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Comparative and Interactive Biochemical Effects of Sub-Lethal Concentrations of Cadmium and Lead on Some Tissues of the African Catfish (Clarias gariepinus)

  • Received : 2018.09.13
  • Accepted : 2018.11.20
  • Published : 2019.07.15

Abstract

Cadmium is a strong toxic heavy metal which presents in paints and liquid wastes and causes oxidative stress in fish. On the other hand, lead is widely used for different purposes, e.g. lead pipes, it targets vital organs such as liver and kidney causing biochemical alterations. The present study evaluates the effects of 60 days exposure to Cd and Pb either single or combined together in African catfish. Sixty-four fishes were divided into 3 groups and exposed to $CdCl_2$ (7.02 mg/L) or $PbCl_2$ (69.3 mg/L) or a combination of them along with control group. Activities of acid phosphatase (ACP), lactate dehydrogenase (LDH) and glucose-6-phosphate dehydrogenase (G-6-PDH) were estimated. Moreover, gill, liver and kidney were assayed for activities of superoxide dismutase (SOD), catalase (CAT) and levels of glutathione (GSH) and malondialdehyde (MDA). Individual exposure showed that both Cd and Pb significantly decreased LDH activity and SOD activity in the kidney. Pb significantly increased G-6-PDH activity and decreased GSH level in the gill. CAT activity in liver and kidney elevated significantly on Cd exposure while lead caused a significant depletion in the liver and significant elevation in the kidney. Both Cd and Pb significantly increased MDA levels in liver and kidney while Pb increased its level in gills. The combined exposure resulted in normalization of LDH, G-6-PDH activity, and CAT activity in liver and kidney as well as GSH level in both tissues and MDA in gill and kidney. The combination increased SOD activity and MDA level in liver and decreased SOD activity in kidney and GSH level in gills. In conclusion, the antioxidant system of African catfish was adversely affected by prolonged exposure to Cd and Pb. The combined exposure caused less damage than individual exposure and returned most parameters to those of controls.

Keywords

References

  1. Mahurpawar, M. (2015) Effects of heavy metals on human health. Int. J. Res. Granthaalayah, 1-7.
  2. Perez, M. and Wallace, W. (2004) Differences in prey capture in grass shrimp, Palaemonetes pugio, collected along an environmental impact gradient. Arch. Environ. Contam. Toxicol., 46, 81-89. https://doi.org/10.1007/s00244-002-0249-9
  3. Ryan, P.B., Huet, N. and McIntosh, D.L. (2000) Longitudinal investigation of exposure to arsenic, cadmium, and lead in drinking water. Environ. Health Perspect., 108, 731. https://doi.org/10.1289/ehp.00108731
  4. Flora, G., Gupta, D. and Tiwari, A. (2012) Toxicity of lead: a review with recent updates. Interdiscip. Toxicol., 5, 47-58. https://doi.org/10.2478/v10102-012-0009-2
  5. Jhamtani, R.C., Shukla, S., Dahiya, M.S. and Agarwal, R. (2017) Evaluation of acute effects of lead at sub-lethal concentrations in zebrafish. Res. J. Environ. Toxicol., 11, 97-103. https://doi.org/10.3923/rjet.2017.97.103
  6. Szebedinszky, C., McGeer, J.C., McDonald, D.G. and Wood, C.M. (2001) Effects of chronic Cd exposure via the diet or water on internal organ-specific distribution and subsequent gill Cd uptake kinetics in juvenile rainbow trout (Oncorhynchus mykiss). Environ. Toxicol. Chem., 20, 597-607. https://doi.org/10.1002/etc.5620200320
  7. Hosseini, M., Naderi, M., Gholami, S. and Hadipour, M. (2018) Toxic metals in the muscle and liver of five main commercially-important fishes from the Persian Gulf, Southern Iran. Caspian J. Environ. Sci., 16, 191-198.
  8. Lee, J. and Freeman, J.L. (2014) Zebrafish as a model for investigating developmental lead (Pb) neurotoxicity as a risk factor in adult neurodegenerative disease: a mini-review. Neurotoxicology, 43, 57-64. https://doi.org/10.1016/j.neuro.2014.03.008
  9. Nimmy, M. and Joseph, P.V. (2018) Effect of lead nitrate on the histopathology of the gill, liver and kidney of the freshwater fish, cirrhinusmrigala. Eur. J. Pharm. Med. Res., 5, 416-420.
  10. Asagba, S.O., Eriyamremu, G.E. and Igberaese, M.E. (2008) Bioaccumulation of cadmium and its biochemical effect on selected tissues of the catfish (Clarias gariepinus). Fish Physiol. Biochem., 34, 61-69. https://doi.org/10.1007/s10695-007-9147-4
  11. Kock, G., Triendl, M. and Hofer, R. (1996) Seasonal patterns of metal accumulation in Arctic char (Salvelinus alpinus) from an oligotrophic Alpine lake related to temperature. Can. J. Fish. Aquat. Sci., 53, 780-786. https://doi.org/10.1139/f95-243
  12. Elarabany, N., Bahnasawy, M., Edrees, G. and Alkazagli, R. (2017) Effects of salinity on some haematological and biochemical parameters in nile tilapia, Oreochromis niloticus. Agri. Forest. Fish., 6, 200-205. https://doi.org/10.11648/j.aff.20170606.13
  13. Das, P., Ayyappan, S., Das, B. and Jena, J. (2004) Nitrite toxicity in Indian major carps: sublethal effect on selected enzymes in fingerlings of Catla catla, Labeo rohita and Cirrhinus mrigala. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 138, 3-10. https://doi.org/10.1016/j.cca.2004.03.010
  14. Barnhoorn, I. and Van Vuren, J. (2004) The use of different enzymes in feral freshwater fish as a tool for the assessment of water pollution in South Africa. Ecotox. Environ. Safe., 59, 180-185. https://doi.org/10.1016/j.ecoenv.2003.09.004
  15. OECD (2004) OECD Guidelines for the Testing of Chemicals/ Section 2: Effects on Biotic Systems Test No. 202: Daphnia sp. Acute Immobilisation Test, OECD Publishing, USA, pp. 12.
  16. Farombi, E., Adelowo, O. and Ajimoko, Y. (2007) Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African catfish (Clarias gariepinus) from Nigeria Ogun River. Int. J. Environ. Res. Public Health, 4, 158-165. https://doi.org/10.3390/ijerph2007040011
  17. Saliu, J.K. and Bawa-Allah, K.A. (2012) Toxicological effects of lead and zinc on the antioxidant enzyme activities of post-juvenile Clarias gariepinus. Res. Environ., 2, 21-26. https://doi.org/10.5923/j.re.20120201.03
  18. Mir, G., Tharani, M., Hussain, A., Ahmad, Y. and Rashid, A. (2016) Variations in acid phosphatase (ACP) and alkaline phosphatase (ALP) activities in liver and kidney of a freshwater fish Labeo rohita exposed to heavy metal concentrations. Eur. J. Pharm. Med. Res., 3, 398-401.
  19. Thirumavalavan, R. (2010) Research article effect of cadmium on biochemical parameters in freshwater fish, Oreochromis mossambicus. Asian J. Sci. Technol., 5, 100-104.
  20. Long, S.M., Ryder, K.J. and Holdaway, D.A. (2003) The use of respiratory enzymes as biomarkers of petroleum hydrocarbon exposure in Mytilus edulis planulatus. Ecotoxicol. Environ. Saf., 55, 261-270. https://doi.org/10.1016/S0147-6513(02)00137-9
  21. Winzer, K., Van Noorden, C.J. and Kohler, A. (2001) Quantitative cytochemical analysis of glucose-6-phosphate dehydrogenase activity in living isolated hepatocytes of European flounder for rapid analysis of xenobiotic effects. J. Histochem. Cytochem., 49, 1025-1032. https://doi.org/10.1177/002215540104900810
  22. Osman, A.G., Mekkawy, I.A., Verreth, J. and Kirschbaum, F. (2007) Effects of lead nitrate on the activity of metabolic enzymes during early developmental stages of the African catfish, Clarias gariepinus (Burchell, 1822). Fish Physiol. Biochem., 33, 1-13. https://doi.org/10.1007/s10695-006-9111-8
  23. Rosety-Rodriguez, M., Ordonez, F., Rosety, I., Rosety, J. and Rosery, M. (2005) Erythrocyte antioxidant enzymes of gilthead as early-warning bio-indicators of oxidative stress induced by malathion. Haema, 8, 237-240.
  24. Leopold, J.A., Zhang, Y.-Y., Scribner, A.W., Stanton, R.C. and Loscalzo, J. (2003) Glucose-6-phosphate dehydrogenase overexpression decreases endothelial cell oxidant stress and increases bioavailable nitric oxide. Arterioscler. Thromb. Vasc. Biol., 23, 411-417. https://doi.org/10.1161/01.ATV.0000056744.26901.BA
  25. Singh, R.K. and Sharma, B. (1998) Carbofuran?induced biochemical changes in Clarias batrachus. Pestic. Sci., 53, 285-290. https://doi.org/10.1002/(SICI)1096-9063(199808)53:4<285::AID-PS771>3.0.CO;2-0
  26. Almeida, J., Novelli, E., Silva, M.D.P. and Júnior, R.A. (2001) Environmental cadmium exposure and metabolic responses of the Nile tilapia, Oreochromis niloticus. Environ. Pollut., 114, 169-175. https://doi.org/10.1016/S0269-7491(00)00221-9
  27. Rajanna, B., Chetty, C., McBride, V. and Rajanna, S. (1990) Effects of lead on K (+)-para-nitrophenyl phosphatase activity and protection by thiol reagents. Biochem. Int., 20, 1011-1018.
  28. Ercal, N., Gurer-Orhan, H. and 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. https://doi.org/10.2174/1568026013394831
  29. Asagba, S. and Obi, F. (2000) Effect of cadmium on kidney and liver cell membrane integrity and antioxidant enzyme status: implications for Warri River cadmium level. Trop. J. Environ. Sci. Health, 3, 33-39.
  30. Timbrell, J.A. (2008) Principles of Biochemical Toxicology, CRC Press.
  31. Zhang, H., Liu, Y., Liu, R., Liu, C. and Chen, Y. (2014) Molecular mechanism of lead-induced superoxide dismutase inactivation in zebrafish livers. J. Phys. Chem. B, 118, 14820-14826. https://doi.org/10.1021/jp511056t
  32. McCord, J.M. (1996) Effects of positive iron status at a cellular level. Nutr. Res., 54, 85-88.
  33. Atli, G., Alptekin, O., Tukel, S. and Canli, M. (2006) Response of catalase activity to $Ag^+,\;Cd^{2+},\;Cr^{6+},\;Cu^{2+}$ and $Zn^{2+}$ in five tissues of freshwater fish Oreochromis niloticus. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 143, 218-224. https://doi.org/10.1016/j.cbpc.2006.02.003
  34. Gul, S., Belge-Kurutas, E., Yildiz, E., Sahan, A. and Doran, F. (2004) Pollution correlated modifications of liver antioxidant systems and histopathology of fish (Cyprinidae) living in Seyhan Dam Lake, Turkey. Environ. Int., 30, 605-609. https://doi.org/10.1016/S0160-4120(03)00059-X
  35. Hidalgo, M.C., Exposito, A., Palma, J.M. and de la Higuera, M. (2002) Oxidative stress generated by dietary Zn-deficiency: studies in rainbow trout (Oncorhynchus mykiss). Int. J. Biochem. Cell Biol., 34, 183-193. https://doi.org/10.1016/S1357-2725(01)00105-4
  36. Ahmad, I., Hamid, T., Fatima, M., Chand, H.S., Jain, S.K., Athar, M. and Raisuddin, S. (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. https://doi.org/10.1016/S0304-4165(00)00098-2
  37. Stanic, B. and Andric, N., Zoric, S., Grubor-Lajsic, G. and Kovacevic, R. (2006) Assessing pollution in the Danube River near Novi Sad (Serbia) using several biomarkers in sterlet (Acipenser ruthenus L.). Ecotoxicol. Environ. Saf., 65, 395-402. https://doi.org/10.1016/j.ecoenv.2005.08.005
  38. Jan, A., Ali, A. and Haq, Q. (2011) Glutathione as an antioxidant in inorganic mercury induced nephrotoxicity. J. Postgrad. Med., 57, 72-77. https://doi.org/10.4103/0022-3859.74298
  39. Ansari, S. and Ansari, B.A. (2014) Temporal variations of CAT, GSH, and LPO in gills and livers of zebrafish, Danio rerio, exposed to dimethoate. Arch. Pol. Fish., 22, 101-109. https://doi.org/10.2478/aopf-2014-0009
  40. Allen, P. (1996) Comparative and interactive effects of mercury, cadmium and lead on tissue GSH levels in Oreochromis aureus (Steindachner): implications for monitoring heavy metal pollution. J. Appl. Ichthyol., 12, 21-26. https://doi.org/10.1111/j.1439-0426.1996.tb00054.x
  41. Wallace, K.B. (1989) Glutathione?dependent metabolism in fish and rodents. Environ. Toxicol. Chem., 8, 1049-1055. https://doi.org/10.1002/etc.5620081110
  42. Doherty, V., Ogunkuade, O. and Kanife, U. (2010) Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in some selected fishes in Lagos, Nigeria. Am. Eurasian J. Agric. Environ. Sci., 7, 359-365.
  43. Wang, J., Zhu, X., Huang, X., Gu, L., Chen, Y. and Yang, Z. (2016) Combined effects of cadmium and salinity on juvenile Takifugu obscurus: cadmium moderates salinity tolerance; salinity decreases the toxicity of cadmium. Sci. Rep., 6, 30968. https://doi.org/10.1038/srep30968
  44. Romeo, M., Bennani, N., Gnassia-Barelli, M., Lafaurie, M. and Girard, J. (2000) Cadmium and copper display different responses towards oxidative stress in the kidney of the sea bass Dicentrarchus labrax. Aquat. Toxicol., 48, 185-194. https://doi.org/10.1016/S0166-445X(99)00039-9
  45. Pandey, S., Ahmad, I., Parvez, S., Bin-Hafeez, B., Haque, R. and Raisuddin, S. (2001) Effect of endosulfan on antioxidants of freshwater fish Channa punctatus Bloch: 1. Protection against lipid peroxidation in liver by copper preexposure. Arch. Environ. Contam. Toxicol., 41, 345-352. https://doi.org/10.1007/s002440010258
  46. De Smet, H., De Wachter, B., Lobinski, R. and Blust, R. (2001) Dynamics of (Cd, Zn)-metallothioneins in gills, liver and kidney of common carp Cyprinus carpio during cadmium exposure. Aquat. Toxicol., 52, 269-281. https://doi.org/10.1016/S0166-445X(00)00136-3
  47. Schlenk, D. and Rice, C. (1998) Effect of zinc and cadmium treatment on hydrogen peroxide-induced mortality and expression of glutathione and metallothionein in a teleost hepatoma cell line. Aquat. Toxicol., 43, 121-129. https://doi.org/10.1016/S0166-445X(98)00050-2