Skip to main content

Antioxidant Responses and Nuclear Deformations in Freshwater Fish, Oreochromis niloticus, Facing Degraded Environmental Conditions

Abstract

Two sites of collection along river Nile, nearby metal-related factories (site2) and 7 km downstream (site3) were compared to unpolluted reference fish farm (site1). Metals concentration (Cu, Zn, Pb, Fe, Mn and Cd) in water and sediment samples showed highly significant (p < 0.01) differences among sites. According to contamination factor and pollution load index values, overall pollution was ordered as site2 > site3 > site1. Compared with Oreochromis niloticus of site1, activities of superoxide dismutase, catalase and glutathione-S-transferase as well as malondialdehyde formation were significantly (p < 0.01) increased in both liver and gills of fish collected from metal contaminated sites. This increment showed a tissue-specific pattern with higher rate of increment in liver than in gills. While reduced glutathione level was sharply decreased in site2 and site3. Micronucleus test was assessed as an environmental genotoxic endpoint in erythrocytes. Assessment of eight nuclear deformations showed gradient frequencies related to the distance from the industrial discharges.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  Google Scholar 

  2. AEP (1997) Alberta water quality guideline for the protection of freshwater aquatic life: Dissolved oxygen. Standards and Guidelines Branch, Alberta Environmental Protection, Edmonton

    Google Scholar 

  3. APHA (2005) Standard methods for the examination of water and wastewater. American Public Health Association, New York

    Google Scholar 

  4. Atli G, Alptekin O, Tukel S, Canli M (2006) Response of catalase activity to Ag2+, Cd2+, Cr2+, Cu2+ and Zn2+ in five tissues of freshwater fish Oreochromis niloticus. Comp Biochem Physiol C 143:218–224

    Article  Google Scholar 

  5. Baysoy E, Atli G, Gürler CÖ, Dogan Z, Eroglu A, Kocalar K, Canli M (2012) The effects of increased freshwater salinity in the biodisponibility of metals (Cr, Pb) and effects on antioxidant systems of Oreochromis niloticus. Ecotoxicol Environ Saf 84:249–253

    Article  CAS  Google Scholar 

  6. Beutler E, Duron O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888

    CAS  Google Scholar 

  7. Boyd CE (1990) Water quality in ponds for aquaculture. Birmingham Publishing Co., Birmingham, Alabama

    Google Scholar 

  8. Burton CA, Hatlelid K, Divine K, Carter DE, Fernando Q, Brendel K, Gandolfi AJ (1995) Glutathione effects on toxicity and uptake of mercuric chloride and sodium arsenite in rabbit renal cortical slices. Environ Health Perspect 103:81–84

    Article  CAS  Google Scholar 

  9. Cabrera F, Conde B, Flores V (1992) Heavy metals in the surface sediments of the tidal river Tinto (SW Spain). Fresenius Environ Bull 1:400–405

    CAS  Google Scholar 

  10. Cao L, Huang W, Liu J, Yin X, Dou S (2010) Accumulation and oxidative stress biomarkers in Japanese flounder larvae and juveniles under chronic cadmium exposure. Comp Biochem Physiol C 151:386–392

    Google Scholar 

  11. Cao L, Huang W, Shan X, Ye Z, Dou S (2012) Tissue-specific accumulation of cadmium and its effects on antioxidative responses in Japanese flounder juveniles. Environ Toxicol Pharmacol 33:16–25

    Article  CAS  Google Scholar 

  12. CCME (1999) Canadian water quality guidelines for the protection of aquatic life: summary table. In: Canadian environmental quality guidelines. Canadian Council of Ministers of the Environment, Winnipeg, Canada

  13. Da Silva Souza T, Fontanetti CS (2006) Micronucleus test and observation of nuclear alterations in erythrocytes of Nile tilapia exposed to waters affected by refinery effluent. Mutat Res 605(1–2):87–93

    Article  Google Scholar 

  14. Dautremepuits C, Marcogliese DJ, Gendron AD, Fournier M (2009) Gill and kidney antioxidant processes and innate immune system responses of yellow perch (Perca flavescens) exposed to different contaminants in the St. Lawrence River, Canada. Sci Total Environ 407:1055–1064

    Article  CAS  Google Scholar 

  15. Ergene S, Avas TC, Celik A, Koleli N, Kaya F, Karahan A (2007) Monitoring of nuclear abnormalities in peripheral erythrocytes of three fish species from the Goksu Delta (Turkey): genotoxic damage in relation to water pollution. Ecotoxicology 16(4):385–391

    Article  CAS  Google Scholar 

  16. Fenech M (1993) The cytokinesis-block micronucleus technique: a detailed description of the method and its application to genotoxicity studies in human populations. Mutat Res 285:35–44

    Article  CAS  Google Scholar 

  17. Fenech M, Chang WP, Kirsch-Volders M, Holland N, Bonassi S, Zeiger E (2003) HUMN project: detailed description of the scoring criteria for the cytokinesis block micronucleus assay using isolated human lymphocyte cultures. Mutat Res 534(1–2):65–75

    Article  CAS  Google Scholar 

  18. Guilherme S, Válega M, Pereira ME, Santos MA, Pacheco M (2008) Antioxidant and biotransformation responses in Liza aurata under environmental mercury exposure–relationship with mercury accumulation and implications for public health. Mar Poll Bull 56:845–859

    Article  CAS  Google Scholar 

  19. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  Google Scholar 

  20. Hakanson L (1980) An ecological risk index for aquatic pollution control a sedimentological approaches. Water Res 14(8):975–1001

    Article  Google Scholar 

  21. Harabawy AS, Mosleh YY (2014) The role of vitamins A, C, E and selenium as antioxidants against genotoxicity and cytotoxicity of cadmium, copper, lead and zinc on erythrocytes of Nile tilapia, Oreochromis niloticus. Ecotoxicol Environ Saf 104:28–35

    Article  CAS  Google Scholar 

  22. Has-Schon E, Bogut I, Strelec I (2006) Heavy metal profile in five fish species included in human diet, domiciled in the end flow of River Neretva (Croatia). Arch Environ Contam Toxicol 50(4):545–551

    Article  CAS  Google Scholar 

  23. Hseu ZY (2004) Evaluating heavy metal contents in nine composts using four digestion methods. Bioresour Technol 95:53–59

    Article  CAS  Google Scholar 

  24. Issac RA, Kerber JD (1971) Atomic absorption and flame photometry. Techniques and uses in soil, plant and water analysis. In: Walsh LM (ed) Instrumental methods for analysis of soil and plant tissue. Soil Science Society of America-Agronomy Society of America Inc, Madison, WI, pp 17–37

    Google Scholar 

  25. MacDonald DD, Ingersoll CG, Berger TA (2000) Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Arch Environ Contam Toxicol 39:20–31

    Article  CAS  Google Scholar 

  26. Martin J, Meybeck M (1979) Elemental mass-balance of material carried by major world rivers. Mar Chem 7(3):178–206

    Article  Google Scholar 

  27. Melegaria SP, Perreault F, Costa RHR, Popovic R, Matias WG (2013) Evaluation of toxicity and oxidative stress induced by copper oxide nanoparticles in the green alga Chlamydomonas reinhardtii. Aquat Toxicol 142–143:431–440

    Article  Google Scholar 

  28. Nishikimi M, Appaji N, Yagi K (1972) The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 46:849–854

    Article  CAS  Google Scholar 

  29. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  Google Scholar 

  30. Omar WA, Zaghloul KH, Abdel-Khalek AA, Abo-Hegab S (2012) Genotoxic effects of metal pollution in two fish species, Oreochromis niloticus and Mugil cephalus, from highly degraded aquatic habitats. Mutat Res 746:7–14

    Article  CAS  Google Scholar 

  31. Persaud D, Jaagumagi R, Hayton A (1993) Guidelines for the protection and management of aquatic sediment quality in Ontario. Ontario Ministry of the Environment, Queen’s Printer of Ontario, Ontario

    Google Scholar 

  32. Qu R, Feng M, Wang X, Qin L, Wang C, Wang Z, Wang L (2014) Metal accumulation and oxidative stress biomarkers in liver of freshwater fish Carassius auratus following in vivo exposure to waterborne zinc under different pH values. Aquat Toxicol 150:9–16

    Article  CAS  Google Scholar 

  33. Robert FC, David FB, Gary AC (1986) Effects of pH on the Toxicities of cadmium, copper, and zinc to Steelhead Trout (Salmo gairdneri). Can J Fish Aquat Sci 43(8):1497–1503

    Article  Google Scholar 

  34. Ruas CBG, Carvalho Cd-S, de Araújo HSS, Espíndola ELG, Fernandes MN (2008) Oxidative stress biomarkers of exposure in the blood of cichlid species from a metal-contaminated river. Ecotoxicol Environ Saf 71:86–93

    Article  CAS  Google Scholar 

  35. Sampaio FG, Boijink CL, Oba ET, Santos LRB, Kalinin AL, Rantin FT (2008) Antioxidant defenses and biochemical changes in pacu (Piaractus mesopotamicus) in response to single and combined copper and hypoxia exposure. Comp Biochem Physiol C 147:43–51

    Google Scholar 

  36. Souid G, Souayed N, Yaktiti F, Maaroufi K (2014) Lead accumulation pattern and molecular biomarkers of oxidative stress in sea bream (Sparus aurata) under short-term metal treatment. Drug Chem Toxicol 15:1–8

    Google Scholar 

  37. Tomlinson DC, Wilson JG, Harris CR, Jeffrey DW (1980) Problems in assessment of heavy metals in estuaries and the formation of pollution index. Helgol Mar Res 33:566–575

    Google Scholar 

  38. Turkmen A, Turkmen M, Tepe Y, Mazlum Y, Oymael S (2006) Metal concentrations in Blue Crab (Callinectes sapidus) and Mullet (Mugil cephalus) in Iskenderun Bay, Northern East Mediterranean, Turkey. Bull Environ Contam Toxicol 77:186–193

    Article  CAS  Google Scholar 

Download references

Conflict of interest

Amr Adel Abdel-Khalek declares that he has no conflict of interest.

Compliance with Ethical Standards

This manuscript complies to the Ethical Rules applicable for this journal.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Amr Adel Abdel-Khalek.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Abdel-Khalek, A.A. Antioxidant Responses and Nuclear Deformations in Freshwater Fish, Oreochromis niloticus, Facing Degraded Environmental Conditions. Bull Environ Contam Toxicol 94, 701–708 (2015). https://doi.org/10.1007/s00128-015-1509-5

Download citation

Keywords

  • Antioxidant biomarkers
  • Metal toxicity
  • Nuclear anomalies