FH (2002) Metabolites from the biodegradation of pharmaceutical residues of ibuprofen in biofilm reactors and batch experiments. Anal Bioanal Chem 372:569–575

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was made possible by support from the Consejo Nacional de Ciencia y Tecnología (CONACyT-Mexico, Project 151665) and (CONACyT-Mexico, Project 181541).

Author information

Authors and Affiliations

  1. Laboratorio de Toxicología Ambiental, Departamento de Farmacia, Facultad de Química, Universidad Autónoma del Estado de México, Paseo Colón intersección Paseo Tollocan s/n. Col. Residencial Colón, 50120, Toluca, Estado de México, Mexico

    Edgar David González-González, Leobardo Manuel Gómez-Oliván & Hariz Islas-Flores

  2. Laboratorio de Toxicología Acuática, Departamento de Farmacia, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Ciudad de México, DF, Mexico

    Marcela Galar-Martínez, Sandra García-Medina, Celene Razo-Estrada & Ricardo Pérez-Pastén

  3. Laboratorio de Neurofisiología de la Conducta, Facultad de Medicina, Universidad Autónoma del Estado de México, Toluca, Estado de México, Mexico

    Patricia Vieyra-Reyes

  4. Unidad de Farmacología Clínica, Facultad de Medicina, Universidad Nacional Autónoma de México, Ciudad de México, DF, Mexico

    Juan Manuel Jiménez-Vargas

Authors
  1. Edgar David González-González
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leobardo Manuel Gómez-Oliván
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marcela Galar-Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patricia Vieyra-Reyes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hariz Islas-Flores
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sandra García-Medina
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Juan Manuel Jiménez-Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Celene Razo-Estrada
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ricardo Pérez-Pastén
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Leobardo Manuel Gómez-Oliván.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González-González, E.D., Gómez-Oliván, L.M., Galar-Martínez, M. et al. Metals and Nonsteroidal Anti-inflammatory Pharmaceuticals Drugs Present in Water from Madín Reservoir (Mexico) Induce Oxidative Stress in Gill, Blood, and Muscle of Common Carp (Cyprinus carpio). Arch Environ Contam Toxicol 67, 281–295 (2014). https://doi.org/10.1007/s00244-014-0048-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-014-0048-0

Keywords

Search

Navigation