Skip to main content
Log in

Oxidative stress in Cyprinus carpio induced by hospital wastewater in Mexico

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

The very wide range of activities performed in hospitals (care, diagnosis, hygiene, maintenance, research) require the use of a large variety of potentially ecotoxic substances such as surfactants, metals, disinfectants and pharmaceuticals. This study aimed to determine oxidative stress in the common carp Cyprinus carpio induced by hospital wastewater (HWW) in Mexico. The median lethal concentration (LC50) and subsequently the lowest observed adverse effect level were determined. Carp were exposed to the latter value (0.5 %) for 24, 48, 72 and 96 h, and the following biomarkers were evaluated in gill, brain, liver and blood: hydroperoxide content (HPC), malondialdehyde (MDA) content, protein carbonyl content (PCC) and activity of the antioxidant enzymes superoxide dismutase (SOD) and catalase (CAT). Significant increases in HPC, MDA content and PCC were observed in exposed specimens, particularly in gill, liver and brain. SOD and CAT activity also increased in liver and brain. In conclusion, this particular HWW induces oxidative stress on C. carpio, this damage being most evident in gill, liver and brain.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

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

  • Asensio C, Levoin N, Guillaume C, Guerquin MJ, Rouguieg K, Chrétien F, Chapleur Y, Netter P, Minn A, Lapicque F (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 

  • Baillie TA (2006) Future of toxicology—metabolic activation and drug design: challenges and opportunities in chemical toxicology. Chem Res Toxicol 19(7):889–893

    Article  CAS  Google Scholar 

  • Boillot C, Bazin C, Tissot-Guerraz F, Droguet J, Perraud M, Cetre JC, Trépo D, Perrodin Y (2008) Daily physicochemical, microbiological and ecotoxicological fluctuations of a hospital effluent according to technical and care activities. Sci Total Environ 403:113–129

    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 Methods 56:18–22

    Article  CAS  Google Scholar 

  • Cabiscol E, Tamarit J, Ros J (2010) Oxidative stress in bacteria and protein damage by reactive oxygen species. Intern Microbiol 3(1):3–8

    Google Scholar 

  • Comisión Nacional del Agua (CNA) (1995) Feasibility study for the sanitation of the Valley of Mexico. Final report. December 1995, Mexico

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

    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 

  • 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(11):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 

  • Emmanuel E, Keck G, Blanchard J-M, Vermande P, Perrodin Y (2004) Toxicological effects of disinfections using sodium hypochlorite on aquatic organisms and its contribution to AOX formation in hospital wastewater. Environ Int 30:891–900

    Article  CAS  Google Scholar 

  • Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr Top Med Chem 1:529–539

    Article  CAS  Google Scholar 

  • Ericson H, Thorsén G, Kumblad L (2010) Physiological effects of diclofenac, ibuprofen and propranolol on Baltic Sea blue mussels. Aquat Toxicol 99(2):223–231

    Article  CAS  Google Scholar 

  • Fent K, Weston AA, Caminada D (2006) Ecotoxicology of human pharmaceuticals. Aquat Toxicol 76(2):122–159

    Article  CAS  Google Scholar 

  • Gagné F, Blaise C, André C (2006) Occurrence of pharmaceutical products in a municipal effluent and toxicity to rainbow trout (Oncorhynchus mykiss) hepatocytes. Ecotoxicol Environ Saf 64(3):329–336

    Article  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 Part A 45(2):155–160

    Article  Google Scholar 

  • Gómez-Oliván 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, Dublán-García O, Corral-Avitia AY (2012) Assessing the oxidative stress induced by paracetamol spiked in artificial sediment on Hyalella azteca. Water Air Soil Pollut 223(1):5097–5104

    Article  Google Scholar 

  • Gómez-Oliván LM, Galar-Martínez M, Islas-Flores H, García-Medina S, SanJuan-Reyes N (2014) DNA damage and oxidative stress induced by acetylsalicylic acid in Daphnia magna. Comp Biochem Phys C 164:21–26

  • González Rey M, Bebianno MJ (2011) Nonsteroidal antiinflammatory drug (NSAID) ibuprofen distresses antioxidant defense system in mussel Mytilus galloprovincialis gills. Aquat Toxicol 105:264–269

    Article  Google Scholar 

  • Halliwell B (2006) Oxidative stress and neurodegeneration: where are we now? J Neurochem 97(6):1634–1658

    Article  CAS  Google Scholar 

  • Heckmann LH, Sibly RM, Timmermans MJ, Callaghan A (2008) Outlining eicosanoid biosynthesis in the crustacean Daphnia. Front Zool 5(11). doi:10.1186/1742-9994-5-11

  • Hermens J, Leeuwangh P (1982) Joint toxicity of mixtures of 8 and 24 chemicals to the guppy. Ecotoxicol Environ Saf 6:302–310

    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 

  • Islas-Flores H, Gómez-Oliván LM, Galar-Martínez M, García-Medina S, Neri-Cruz N, Dublán-García O (2014) Effect of ibuprofen exposure on blood, gill, liver, and brain on common carp (Cyprinus carpio) using oxidative stress biomarkers. Environ Sci Pollut Res 21(7):5157–5166

    Article  CAS  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 

  • Jiménez BC, Landa H (1998) Physicochemical and bacteriological characterization of wastewater from Mexico City. Water Sci Technol 37:1–8

    Article  Google Scholar 

  • Joss A, Keller E, Alder AC, Göbel A, McArdell CS, Ternes T, Siegrist H (2005) Removal of pharmaceuticals and fragrances in biological wastewater treatment. Water Res 39:3139–3152

    Article  CAS  Google Scholar 

  • Karan V, Vitorović S, Tutundžić V, Poleksić V (1998) Functional enzymes activity and gill histology of carp after copper sulfate exposure and recovery. Ecotoxicol Environ Saf 40(1):49–55

    Article  CAS  Google Scholar 

  • Kümmerer K (2001) Drugs in the environment: emission of drugs, diagnostic aids and disinfectants into wastewater by hospitals in relation to other sources—a review. Chemosphere 45:957–969

    Article  Google Scholar 

  • Lam MW, Young CJ, Brain RA, Johnson DJ, Hanson MA, Wilson CJ, Richards SM, Solomon KR, Mabury SA (2004) Aquatic persistence of eight pharmaceuticals in a microcosm study. Environ Toxicol Chem 23(6):1431–1440

    Article  CAS  Google Scholar 

  • Langford KH, Thomas KV (2009) Determination of pharmaceutical compounds in hospital effluents and their contribution to wastewater treatment works. Environ Int 35:766–770

    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 

  • Lushchak OV, Lushchak VI (2009) Possible pathways involved in activation of catalase and superoxide dismutase with sodium nitroprusside in yeast Saccharomyces cerevisiae. Ukr Biokhim Zh 81(2):34–39

  • Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101(1):13–30

    Article  CAS  Google Scholar 

  • Martin-Diaz L, Franzellitti S, Buratti S, Valbonesi P, Capuzzo A, Fabbri E (2009) Effects of environmental concentrations of the antiepilectic drug carbamazepine on biomarkers and cAMP-mediated cell signaling in the mussel Mytilus gallo provincialis. Aquat Toxicol 94(3):177–185

    Article  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(6):2176–2182

    Article  CAS  Google Scholar 

  • Mendonça E, Picado A, Paixão SM, Silva L, Cunha MA, Leitão S, Moura I, Cortez X, Brito F (2009) Ecotoxicity test in the environmental analysis of wastewater treatment plants: case study in Portugal. J Hazard Mater 163(2–3):665–670

    Article  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 

  • Montague P (2006) Drugs in the water. Rachel’s Environ Health Wkly 614(1):15–22

    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 Toxicol Pharmacol 143:141–149

    Article  Google Scholar 

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

  • NOM-001-SEMARNAT-1996. Norma Oficial Mexicana que establece los límites máximos 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

  • NOM-002-SEMARNAT-1996. Norma Oficial Mexicana que establece los límites máximos permisibles de contaminantes en las descargas de aguas residuales a los sistemas de alcantarillado urbano o municipal. Secretaría del Medio Ambiente y Recursos Naturales. Diario Oficial de la Federación 18-10-1993

  • NOM-CCA-029-ECOL-1993. Norma Oficial Mexicana. Límites máximos permisibles de contaminantes en las descargas de aguas residuales a cuerpos receptores provenientes de hospitales. Secretaría de Desarrollo Social. Diario Oficial de la Federación 18-10-1993

  • Nunes B, Gaio AR, Carvalho F, Guilhermino L (2008) Behavior and biomarkers of oxidative stress in Gambusia holbrooki after acute exposure to widely used pharmaceuticals and a detergent. Ecotoxicol Environ Saf 71(2):341–354

    Article  CAS  Google Scholar 

  • Oviedo-Gómez DGC, 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(1):39–43

    Article  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 

  • Postma JF, De Valk S, Dubbeldam M, Maas JL, Tonkes M, Schipper CA, Kater BJ (2002) Confounding factors in bioassays with freshwater and marine organisms. Ecotoxicol Environ Saf 53(2):226–237

    Article  CAS  Google Scholar 

  • Pozzetti L, Broccoli M, Potenza G, Canestro D, Affatato A, Sapone A, Antelli A, D’Amico E, Vangelisti S, Cantelli-Forti G, Paolini M, Ferrara G, Elia Ac, Dorr AJM, Taticchi MI, Mantilacci L, Natali M (2003) Techniche enzimatiche per valutare la tossicita di acque potabilizzate. Acqua Aria 4:64–68

    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 

  • Richardson SD (2009) Water analysis: emerging contaminants and current issues. Anal Chem 81(12):4645–4677

    Article  CAS  Google Scholar 

  • Salgueiro-Pagadigorria C, Kelmer-Bracht A, Bracht A, Ishii-Iwamoto E (2004) Naproxen affects Ca2+ fluxes in mitochondria, microsomes and plasma membrane vesicles. Chem Biol Interact 147:49–63

    Article  CAS  Google Scholar 

  • Sarasquete C, Segner H (2000) Cytochrome P4501A (CYP1A) in teleostean fishes. A review of immunohistochemical studies. Sci Total Environ 247(2):313–332

    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(2):141–150

    Article  CAS  Google Scholar 

  • Shacter E (2000) Quantification and significance of protein oxidation in biological samples. Drug Metab Rev 32:307–326

    Article  CAS  Google Scholar 

  • Sturve J, Almroth BC, Förlin L (2008) Oxidative stress in rainbow trout (Oncorhynchus mykiss) exposed to sewage treatment plant effluent. Ecotoxicol Environ Saf 70:446–452

    Article  CAS  Google Scholar 

  • Ueno H, Sayato Y, Nakamuro K (2000) Hematological effects of chlorine dioxide on in vitro exposure in mouse, rat and human blood and on subchronic exposure in mice. J Health Sci 46:110–116

    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 

  • Vasquez MI, Fatta-Kassinos D (2013) Is the evaluation of traditional physicochemical parameters sufficient to explain the potential toxicity of the treated wastewater at sewage treatment plants? Environ Sci Pollut Res 20:3516–3528

    Article  CAS  Google Scholar 

  • Vazquez-Roig P, Andreu V, Blasco C, Picó Y (2012) Risk assessment on the presence of pharmaceuticals in sediments, soils and waters of the Pego–Oliva Marshlands (Valencia, eastern Spain). Sci Total Environ 440:24–32

    Article  CAS  Google Scholar 

  • Verlicchi P, Galletti A, Petrovic M, Barceló D (2010) Hospital effluents as a source of emerging pollutants: an overview of micropollutants and sustainable treatment options. J Hydrol 389:416–428

    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 EA, Jesse CR, Leite MR, Nogueira CW (2009) Studies on preventive effects of diphenyl diselenide on acetaminophen-induced hepatotoxicity in rats. Pathophysiology 16(1):31–37

    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 

Download references

Acknowledgments

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

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

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

Neri-Cruz, N., Gómez-Oliván, L.M., Galar-Martínez, M. et al. Oxidative stress in Cyprinus carpio induced by hospital wastewater in Mexico. Ecotoxicology 24, 181–193 (2015). https://doi.org/10.1007/s10646-014-1371-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-014-1371-y

Keywords

Navigation