The Protective Role of Vitamin C and Chitosan Against Paraquat-induced Oxidative Stress in Muscles of Common Carp (Cyprinus carpio)

Open access


The purpose of this study was to examine the effects of antioxidants, including vitamin C, chitosan or a combination of both, on oxidative stress markers in muscles, as edible tissues of fish, exposed to paraquat. Fish exposed to 0.02 mg/L paraquat for 21 days were fed different diets: a normal diet, a diet containing chitosan (1000 mg/kg diet), a diet with vitamin C (1000 mg/kg diet) or both vitamin C and chitosan. Oxidative stress markers, including the activity of catalase, total antioxidant and malondialdehyde (MDA), as well as biochemical parameters including the activity of aspartate aminotransferase (AST), alanine aminotransferase (ALT), creatine phosphokinase (CPK), lactate dehydrogenase (LDH) and acetylcholinesterase (AChE), were measured in muscles. Fish exposure to paraquat increased LDH, CPK, catalase and MDA activity significantly, while it significantly decreased AST, ALT and AChE activity and total antioxidant capacity in muscles. Administration of vitamin C, combined with chitosan, to fish exposed to paraquat was effective in regulating AChE, AST, ALT, LDH, CPK and catalase activity. A significant increase in the total antioxidant status and a significant decrease in MDA levels were observed in fish fed chitosan-vitamin C complex. In conclusion, it is suggested that combined supplementation with vitamin C and chitosan may improve the detoxification system in the muscles of fish and protect common carp from paraquat toxicity.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Agrawal P. Strijkers G. Nicolay K. (2010): Chitosan-based systems for molecular imaging. Advanced Drug Delivery Reviews 62 42-58.

  • Alcaro S. Arcone R. Vecchio I. Ortuso F. Gallelli A. Pasceri R. Procopio A. Iannone M. (2007): Molecular modelling and enzymatic studies of acetylcholinesterase and butyrylcholinesterase recognition with paraquat and related compounds. SAR and QSAR in Environmental Research 18 5 595-602.

  • Alishahi A. Mirvaghefi A. Tehrani M. Farahmand H. Koshio S. D. F. Elsabee M. (2011a): Chitosan nanoparticle to carry vitamin C through the gastrointestinal tract and induce the non-specific immunity system of rainbow trout (Oncorhynchus mykiss). Carbohydrate Polymers 86 1 142-146.

  • Alishahi A. Mirvaghefi A. Tehrani M. Farahmand H. Shojaosadati S. Dorkoosh F. Elsabee M. (2011b): Shelf life and delivery enhancement of vitamin C using chitosan nanoparticles. Food Chemistry 126 3 935-940.

  • Baltusnikas J. Venckunas T. Kilikevicius A. Fokin A. Ratkevicius A. (2015): Efflux of Creatine kinase from isolated soleus muscle depends on age sex and type of exercise in mice. Journal of Sports Science and Medicine 14 379-385.

  • Banaee M. Ahmadi K. (2011): Sub-lethal toxicity impacts of endosulfan on some biochemical parameters of the freshwater crayfish (Astacus leptodactylus). Research Journal of Environmental sciences 5 11 827-835.

  • Banaee M. Mehrpak M. Nematdoost Hagi B. Noori A. (2015a): Amelioration of cadmium-induced changes in biochemical parameters of the muscle of Common Carp (Cyprinus carpio) by Vitamin C and Chitosan. International Journal of Aquatic Biology 3 6 362-371.

  • Banaee M. Sureda A. Shahaf S. Fazilat N. (2015b): Protective effects of silymarin extract on malthion-induced zebra cichlid (Cichlasoma nigrofasciatum) hepatotoxicity. Iranian Journal of Toxicology 9 28 1239-1246.

  • Banaee M. Nematdoust haghi B. Ibrahim A. (2013a): Sublethal toxicity of chlorpyrifos on Common carp Cyprinus carpio (Linnaeus 1758) Biochemical response. International Journal of Aquatic Biology 1 6 281-288.

  • Banaee M. Sureda A. Mirvaghefi A.R. Ahmadi K. (2013b): Biochemical and histological changes in the liver tissue of Rainbow trout (Oncorhynchus mykiss) exposed to sublethal concentrations of diazinon. Fish Physiology and Biochemistry 39 489-501.

  • Banaee M. Shahfve S. Vaziriyan M. Taheri S. Nematdoost Haghi B. (2016): Effects of sewage effluent on blood biochemical parameters of common carp (Cyprinus carpio): A case study of Behbahan Khuzestan Province. Journal of Chemical Health Risks 6 3 161-173.

  • Banaee M. Sureda A. Zohiery F. Nematdoost Hagi B. Garanzini D. (2014): Alterations in biochemical parameters of the freshwater fish Alburnus mossulensis exposed to sub-lethal concentrations of Fenpropathrin. International Journal of Aquatic Biology 2 2 58-68.

  • Benzie I. Strain J. (1996): The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power” the FRAP assay. Analytical Biochemistry 239 1 70-76.

  • Carageorgiou H. Tzotzes V. Sideris A. Zarros A. Tsakiris S. (2005): Cadmium effects on brain acetylcholinesterase activity and antioxidant status of adult rats: modulation by zinc calcium and L-cysteine co-administration. Basic & Clinical Pharmacology & Toxicology 97 320-324.

  • Chimela W. Mesua N. Abdulraheem B.A. (2014): Aspartate transaminase (AST) activity in selected tissues & organs of Clarias Gariepinus exposed to different levels of paraquat. Journal of Environmental & Analytical Toxicology 4 214. doi: 10.4172/2161-0525.1000214.

  • Chua B. Al Kobiasi M. Zeng W. Mainwaring D. Jackson D. (2012): Chitosan-based particles as biocompatible delivery vehicles for peptide and protein-based vaccines. 5th Vaccine and ISV Global Annual Congress Proccedia in Vaccinology 6 74-79.

  • Eisler R. (1999): Paraquat Hazards to Fish Wildlife and Invertebrates: A Synoptic Review. U.S. Fish and Wildlife Service Patuxent Wildlife Research Center Laurel Maryland 20708. Biological Report 85(1.22) 38 pages.

  • Ergul Y. Erkan T. Uzun H. Genc H. Altug T. Erginoz E. (2010): Effect of vitamin C on oxidative liver injury due to isoniazid in rats. Pediatrics International 52 1 69-74.

  • Gil H. Hong J. Jang S. Hong S. (2014): Diagnostic and therapeutic approach for acute paraquat intoxication. Journal of Korean Medical Science 29 11 1441-1449.

  • Goulding A.T. Shelley L.K. Ross P.S. Kennedy C.J. (2013): Reduction in swimming performance in juvenile rainbow trout (Oncorhynchus mykiss) following sublethal exposure to pyrethroid insecticides. Comparative Biochemistry and Physiology Part C 157 280–286.

  • Grenha A. Al-Qadi S. Seijo B. Remuñán-Lopez C. (2010a): The potential of chitosan for pulmonary drug delivery. Journal of Drug Delivery Science and Technology 20 33-43.

  • Grenha A. Gomes M. Rodrigues M. Santo V. Mano J. Neves N. Reis R. (2010b): Development of new chitosan/carrageenan nanoparticles for drug delivery applications. Journal of Biomedical Materials Research Part A 92 1265-1272.

  • Halappa R. David M. (2009): Behavioural responses of the freshwater fish Cyprinus carpio (Linnaeus) following sublethal exposure to chlorpyrifos. Turkish Journal of Fisheries and Aquatic Sciences 9 233-238.

  • Isik I. Celik I. (2008): Acute effects of methyl parathion and diazinon as inducers for oxidative stress on certain biomarkers in various tissues of rainbowtrout (Oncorhynchus mykiss). Pesticide Biochemistry and Physiology 92 38-42.

  • Ismail S M. (2013): Protective effects of vitamin C against biochemical toxicity induced by malathion pesticides in male albino rat. Journal of Evolutionary Biology Research 5 1 1-5.

  • Johnson A. Rohlfs E. Silverman L. (1999): Proteins. In Tietz Textbook of Clinical Chemistry. 3rd Ed W.B. Saunders Company Philadelphia 1999 pp 477-540.

  • Knedel M. Boetteger R. (1967): Kinetic method for determination of pseudocholinesterase (acylcholine acylhydrolase) activity. Wiener klinische Wochenschrift 45 325-327.

  • Lekka M. Laidler P. Ignacak J. Łabedz M. Lekki J. Struszczyk H. Stachura Z. Hrynkiewicz A.Z. (2001): The effect of chitosan on stiffness and glycolytic activity of human bladder cells. Biochimica et Biophysica Acta 1540 2 127-136.

  • Li Z.H. Velisek J. Zlabek V. Grabic R. Machova J. Kolarova J. Randak T. (2010): Hepatic antioxidant status and hematological parameters in rainbow trout Oncorhynchus mykiss after chronic exposure to carbamazepine. Chemico-Biological Interactions 183 98-104.

  • Mehrpak M. Banaee M. Nematdoost Haghi B. Noori A. (2015): Protective effects of vitamin C and chitosan against cadmium-induced oxidative stress in the liver of common carp (Cyprinus carpio): Iranian Journal of Toxicology 9 30 1360-1367.

  • Mirvaghefi A.R. Ali M. Poorbagher H. (2016): Effects of vitamin C on oxidative stress parameters in rainbow trout exposed to diazinon. Ege Journal of Fisheries and Aquatic Sciences 32 2 113-120.

  • Mobasher M. Aramesh K. Aldavoud S. J. Ashrafganjooei N. Divsalar K. Phillips C. Larijani B. (2008): Proposing a national ethical framework for animal research in Iran. Iranian Journal of Public Health 37 1 39-46.

  • Monteiro D.A. de Almeida J.A. Rantin F.T. Kalinin A.L. (2006): Oxidative stress biomarkers in the freshwater characid fish Brycon cephalus exposed to organophosphorus insecticide Folisuper 600 (methyl parathion). Comparative Biochemistry and Physiology Part C 143 141-149.

  • Moss D. Henderson A. (1999): Clinical enzymology. In Tietz Textbook of Clinical Chemistry. 3rd Ed. W.B. Saunders Company Philadelphia 1999 pp 617-721.

  • Murray R. Granner D. Mayes P. Rodwell V. (2003): Harper’s Illustrated Biochemistry Twenty-Sixth Edition Lange Medical Books/McGraw-Hill (Medical Publishing Division) New York 2003.

  • Naziroğlu M. Kilinç F. Uğuz A. Çelik Ö. Bal R. Butterworth P. Baydar ML. (2010): Oral vitamin C and E combination modulates blood lipid peroxidation and antioxidant vitamin levels in maximal exercising basketball players. Cell Biochemistry and Function 28 300-305.

  • Oruç E.Ö. Usta D. (2007): Evaluation of oxidative stress responses and neurotoxicity potential of diazinon in different tissues of Cyprinus carpio. Environmental Toxicology and Pharmacology 23 48-55.

  • Ozturk I. Ozturk F. Gul M. Ates B. Cetin A. (2009): Protective effects of ascorbic acid on hepatotoxicity and oxidative stress caused by carbon tetrachloride in the liver of Wistar rats. Cell Biochemistry and Function 27 309-315.

  • Pangestuti R. Kim S.K. (2010): Neuroprotective Properties of Chitosan and Its Derivatives. Marine Drugs 8 7 2117-2128.

  • Parvez S. Raisuddin S. (2006): Effects of paraquat on the freshwater fish Channa punctata (Bloch): non-enzymatic antioxidants as biomarkers of exposure. Archives of Environmental Contamination and Toxicology 50 3 392-397.

  • Patil V.K. David M. (2008): Behaviour and respiratory dysfunction as an index of malathion toxicity in the freshwater fish Labeo rohita (Hamilton). Turkish Journal of Fisheries and Aquatic Sciences 8 233-237.

  • Paulino M.G. Sakuragui M.M. Fernandes M.N. (2012): Effects of atrazine on the gill cells and ionic balance in a neotropical fish Prochilodus lineatus. Chemosphere 86 1-7.

  • Placer Z. Cushman L. Johnson B. (1996): Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems. Analytical Biochemistry 16 2 359-364.

  • Rad E. Alishahi M. Ghorbanpour M. Zarei M. (2014): The effects of oral administration of extracted chitosan from white leg shrimp (Litopenaeus vannamei) on hematological and growth indices in common carp (Cyprinus carpio). Journal of Veterinary Research 69 4 385-393.

  • Rao J.V. (2006): Biochemical alterations in euryhaline fish Oreochromis mossambicus exposed to sub-lethal concentrations of an organophosphorus insecticide monocrotophos. Chemosphere 65 1814-1820.

  • Sabullah M. K. Sulaiman M. R. Abd Shukor M. Y. shaman N. A. Khalid A. Ahmad S. A. (2014): The assessment of cholinesterase from the liver of Puntinus javanicus detection of metal ions. The Scientific World Journal ID 571094 9. doi: 10.1155/2014/571094.

  • Santhosh S. Sini T. Anandan R. Mathew P. (2007): Hepatoprotective activity of chitosan against isoniazid and rifampicin-induced toxicity in experimental rats. European Journal of Pharmacology 572 1 69-73.

  • Santos T.G. Martinez C.B.R. (2012): Atrazine promotes biochemical changes and DNA damage in a Neotropical fish species. Chemosphere 89 1118-1125.

  • Sepici-Dinçel A. Cağlan Karasu Benli A. Selvi M. Sarıkaya R. Şahin D. Özkul I.A. Erkoç F. (2009): Sublethal cyfluthrin toxicity to carp (Cyprinus carpio L.) fingerlings: biochemical hematological histopathological alterations. Ecotoxicology and Environmental Safety 72 1433-1439.

  • Sharifinasab Z. Banaee M. Mohiseni M. Noori A. (2016): Vitamin C and chitosan alleviate toxicity effects of paraquat on some biochemical parameters in hepatocytes of common carp. Iranian Journal of Toxicology 10 1 31-40.

  • Slenzka K. Appel R. Rahmann H. (1993): Brain creatine kinase activity during ontogeny of the cichlid fish Oreochromis mossambicus and the clawed toad Xenopus laevis influence of gravity? Neurochemistry International 22 4 405-411.

  • Sun T. Zhu Y. Xie J. Yin X. (2011): Antioxidant activity of N-acyl chitosan oligosaccharide with same substituting degree. Bioorganic and Medicinal Chemistry Letters 21 2 798-800.

  • Uetaki M. Tabata S. Nakasuka F. Soga T. Tomita M. (2016): Metabolomic alterations in human cancer cells by vitamin C-induced oxidative stress. Scientific Reports 5 13896 doi:10.1038/srep13896.

  • Velisek J. Svobodova Z. Machova J. (2008): Effects of bifenthrin on some haematological biochemical and histopathological parameters of common carp (Cyprinus carpio L.). Fish Physiology and Biochemistry 35 4 583-590.

  • Wei W. Lv P. Chen X. Yue Z. Fu Q. Liu S. Yue H. Ma G. (2013): Codelivery of mTERT siRNA and paclitaxel by chitosan-based nanoparticles promoted synergistic tumor suppression. Biomaterials 34 15 3912-23.

  • Yonar M.E. Sakin F. (2011): Ameliorative effect of lycopene on antioxidant status in Cyprinus carpio during pyrethroid deltamethrin exposure. Pesticide Biochemistry and Physiology 99 226-231.

  • Yoon S. Han M. Kim J. Chang I. Kim H. Chung J. Shin B. (2011): Protective effects of chitosan oligosaccharide on paraquat-induced nephrotoxicity in rats. Food and Chemical Toxicology 49 8 1828-1833.

Journal information
Impact Factor

CiteScore 2018: 0.84

SCImago Journal Rank (SJR) 2018: 0.195
Source Normalized Impact per Paper (SNIP) 2018: 0.772

Cited By
All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 233 106 5
PDF Downloads 93 58 3