Oxidative stress biomarkers in different tissues of rainbow trout (Oncorhynchus mykiss) exposed to Disinfectant-CIP formulated with peracetic acid and hydrogen peroxide

Open access

Abstract

The aim of study was to determine the effects of exposure to the product DEZYNFEKTANT-CIP (Eng. - Disinfectant-CIP), which is formulated with peracetic acid and hydrogen peroxide, on oxidative stress biomarkers (lipid peroxidation (LPO) levels and the carbonyl content of oxidatively modified proteins) and antioxidant defenses (superoxide dismutase (SOD), catalase (CAT), glutathione reductase (GR), glutathione peroxidase (GPx), total antioxidant capacity) in muscle, gill, hepatic, and cardiac tissues of rainbow trout, Oncorhynchus mykiss (Walbaum). LPO and carbonyl contents changed with tissue type. Exposure to Disinfectant-CIP led to a significant decrease in LPO in muscle tissues and carbonyl content in muscle and gill tissues. The inhibition of SOD and CAT activity in muscle, hepatic, and cardiac tissues was observed probably because of increased oxidative stress during disinfection; however, hepatic and cardiac GPx activity increased in an attempt to counteract oxidative stress. We suggest that oxidative stress during the oxidation of peracetic acid and hydrogen peroxide could be counteracted by the antioxidant system in trout tissues. Correlative analysis between oxidative stress biomarkers and antioxidant defense confirms the pivotal role of SOD and CAT against CIP-induced oxidative stress

References

  • Adams M.B. Crosbie P.B.B. Nowak B.F. 2012 - Preliminary success using hydrogen peroxide to treat Atlantic salmon Salmo salar L. affected with experimentally induced amoebic gill disease (AGD) - J. Fish Dis. 35: 839-848.

  • Alasri A. Roques C. Michel G. Cabassud C. Aptel P. 1992 - Bactericidal properties of peracetic acid and hydrogen peroxide alone and in combination and chlorine and formaldehyde against bacterial water strains - Can. J. Microbiol. 38: 635-642

  • Alasri A. Valverde M. Roques C. Michel G. Cabassud C. Aptel P. 1993 - Sporocidal properties of peracetic acid and hydrogen peroxide alone and in combination in comparison with chlorine and formaldehyde for ultrafiltration membrane disinfection - Can. J. Microbiol. 39: 52-60.

  • Antonelli M. Rossi S. Mezzanotte V. Nurizzo C. 2006 - Secondary effluent disinfection: PAA long term efficiency - Environ. Sci. Technol. 40: 4771-4775.

  • Baldry M.G.C. 1983 - The bactericidal fungicidal and sporicidal properties of hydrogen peroxide and peracetic acid - J. Appl. Bacteriol. 54: 417-423.

  • Bradford M.M. 1976 - A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding - Anal. Biochem. 72: 248-254.

  • Chaudi_re J. Ferrari-Iliou R. 1999 - Intracellular antioxidants: from chemical to biochemical mechanisms - Food Chem. Toxicol. 37: 949-962.

  • Coyle C.H. Martinez L.J. Coleman M.C. Spitz D.R. Weintraub N.L. Kader K.N. 2006 - Mechanisms of H2O2-induced oxidative stress in endothelial cells - Free Radic. Biol. Med. 40: 2206-2213.

  • Dubinina E.E. Burmistrov S.O. Khodov D.A. Porotov I.G. 1995 - Oxidative modification of human serum proteins. A method of determining it - Vopr. Med. Khim. 41: 24-26 (in Russian with English abstract).

  • Ebert-Dumig R. Seufert J. Schneider D. Kohrle J. Schutze N. Jakob F. 1999 - Expression of selenoproteins in monocytes and macrophages - implicationen for immune system - Med. Klin. (Munich) 94: 29-34 (in German).

  • Elia A.C. Anastasi V. Dorr A.J. 2006 - Hepatic antioxidant enzymes and total glutathione of Cyprinus carpio exposed to three disinfectants chlorine dioxide sodium hypochlorite and peracetic acid for superficial water potabilization - Chemosphere 64: 1633-1641.

    • Crossref
  • Ferraris M. Chiesara E. Radice S. Giovara A. Frigerio S. Fumagalli R. Marabini L. 2005 - Study of potential toxic effects on rainbow trout hepatocytes of surface water treated with chlorine or alternative disinfectants - Chemosphere 60: 65-73.

  • Galaktionova L.P. Molchanov A.V. El’chaninova S.A. Varshavskii B.I. 1998 - Lipid peroxidation in patients with gastric and duodenal peptic ulcers - Klin. Lab. Diagn. 6: 10-14 (in Russian with English abstract) Gerard-Monnier D. Chaudiere J. 1996 - Metabolism and antioxidant function of glutathione - Pathol. Biol. 44: 77-85.

  • Glatzle D. Vuilleumier J.P. Weber F. Decker K. 1974 - Glutathione reductase test with whole blood a convenient procedure for the assessment of the riboflavin status in humans - Experientia 30: 665-667.

  • Grudniewska J. Dobosz S. 2007 - Use of Bronopol and Oxim treatments during incubations rainbow trout eggs - In: XII European Congress of Ichthyology Book of abstract 9-13 September 2007 Cavtat (Dubrovnik) Croatia: 92-93.

  • Grudniewska J. Terech-Majewska E. Goral C. 2008. - Evaluate the efficacy of the biocidal product in the hatchery during egg incubation and prophylactic bathing rainbow trout (Oncorhynchus mykiss) fry - In: Biotechnology in aquaculture (Eds) Z. Zakeoe J. Wolnicki K.

  • Demska-Zakeoe R. Kaminski Wyd. IRS Olsztyn: 395-401 (in Polish).

  • Grudniewska J. Terech-Majewska E. Kazun B. Dyszkiewicz L. Olszewski A. 2007 - The use of acid biocidal product in the hatchery and rearing of salmonids - Komun. Ryb. 5: 11-15 (in Polish) Halliwell B. Gutteridge J.M.C. 2007 - Free Radicals in Biology and Medicine 4th Ed. - Oxford University Press New York.

  • Hebert N. Gagne F. Cejka P. Bouchard B. Hausler R. Cyr D.G. Blaise C. Fournier M. 2008 - Effects of ozone ultraviolet and peracetic acid disinfection of a primary- treated municipal effluent on the immune system of rainbow trout (Oncorhynchus mykiss) - Comp. Biochem. Physiol. C Toxicol. Pharmacol. 148: 122-127.

  • Jussila J. Makkonen J. Kokko H. 2011 - Peracetic acid (PAA) treatment is an effective disinfectant against crayfish plague (Aphanomyces astaci) spores in aquaculture - Aquaculture 320: 37-42.

  • Kamyshnikov V.S. 2004 - Reference book on clinic and biochemical researches and laboratory diagnostics - MEDpress-inform Moscow (in Russian).

  • Kitis M. 2004 - Disinfection of wastewater with peracetic acid: a review - Environ. Int. 30: 47-55.

  • Koroliuk M.A. Ivanova L.I. Maiorova I.G. Tokarev V.E. 1988 - A method of determining catalase activity - Lab. Delo. 1: 16-19.

  • Kostiuk V.A. Potapovich A.I. Kovaleva Zh.V. 1990 - A simple and sensitive method of determination of superoxide dismutase activity based on the reaction of quercetin oxidation - Vopr. Med. Khim. 36: 88-91.

  • Levine R.L. Garland D. Oliver C.N. Amici A. Climent I. Lenz A.G. Ahn B.W. Shaltiel S. Stadtman E.R. 1990 - Determination of carbonyl content in oxidatively modified proteins - Methods Enzymol. 186: 464-478.

  • Liberti L. Notarnicola M. 1999 - Advanced treatment and disinfection for municipal wastewater reuse in agriculture - Water Sci. Technol. 40: 235-245.

  • Mansell B. Powell M.D. Ernst I. Nowak B.F. 2005 - Effects of the gill monogenean Zeuxapta seriolae (Meserve 1938) and treatment with hydrogen peroxide on pathophysiology of kingfish Seriola lalandi Valenciennes 1833 - J. Fish Dis. 28: 253-262. 218 Halyna Tkachenko et al.

  • Marabini L. Frigerio S. Chiesara E. Radice S. 2006 - Toxicity evaluation of surface water treated with different disinfectants in HepG2 cells - Water Res. 40: 267-272.

  • Marjani A. Golalipour M.J. Gharravi A.M. 2010 - The effects of subacute exposure of peracetic acid on lipid peroxidation and hepatic enzymes in Wistar rats - Oman Med. J. 25: 256-260.

  • McAndrew K.J. Sommerville C. Wootten R. Bron J.E. 1998 - The effects of hydrogen peroxide treatment on different life-cycle stages of the salmon louse Lepeophtheirus salmonis (Kr_yer 1837) - J. Fish Dis. 21: 221-228.

  • Meister A. 1994 - The glutathione-ascorbic acid antioxidant systems in animal - J. Biol. Chem. 269: 9397-9400.

  • Moin V.M. 1986 - A simple and specific method for determining glutathione peroxidase activity in erythrocytes - Lab.Delo. 12: 724-727.

  • Picon-Camacho S.M. Marcos-Lopez M. Bron J.E. Shinn A.P. 2012 - An assessment of the use of drug and non-drug interventions in the treatment of Ichthyophthirius multifiliis Fouquet 1876 a protozoan parasite of freshwater fish - Parasitology 139: 149-190.

  • Ross S.W. Dalton D.A. Kramer S. Christensen B.L. 2001 - Physiological (antioxidant) responses of estuarine fishes to variability in dissolved oxygen - Comp. Biochem. Physiol. C Toxicol. Pharmacol. 130: 289-303.

  • Rudd T. Hopkinson L.M. 1989 - Comparison of disinfection techniques for sewage and sewage effluents - J. Inst. Water Environ. Manag. 3: 612-618.

  • Russo R. Curtis E.W. Yanong R.P. 2007 - Preliminary investigations of hydrogen peroxide treatment of selected ornamental fishes and efficacy against external bacteria and parasites in green swordtails - J. Aquat. Anim. Health 19: 121-127.

  • Santos C.X.C. Anilkumar N. Zhang M. Brewer A.C. Shah A.M. 2011 - Redox signaling in cardiac myocytes - Free Rad. Biol. Med. 50: 777-793.

  • Sies H. 1997 - Oxidative stress: oxidants and antioxidants - Exp. Physiol. 82: 291-295.

  • Srikanth K. Pereira E. Duarte A.C. Ahmad I. 2013 - Glutathione and its dependent enzymes’ modulatory responses to toxic metals and metalloids in fish - a review - Environ. Sci. Pollut. Res. 20: 2133-2149.

  • Stone J. R. Yang S. 2006 - Hydrogen peroxide: a signaling messenger - Antioxid. Redox Signal. 8: 243-270.

  • Straus D.L. Meinelt T. 2009 - Acute toxicity of peracetic acid (PAA) formulations to Ichthyophthirius multifiliis theronts - Parasitol. Res. 104: 1237-1241.

  • Straus D.L. Meinelt T. Farmer B.D. Mitchell A.J. 2012 - Peracetic acid is effective for controlling fungus on channel catfish eggs - J. Fish Dis. 35: 505-511.

  • Van der Oost R. Beyer J. Vermeulen N.P. 2003 - Fish bioaccumulation and biomarkers in environmental risk assessment: a review - Environ. Toxicol. Pharmacol. 13: 57-149.

  • Van Kuijk F.J.G.M. Sevanian A. Handelman G.J. Dratz E.A. 1987 - A new role for phosholipase A2: protection of membranes from lipid peroxidation damage - TIBS 12: 31-34.

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

  • Wilhelm Filho D. 2007 - Reactive oxygen species antioxidants and fish mitochondria - Front. Biosci. 12: 1229-1237.

  • Yim M.B. Chock P.B. Stadtman E.R. 1990 - Copper zinc superoxide dismutase catalyzes hydroxyl radical production from hydrogen peroxide - Proc. Natl. Acad. Sci. USA 87: 5006-5010.

  • Yin X. Zheng Y. Liu Q. Cai J. Cai L. 2012 - Cardiac response to chronic intermittent hypoxia with a transition from adaptation to maladaptation: the role of hydrogen peroxide - Oxid. Med. Cell Longev. Article ID: 569520 doi: 10.1155/2012/569520.

    • Crossref
  • Zar J.H. 1999 - Biostatistical Analysis - Prentice-Hall Inc. Englewood Cliffs New Jersey.

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  • Adams M.B. Crosbie P.B.B. Nowak B.F. 2012 - Preliminary success using hydrogen peroxide to treat Atlantic salmon Salmo salar L. affected with experimentally induced amoebic gill disease (AGD) - J. Fish Dis. 35: 839-848.

  • Alasri A. Roques C. Michel G. Cabassud C. Aptel P. 1992 - Bactericidal properties of peracetic acid and hydrogen peroxide alone and in combination and chlorine and formaldehyde against bacterial water strains - Can. J. Microbiol. 38: 635-642

  • Alasri A. Valverde M. Roques C. Michel G. Cabassud C. Aptel P. 1993 - Sporocidal properties of peracetic acid and hydrogen peroxide alone and in combination in comparison with chlorine and formaldehyde for ultrafiltration membrane disinfection - Can. J. Microbiol. 39: 52-60.

  • Antonelli M. Rossi S. Mezzanotte V. Nurizzo C. 2006 - Secondary effluent disinfection: PAA long term efficiency - Environ. Sci. Technol. 40: 4771-4775.

  • Baldry M.G.C. 1983 - The bactericidal fungicidal and sporicidal properties of hydrogen peroxide and peracetic acid - J. Appl. Bacteriol. 54: 417-423.

  • Bradford M.M. 1976 - A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding - Anal. Biochem. 72: 248-254.

  • Chaudi_re J. Ferrari-Iliou R. 1999 - Intracellular antioxidants: from chemical to biochemical mechanisms - Food Chem. Toxicol. 37: 949-962.

  • Coyle C.H. Martinez L.J. Coleman M.C. Spitz D.R. Weintraub N.L. Kader K.N. 2006 - Mechanisms of H2O2-induced oxidative stress in endothelial cells - Free Radic. Biol. Med. 40: 2206-2213.

  • Dubinina E.E. Burmistrov S.O. Khodov D.A. Porotov I.G. 1995 - Oxidative modification of human serum proteins. A method of determining it - Vopr. Med. Khim. 41: 24-26 (in Russian with English abstract).

  • Ebert-Dumig R. Seufert J. Schneider D. Kohrle J. Schutze N. Jakob F. 1999 - Expression of selenoproteins in monocytes and macrophages - implicationen for immune system - Med. Klin. (Munich) 94: 29-34 (in German).

  • Elia A.C. Anastasi V. Dorr A.J. 2006 - Hepatic antioxidant enzymes and total glutathione of Cyprinus carpio exposed to three disinfectants chlorine dioxide sodium hypochlorite and peracetic acid for superficial water potabilization - Chemosphere 64: 1633-1641.

    • Crossref
  • Ferraris M. Chiesara E. Radice S. Giovara A. Frigerio S. Fumagalli R. Marabini L. 2005 - Study of potential toxic effects on rainbow trout hepatocytes of surface water treated with chlorine or alternative disinfectants - Chemosphere 60: 65-73.

  • Galaktionova L.P. Molchanov A.V. El’chaninova S.A. Varshavskii B.I. 1998 - Lipid peroxidation in patients with gastric and duodenal peptic ulcers - Klin. Lab. Diagn. 6: 10-14 (in Russian with English abstract) Gerard-Monnier D. Chaudiere J. 1996 - Metabolism and antioxidant function of glutathione - Pathol. Biol. 44: 77-85.

  • Glatzle D. Vuilleumier J.P. Weber F. Decker K. 1974 - Glutathione reductase test with whole blood a convenient procedure for the assessment of the riboflavin status in humans - Experientia 30: 665-667.

  • Grudniewska J. Dobosz S. 2007 - Use of Bronopol and Oxim treatments during incubations rainbow trout eggs - In: XII European Congress of Ichthyology Book of abstract 9-13 September 2007 Cavtat (Dubrovnik) Croatia: 92-93.

  • Grudniewska J. Terech-Majewska E. Goral C. 2008. - Evaluate the efficacy of the biocidal product in the hatchery during egg incubation and prophylactic bathing rainbow trout (Oncorhynchus mykiss) fry - In: Biotechnology in aquaculture (Eds) Z. Zakeoe J. Wolnicki K.

  • Demska-Zakeoe R. Kaminski Wyd. IRS Olsztyn: 395-401 (in Polish).

  • Grudniewska J. Terech-Majewska E. Kazun B. Dyszkiewicz L. Olszewski A. 2007 - The use of acid biocidal product in the hatchery and rearing of salmonids - Komun. Ryb. 5: 11-15 (in Polish) Halliwell B. Gutteridge J.M.C. 2007 - Free Radicals in Biology and Medicine 4th Ed. - Oxford University Press New York.

  • Hebert N. Gagne F. Cejka P. Bouchard B. Hausler R. Cyr D.G. Blaise C. Fournier M. 2008 - Effects of ozone ultraviolet and peracetic acid disinfection of a primary- treated municipal effluent on the immune system of rainbow trout (Oncorhynchus mykiss) - Comp. Biochem. Physiol. C Toxicol. Pharmacol. 148: 122-127.

  • Jussila J. Makkonen J. Kokko H. 2011 - Peracetic acid (PAA) treatment is an effective disinfectant against crayfish plague (Aphanomyces astaci) spores in aquaculture - Aquaculture 320: 37-42.

  • Kamyshnikov V.S. 2004 - Reference book on clinic and biochemical researches and laboratory diagnostics - MEDpress-inform Moscow (in Russian).

  • Kitis M. 2004 - Disinfection of wastewater with peracetic acid: a review - Environ. Int. 30: 47-55.

  • Koroliuk M.A. Ivanova L.I. Maiorova I.G. Tokarev V.E. 1988 - A method of determining catalase activity - Lab. Delo. 1: 16-19.

  • Kostiuk V.A. Potapovich A.I. Kovaleva Zh.V. 1990 - A simple and sensitive method of determination of superoxide dismutase activity based on the reaction of quercetin oxidation - Vopr. Med. Khim. 36: 88-91.

  • Levine R.L. Garland D. Oliver C.N. Amici A. Climent I. Lenz A.G. Ahn B.W. Shaltiel S. Stadtman E.R. 1990 - Determination of carbonyl content in oxidatively modified proteins - Methods Enzymol. 186: 464-478.

  • Liberti L. Notarnicola M. 1999 - Advanced treatment and disinfection for municipal wastewater reuse in agriculture - Water Sci. Technol. 40: 235-245.

  • Mansell B. Powell M.D. Ernst I. Nowak B.F. 2005 - Effects of the gill monogenean Zeuxapta seriolae (Meserve 1938) and treatment with hydrogen peroxide on pathophysiology of kingfish Seriola lalandi Valenciennes 1833 - J. Fish Dis. 28: 253-262. 218 Halyna Tkachenko et al.

  • Marabini L. Frigerio S. Chiesara E. Radice S. 2006 - Toxicity evaluation of surface water treated with different disinfectants in HepG2 cells - Water Res. 40: 267-272.

  • Marjani A. Golalipour M.J. Gharravi A.M. 2010 - The effects of subacute exposure of peracetic acid on lipid peroxidation and hepatic enzymes in Wistar rats - Oman Med. J. 25: 256-260.

  • McAndrew K.J. Sommerville C. Wootten R. Bron J.E. 1998 - The effects of hydrogen peroxide treatment on different life-cycle stages of the salmon louse Lepeophtheirus salmonis (Kr_yer 1837) - J. Fish Dis. 21: 221-228.

  • Meister A. 1994 - The glutathione-ascorbic acid antioxidant systems in animal - J. Biol. Chem. 269: 9397-9400.

  • Moin V.M. 1986 - A simple and specific method for determining glutathione peroxidase activity in erythrocytes - Lab.Delo. 12: 724-727.

  • Picon-Camacho S.M. Marcos-Lopez M. Bron J.E. Shinn A.P. 2012 - An assessment of the use of drug and non-drug interventions in the treatment of Ichthyophthirius multifiliis Fouquet 1876 a protozoan parasite of freshwater fish - Parasitology 139: 149-190.

  • Ross S.W. Dalton D.A. Kramer S. Christensen B.L. 2001 - Physiological (antioxidant) responses of estuarine fishes to variability in dissolved oxygen - Comp. Biochem. Physiol. C Toxicol. Pharmacol. 130: 289-303.

  • Rudd T. Hopkinson L.M. 1989 - Comparison of disinfection techniques for sewage and sewage effluents - J. Inst. Water Environ. Manag. 3: 612-618.

  • Russo R. Curtis E.W. Yanong R.P. 2007 - Preliminary investigations of hydrogen peroxide treatment of selected ornamental fishes and efficacy against external bacteria and parasites in green swordtails - J. Aquat. Anim. Health 19: 121-127.

  • Santos C.X.C. Anilkumar N. Zhang M. Brewer A.C. Shah A.M. 2011 - Redox signaling in cardiac myocytes - Free Rad. Biol. Med. 50: 777-793.

  • Sies H. 1997 - Oxidative stress: oxidants and antioxidants - Exp. Physiol. 82: 291-295.

  • Srikanth K. Pereira E. Duarte A.C. Ahmad I. 2013 - Glutathione and its dependent enzymes’ modulatory responses to toxic metals and metalloids in fish - a review - Environ. Sci. Pollut. Res. 20: 2133-2149.

  • Stone J. R. Yang S. 2006 - Hydrogen peroxide: a signaling messenger - Antioxid. Redox Signal. 8: 243-270.

  • Straus D.L. Meinelt T. 2009 - Acute toxicity of peracetic acid (PAA) formulations to Ichthyophthirius multifiliis theronts - Parasitol. Res. 104: 1237-1241.

  • Straus D.L. Meinelt T. Farmer B.D. Mitchell A.J. 2012 - Peracetic acid is effective for controlling fungus on channel catfish eggs - J. Fish Dis. 35: 505-511.

  • Van der Oost R. Beyer J. Vermeulen N.P. 2003 - Fish bioaccumulation and biomarkers in environmental risk assessment: a review - Environ. Toxicol. Pharmacol. 13: 57-149.

  • Van Kuijk F.J.G.M. Sevanian A. Handelman G.J. Dratz E.A. 1987 - A new role for phosholipase A2: protection of membranes from lipid peroxidation damage - TIBS 12: 31-34.

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

  • Wilhelm Filho D. 2007 - Reactive oxygen species antioxidants and fish mitochondria - Front. Biosci. 12: 1229-1237.

  • Yim M.B. Chock P.B. Stadtman E.R. 1990 - Copper zinc superoxide dismutase catalyzes hydroxyl radical production from hydrogen peroxide - Proc. Natl. Acad. Sci. USA 87: 5006-5010.

  • Yin X. Zheng Y. Liu Q. Cai J. Cai L. 2012 - Cardiac response to chronic intermittent hypoxia with a transition from adaptation to maladaptation: the role of hydrogen peroxide - Oxid. Med. Cell Longev. Article ID: 569520 doi: 10.1155/2012/569520.

    • Crossref
  • Zar J.H. 1999 - Biostatistical Analysis - Prentice-Hall Inc. Englewood Cliffs New Jersey.

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