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Histopathological and Biochemical Effects of Humic Acid Against Cadmium Toxicity in Brown Trout Gills and Muscles

Year 2013, Volume: 13 Issue: 2, - , 01.04.2013
https://doi.org/10.4194/1303-2712-v13_2_13

Abstract

It was biochemically and histopathologically investigated whether humic acid (HA) has protective effects on cadmium (Cd) toxicity on muscle and gills of brown trout (Salmo trutta fario Linnaeus, 1792). The brown trout were exposed to cadmium (2 ppm) and/or humic acid (5 ppm). For this purpose, levels of glutathione peroxidase (GPx), superoxide dismutase (SOD), malondialdehyde (MDA) was investigated in muscle and gills tissues of brown trout. The activities of GPx and SOD in the tissues of fish exposed to Cd was significantly lower than the control groups (P<0.05). MDA levels did not increase in the groups exposed to cadmium (P>0.05). Hovewer, humic acid did not affect biochemical damage in cadmium group. Cd caused a significant increase in histopathological changes in muscle and gills tissues, but histopathological changes were lower in the muscle tissue of Cd+HA group. These results suggest that humic acid may counteract the cadmium toxicity in muscles tissue in histopathologic aspect.

References

  • Alak, G., Atamanalp, M., Topal, A., Arslan, H., Kocaman, E.M., Oruç, E. 2013. Effect of sub-lethal lead toxicity on the histopathological and antioxidant enzyme activity of rainbow trout (Oncorhynchus mykiss). Fresenius Environmental Bulletin, 22: 733-738.
  • Allen, P. 1995. Chronic accumulation of cadmium in the edible tissues of Oreochromis aureus (Steindachner): modification by mercury and lead. Archives of Environmental Contamination and Toxicology, 29: 814
  • Amdur, M.O., Doull, J., Curtis, M.D. and Kloasen, C.D. 19 Cassarett and Doull's Toxicology. Pergamon, New York/Oxford Anderson, D. 1996. Antioxidant defences against reactive oxygen species causing genetic and other damage. Mutation Research, 350: 103-108
  • Andersson, C., Abrahamson, A., Brunstrom, B. and Orberg, J. 2010. Impact of humic substances on EROD activity in gill and liver of three-spined sticklebacks (Gasterosteus aculeatus). Chemosphere, 81: 156-160. Ates, B., Orun, I., Talas, Z.S., Durmaz, G. and Yilmaz, I. 200 Effects of sodium selenite on some biochemical and hematological parameters of rainbow trout (Oncorhynchus mykiss Walbaum, 1792) exposed to Pb 2+ and Cu 2+ . Fish Physiology Biochemistry, 34:53
  • Aydın, A., Alak, G., Kocaman, E.M. and Atamanalp, M. 20 Effects of Carboxin on Glutathione-STransferase Enzyme Activite in Rainbow Trout (Oncorhynchus mykiss). Journal of Animal and Veterinary Advances, 11(15): 2716-2720.
  • Besirovic, H., Alic, A., Prasovic, S., Drommer W. 2010. Histopathological Effects of Chronic Exposure to Cadmium and Zinc on Kidneys and Gills of Brown Trout (Salmo trutta fario) Turkish Journal of Fisheries and Aquatic Sciences, 10: 255-262.
  • Bingöl, S.A. and Kocamiş, H., 2010. The Gene Expression Profile by RT-PCR and Immunohistochemical Expression Pattern of Catalase in the Kidney Tissue of Both Healthy and Diabetic Mice. Kafkas Univ Vet Fak Derg, 16 (5): 825-834, Bradford, M.M. 1976. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochemistry, 72: 248-254.
  • Cankaya, M., Hernandez, A.M., Ciftci, M., Beydemir, S., Ozdemir, H., Budak, H., Gulcin, I., Comakli, V., Emircupani, T., Ekinci, D., Kuzu, M., Jiang, O., Eichele, G. and Kufrevioglu, O.I. 2007. An analysis of expression patterns of genes encoding proteins with catalytic activities. Genomics, 8: 232-248.
  • Ceyhun, S.B., Şenturk, M., Ekinci, D., Erdogan, O., Ciltas, A. and Kocaman, E.M. 2010. Deltamethrin attenuates antioxidant defense system and induces the expression of heat shock protein 70 in rainbow trout. Comparative Biochemistry and Physiology, 152: 2152
  • Ceyhun, S., Şenturk, M., Yerlikaya, E., Erdogan, O. and Kufrevioglu, O. 20 Purification and characterization of carbonic anhydrase from the teleost fish Dicentrarchus labrax (European Seabass) liver and toxicological effects of metals on enzyme activity. Environmental Toxicology and Pharmacology, 32: 69-74. Dabas, A., Nagpure, N.S., Kumar, R., Kushwaha, B., Kumar, P. and Lakra, W.S. 2012. Assessment of tissue-specific effect of cadmium on antioxidant defense system and lipid peroxidation in freshwater murrel, Channa punctatus. Fish Physiology Biochemistry, 38: 469-82.
  • Ekinci, D., Beydemir, S. and Alim, Z. 2007. Some drugs inhibit in vitro hydratase and esterase activities of human carbonic anhydrase - I and II. Pharmacology Reports, 59: 580- 587.
  • Ercal, N., Gurer-Orhan, H. and Aykin-Burns, N. 2001. Toxic metals and oxidative stress Part I: mechanisms involved in metal induced oxidative damage. Current topics in medicinal chemistry, 529-539
  • George, K.T. and Wright, J. 1996. Regulation of metallothionein in teleosts ce induction of MTmRNA and protein by cadmium in hepatic and extrahepatic tissues of a marine flatfish, the turbot (Scophthalmus maximus). Comparative Biochemistry and Physiology, 113: 109-115.
  • Gülcin, İ., Beydemir, Ş., Hisar, O., Koksal, E. and Reiter, R.J. 2009. Melatonin administration increases antioxidant enzymes activities and reduces lipid peroxidation in the rainbow trout (Oncorhynchus mykiss, Walbaum) erythrocytes. Turkish Journal of Veterinary and Animal Sciences, 33: 241-245.
  • Halliwell, B., Aeschbach, R., Loliger, J. and Aruoma, O.I. 19 The characterization of antioxidants. Food and Chemichcal Toxicology, 33: 601-617. Jana, S. and Bandopadhyaya, N. 1987. Effect of heavy metals on some biochemical parameters in the freshwater fish, Clarias punctatus. Environmental Ecology, 5: 488-493.
  • Islam, K.M.S., Schuhmacher, A. and Gropp, J.M. 2005. Humic acid substances in animal agriculture. Pakistan Journal of Nutrition, 4: 126-134.
  • Kamunde, C. and MacPhail, R. 2011. Effect of humic acid during concurrent chronic waterborne exposure of rainbow trout (Oncorhynchus mykiss) to copper, cadmium and zinc. Ecotoxicology Environmental Safety, 74: 259-269.
  • Karadeniz, A., Cemek, M. and Simsek, N. 2009. The effects of Panax ginseng and Spirulina platensis on hepatotoxicity induced by cadmium in rats. Ecotoxicol Environ Saf, 72: 231-235.
  • Kumar, P. and Singh, A. 2010. Cadmium toxicity in fish: An overview. GERF Bulletin of Biosciences December 1: 41-47
  • Lacroix, A. and Hontela, A. 2004. A comparative assessment of the adrenotoxic effects of cadmium in two teleost species, rainbow trout, Oncorhynchus mykiss, and yellow perch, Perca flavescens. Aquatic Toxicology, 67: 13-21.
  • Liu, X.J., Luo, Z., Li, C.H., Xiong, B.X., Zhao, Y.H. and Li ,X.D. 20 Antioxidant responses, hepatic intermediary metabolism, histology and ultrastructure in Synechogobius hasta exposed to water borne cadmium. Ecotoxicology and Environmental Safety, 74: 1156-1163.
  • Ognjanovic, B.I., Markovic, S.D., Pavlovic, S.Z., Zikic, R.V., Stajn, A.S. and Saicic, Z.S. 2008. Effect of chronic cadmium exposure on antioxidant defense system in some tissues of rats: protective effect of selenium. Physiological Research, 57: 403-411.
  • Okocha, R.C. and Adedeji, O.B. 2011. Overview of Cadmium Toxicity in Fish. Journal of Applied Sciences Research, 7: 1195-1207.
  • Oner, G., Senturk, U.K. and Izgut, U.N. 1995. The role of cadmium in the peroxidative response of kidney to stress. Biological Trace Element Research, 48: 111
  • Presnell, J. and Schreibman, M.P. 1997. Animal Tissue. Tissue Techniques. London. The Johns Hopkins University Pres Ltd. 5th ed. 269-271.
  • Pruell, R.J. and Engelhardt, F.R. 1980. Liver cadmium uptake, catalase inhibition and cadmium thionein production in the killifish Fundulus heteroclitus. Induced by experimental cadmium exposure. Marine Environment Research, 3: 101-111.
  • Pruski, A.M. and Dixon, D.R. 2002. Effects of cadmium on nuclear integrity and DNA repair efficiency in the gill cells of Mytilus edulis L. Aquatic Toxicology, 57: 127-1
  • Rath, N.C., Huff, W.E. and Huff, G.R. 2006. Effects of Humic Acid on Broiler Chickens. Poultry Science, 85: 410-4
  • Remyla, S.R., Ramesh, M., Sajwan, K.S. and Kumar, K.S. 200 Influence of zinc on cadmium induced haematological and biochemical responses in a freshwater teleost fish Catla catla. Fish Physiology Biochemistry, 34: 169-174. Senapati, S.K., Dey, S., Dwivedi, S.K. and Swarup, D. 200 Effect of garlic (Allium sativum L.) extract on tissue lead level in rats. Journal of Ethnopharmacology, 76: 229-232 Stajn, A., Zikic, R.V., Ognjanovic , B., Saicic, Z.S., Pavlovic, S.Z., Kostic, M.M. and Petrovic, V.M. 19 Effect of cadmium and selenium on the antioxidant defense system in rat kidneys. Comparative Biochemistry and Physiology, 117: 1671
  • Talas, Z.S., Orun, I., Ozdemir, I., Erdogan, K., Alkan, A. and Yilmaz, I. 2008. Antioxidative role of selenium against the toxic effect of heavy metals (Cd +2 , Cr +3 ) on liver of rainbow trout (Oncorhynchus mykiss Walbaum 1792). Fish Physiology Biochemistry, 34: 217- 222. Thophon, S., Kruatrachue, M., Upatham, E.S., Pokethitiyook, P., Sahaphong, S. and Jaritkhuan, S. 200 Histopathological alterations of white seabass, Lates calcalifer, in acute and subchronic cadmium exposure. Environmental Pollution, 121: 307-320.
  • Yilmaz, M., Ersan, Y., Koc, E., Ozen, H. and Karaman, M. 20 Toxic effects of cadmium sulphate on tissue histopathology and serum protein expression in european chub, Leuciscus cephalus (Linnaeus, 1758). Kafkas Universitesi Veteriner Fakultesi Dergisi, 17: 131-1
  • Zikic, V., Stajn, A.S., Ognjanovic, B.V., Pavlovic, Z.S. and Saicic, Z.S. 1997. Activities of superoxide dismutase and catalase in erythrocytes and transaminases in the plasma of carps (Cyprinus carpio L.) exposed to cadmium. Physiological Research, 46: 391-396.
  • Wiegand, C., Krause, E., Steinberg, C. and Pflugmacher, S. 200 Toxicokinetics of atrazine in embryos of the zebrafish (Danio rerio). Ecotoxicology Environmental Safety, 49: 199-205. Winner, R.W. 1984. The toxicity and bioaccumulation of cadmium and copper as affected by humic acid. Aquatic Toxicology, 5: 267-2.
  • Wong, C.K., Wong, M.H. 2000. Morphological and biochemical changes in the gills of Tilapia (Oreochromis mossambicus) to ambient cadmium exposure. Aquatic Toxicology, 48: 517-527.

Histopathological and Biochemical Effects of Humic Acid Against Cadmium Toxicity in Brown Trout Gills and Muscles

Year 2013, Volume: 13 Issue: 2, - , 01.04.2013
https://doi.org/10.4194/1303-2712-v13_2_13

Abstract

Kadmiyum toksisitesine karşı humik asitin koruyucu etkisi biyokimyasal ve histopatolojik olarak kahverengi alabalık (Salmo trutta fario Linnaeus, 1792) solungaç ve kas dokularında araştırılmıştır. Balıklar kadmiyum ve/veya humik asite (2ppm Cd, 5 ppm humik asit) maruz bırakılmışlardır. Bu amaçla kahverengi alabalıkların kas ve solungaç dokularında glutatyon peroksidaz (GPX ), süperoksit dismutaz (SOD), malondialdehit (MDA) düzeyleri incelenmiştir. Cd’a maruz kalan gruplarda GPX ve SOD enzim aktiviteleri kontrol grubuna kıyasla düşük değerler vermiştir (P<0.05). MDA seviyesi kadmiyuma maruz kalan gruplarda artmamıştır (P>0.05). Bununla beraber kadmiyum uygulanan gruplarda humik asit biyokimyasal zararı önlemede etkili olmamıştır. Cd kas ve solungaç dokularında histopatolojik olarak önemli artışlara neden olurken, Cd+HA’in birlikte uygulandığı grupta kas dokusu daha az etkilenmiştir. Bu sonuçlara göre, humik asit kas dokusunda histopatolojik olarak koruyucu etki gösterebilir

References

  • Alak, G., Atamanalp, M., Topal, A., Arslan, H., Kocaman, E.M., Oruç, E. 2013. Effect of sub-lethal lead toxicity on the histopathological and antioxidant enzyme activity of rainbow trout (Oncorhynchus mykiss). Fresenius Environmental Bulletin, 22: 733-738.
  • Allen, P. 1995. Chronic accumulation of cadmium in the edible tissues of Oreochromis aureus (Steindachner): modification by mercury and lead. Archives of Environmental Contamination and Toxicology, 29: 814
  • Amdur, M.O., Doull, J., Curtis, M.D. and Kloasen, C.D. 19 Cassarett and Doull's Toxicology. Pergamon, New York/Oxford Anderson, D. 1996. Antioxidant defences against reactive oxygen species causing genetic and other damage. Mutation Research, 350: 103-108
  • Andersson, C., Abrahamson, A., Brunstrom, B. and Orberg, J. 2010. Impact of humic substances on EROD activity in gill and liver of three-spined sticklebacks (Gasterosteus aculeatus). Chemosphere, 81: 156-160. Ates, B., Orun, I., Talas, Z.S., Durmaz, G. and Yilmaz, I. 200 Effects of sodium selenite on some biochemical and hematological parameters of rainbow trout (Oncorhynchus mykiss Walbaum, 1792) exposed to Pb 2+ and Cu 2+ . Fish Physiology Biochemistry, 34:53
  • Aydın, A., Alak, G., Kocaman, E.M. and Atamanalp, M. 20 Effects of Carboxin on Glutathione-STransferase Enzyme Activite in Rainbow Trout (Oncorhynchus mykiss). Journal of Animal and Veterinary Advances, 11(15): 2716-2720.
  • Besirovic, H., Alic, A., Prasovic, S., Drommer W. 2010. Histopathological Effects of Chronic Exposure to Cadmium and Zinc on Kidneys and Gills of Brown Trout (Salmo trutta fario) Turkish Journal of Fisheries and Aquatic Sciences, 10: 255-262.
  • Bingöl, S.A. and Kocamiş, H., 2010. The Gene Expression Profile by RT-PCR and Immunohistochemical Expression Pattern of Catalase in the Kidney Tissue of Both Healthy and Diabetic Mice. Kafkas Univ Vet Fak Derg, 16 (5): 825-834, Bradford, M.M. 1976. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochemistry, 72: 248-254.
  • Cankaya, M., Hernandez, A.M., Ciftci, M., Beydemir, S., Ozdemir, H., Budak, H., Gulcin, I., Comakli, V., Emircupani, T., Ekinci, D., Kuzu, M., Jiang, O., Eichele, G. and Kufrevioglu, O.I. 2007. An analysis of expression patterns of genes encoding proteins with catalytic activities. Genomics, 8: 232-248.
  • Ceyhun, S.B., Şenturk, M., Ekinci, D., Erdogan, O., Ciltas, A. and Kocaman, E.M. 2010. Deltamethrin attenuates antioxidant defense system and induces the expression of heat shock protein 70 in rainbow trout. Comparative Biochemistry and Physiology, 152: 2152
  • Ceyhun, S., Şenturk, M., Yerlikaya, E., Erdogan, O. and Kufrevioglu, O. 20 Purification and characterization of carbonic anhydrase from the teleost fish Dicentrarchus labrax (European Seabass) liver and toxicological effects of metals on enzyme activity. Environmental Toxicology and Pharmacology, 32: 69-74. Dabas, A., Nagpure, N.S., Kumar, R., Kushwaha, B., Kumar, P. and Lakra, W.S. 2012. Assessment of tissue-specific effect of cadmium on antioxidant defense system and lipid peroxidation in freshwater murrel, Channa punctatus. Fish Physiology Biochemistry, 38: 469-82.
  • Ekinci, D., Beydemir, S. and Alim, Z. 2007. Some drugs inhibit in vitro hydratase and esterase activities of human carbonic anhydrase - I and II. Pharmacology Reports, 59: 580- 587.
  • Ercal, N., Gurer-Orhan, H. and Aykin-Burns, N. 2001. Toxic metals and oxidative stress Part I: mechanisms involved in metal induced oxidative damage. Current topics in medicinal chemistry, 529-539
  • George, K.T. and Wright, J. 1996. Regulation of metallothionein in teleosts ce induction of MTmRNA and protein by cadmium in hepatic and extrahepatic tissues of a marine flatfish, the turbot (Scophthalmus maximus). Comparative Biochemistry and Physiology, 113: 109-115.
  • Gülcin, İ., Beydemir, Ş., Hisar, O., Koksal, E. and Reiter, R.J. 2009. Melatonin administration increases antioxidant enzymes activities and reduces lipid peroxidation in the rainbow trout (Oncorhynchus mykiss, Walbaum) erythrocytes. Turkish Journal of Veterinary and Animal Sciences, 33: 241-245.
  • Halliwell, B., Aeschbach, R., Loliger, J. and Aruoma, O.I. 19 The characterization of antioxidants. Food and Chemichcal Toxicology, 33: 601-617. Jana, S. and Bandopadhyaya, N. 1987. Effect of heavy metals on some biochemical parameters in the freshwater fish, Clarias punctatus. Environmental Ecology, 5: 488-493.
  • Islam, K.M.S., Schuhmacher, A. and Gropp, J.M. 2005. Humic acid substances in animal agriculture. Pakistan Journal of Nutrition, 4: 126-134.
  • Kamunde, C. and MacPhail, R. 2011. Effect of humic acid during concurrent chronic waterborne exposure of rainbow trout (Oncorhynchus mykiss) to copper, cadmium and zinc. Ecotoxicology Environmental Safety, 74: 259-269.
  • Karadeniz, A., Cemek, M. and Simsek, N. 2009. The effects of Panax ginseng and Spirulina platensis on hepatotoxicity induced by cadmium in rats. Ecotoxicol Environ Saf, 72: 231-235.
  • Kumar, P. and Singh, A. 2010. Cadmium toxicity in fish: An overview. GERF Bulletin of Biosciences December 1: 41-47
  • Lacroix, A. and Hontela, A. 2004. A comparative assessment of the adrenotoxic effects of cadmium in two teleost species, rainbow trout, Oncorhynchus mykiss, and yellow perch, Perca flavescens. Aquatic Toxicology, 67: 13-21.
  • Liu, X.J., Luo, Z., Li, C.H., Xiong, B.X., Zhao, Y.H. and Li ,X.D. 20 Antioxidant responses, hepatic intermediary metabolism, histology and ultrastructure in Synechogobius hasta exposed to water borne cadmium. Ecotoxicology and Environmental Safety, 74: 1156-1163.
  • Ognjanovic, B.I., Markovic, S.D., Pavlovic, S.Z., Zikic, R.V., Stajn, A.S. and Saicic, Z.S. 2008. Effect of chronic cadmium exposure on antioxidant defense system in some tissues of rats: protective effect of selenium. Physiological Research, 57: 403-411.
  • Okocha, R.C. and Adedeji, O.B. 2011. Overview of Cadmium Toxicity in Fish. Journal of Applied Sciences Research, 7: 1195-1207.
  • Oner, G., Senturk, U.K. and Izgut, U.N. 1995. The role of cadmium in the peroxidative response of kidney to stress. Biological Trace Element Research, 48: 111
  • Presnell, J. and Schreibman, M.P. 1997. Animal Tissue. Tissue Techniques. London. The Johns Hopkins University Pres Ltd. 5th ed. 269-271.
  • Pruell, R.J. and Engelhardt, F.R. 1980. Liver cadmium uptake, catalase inhibition and cadmium thionein production in the killifish Fundulus heteroclitus. Induced by experimental cadmium exposure. Marine Environment Research, 3: 101-111.
  • Pruski, A.M. and Dixon, D.R. 2002. Effects of cadmium on nuclear integrity and DNA repair efficiency in the gill cells of Mytilus edulis L. Aquatic Toxicology, 57: 127-1
  • Rath, N.C., Huff, W.E. and Huff, G.R. 2006. Effects of Humic Acid on Broiler Chickens. Poultry Science, 85: 410-4
  • Remyla, S.R., Ramesh, M., Sajwan, K.S. and Kumar, K.S. 200 Influence of zinc on cadmium induced haematological and biochemical responses in a freshwater teleost fish Catla catla. Fish Physiology Biochemistry, 34: 169-174. Senapati, S.K., Dey, S., Dwivedi, S.K. and Swarup, D. 200 Effect of garlic (Allium sativum L.) extract on tissue lead level in rats. Journal of Ethnopharmacology, 76: 229-232 Stajn, A., Zikic, R.V., Ognjanovic , B., Saicic, Z.S., Pavlovic, S.Z., Kostic, M.M. and Petrovic, V.M. 19 Effect of cadmium and selenium on the antioxidant defense system in rat kidneys. Comparative Biochemistry and Physiology, 117: 1671
  • Talas, Z.S., Orun, I., Ozdemir, I., Erdogan, K., Alkan, A. and Yilmaz, I. 2008. Antioxidative role of selenium against the toxic effect of heavy metals (Cd +2 , Cr +3 ) on liver of rainbow trout (Oncorhynchus mykiss Walbaum 1792). Fish Physiology Biochemistry, 34: 217- 222. Thophon, S., Kruatrachue, M., Upatham, E.S., Pokethitiyook, P., Sahaphong, S. and Jaritkhuan, S. 200 Histopathological alterations of white seabass, Lates calcalifer, in acute and subchronic cadmium exposure. Environmental Pollution, 121: 307-320.
  • Yilmaz, M., Ersan, Y., Koc, E., Ozen, H. and Karaman, M. 20 Toxic effects of cadmium sulphate on tissue histopathology and serum protein expression in european chub, Leuciscus cephalus (Linnaeus, 1758). Kafkas Universitesi Veteriner Fakultesi Dergisi, 17: 131-1
  • Zikic, V., Stajn, A.S., Ognjanovic, B.V., Pavlovic, Z.S. and Saicic, Z.S. 1997. Activities of superoxide dismutase and catalase in erythrocytes and transaminases in the plasma of carps (Cyprinus carpio L.) exposed to cadmium. Physiological Research, 46: 391-396.
  • Wiegand, C., Krause, E., Steinberg, C. and Pflugmacher, S. 200 Toxicokinetics of atrazine in embryos of the zebrafish (Danio rerio). Ecotoxicology Environmental Safety, 49: 199-205. Winner, R.W. 1984. The toxicity and bioaccumulation of cadmium and copper as affected by humic acid. Aquatic Toxicology, 5: 267-2.
  • Wong, C.K., Wong, M.H. 2000. Morphological and biochemical changes in the gills of Tilapia (Oreochromis mossambicus) to ambient cadmium exposure. Aquatic Toxicology, 48: 517-527.
There are 34 citations in total.

Details

Primary Language Turkish
Journal Section Articles
Authors

Gonca Alak This is me

Muhammed Atamanalp This is me

Ahmet Topal This is me

Harun Arslan This is me

Ertan Oruç This is me

Publication Date April 1, 2013
Published in Issue Year 2013 Volume: 13 Issue: 2

Cite

APA Alak, G., Atamanalp, M., Topal, A., Arslan, H., et al. (2013). Histopathological and Biochemical Effects of Humic Acid Against Cadmium Toxicity in Brown Trout Gills and Muscles. Turkish Journal of Fisheries and Aquatic Sciences, 13(2). https://doi.org/10.4194/1303-2712-v13_2_13
AMA Alak G, Atamanalp M, Topal A, Arslan H, Oruç E. Histopathological and Biochemical Effects of Humic Acid Against Cadmium Toxicity in Brown Trout Gills and Muscles. Turkish Journal of Fisheries and Aquatic Sciences. April 2013;13(2). doi:10.4194/1303-2712-v13_2_13
Chicago Alak, Gonca, Muhammed Atamanalp, Ahmet Topal, Harun Arslan, and Ertan Oruç. “Histopathological and Biochemical Effects of Humic Acid Against Cadmium Toxicity in Brown Trout Gills and Muscles”. Turkish Journal of Fisheries and Aquatic Sciences 13, no. 2 (April 2013). https://doi.org/10.4194/1303-2712-v13_2_13.
EndNote Alak G, Atamanalp M, Topal A, Arslan H, Oruç E (April 1, 2013) Histopathological and Biochemical Effects of Humic Acid Against Cadmium Toxicity in Brown Trout Gills and Muscles. Turkish Journal of Fisheries and Aquatic Sciences 13 2
IEEE G. Alak, M. Atamanalp, A. Topal, H. Arslan, and E. Oruç, “Histopathological and Biochemical Effects of Humic Acid Against Cadmium Toxicity in Brown Trout Gills and Muscles”, Turkish Journal of Fisheries and Aquatic Sciences, vol. 13, no. 2, 2013, doi: 10.4194/1303-2712-v13_2_13.
ISNAD Alak, Gonca et al. “Histopathological and Biochemical Effects of Humic Acid Against Cadmium Toxicity in Brown Trout Gills and Muscles”. Turkish Journal of Fisheries and Aquatic Sciences 13/2 (April 2013). https://doi.org/10.4194/1303-2712-v13_2_13.
JAMA Alak G, Atamanalp M, Topal A, Arslan H, Oruç E. Histopathological and Biochemical Effects of Humic Acid Against Cadmium Toxicity in Brown Trout Gills and Muscles. Turkish Journal of Fisheries and Aquatic Sciences. 2013;13. doi:10.4194/1303-2712-v13_2_13.
MLA Alak, Gonca et al. “Histopathological and Biochemical Effects of Humic Acid Against Cadmium Toxicity in Brown Trout Gills and Muscles”. Turkish Journal of Fisheries and Aquatic Sciences, vol. 13, no. 2, 2013, doi:10.4194/1303-2712-v13_2_13.
Vancouver Alak G, Atamanalp M, Topal A, Arslan H, Oruç E. Histopathological and Biochemical Effects of Humic Acid Against Cadmium Toxicity in Brown Trout Gills and Muscles. Turkish Journal of Fisheries and Aquatic Sciences. 2013;13(2).