Induction of micronuclei in blood and histopathological alterations in gill, kidney and liver of Channa punctatus (Bloch, 1793) exposed to copper sulphate
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Abstract
Copper is one of the most toxic metals to fish and causes cytotoxic, mutagenic and carcinogenic effects. The accumulation of copper in an aquatic environment directly impacts man and the aquatic ecosystem. The present study aimed to determine the effect of copper sulphate (CuSO4) accumulation on the induction of micronuclei in blood and histological changes in kidney and liver of the fish Channa punctatus. The test chemical LC50 was determined after 96 hours during the first experiment. Later in the second experiment, the test animal was exposed to three sub-lethal concentrations of CuSO4 [0.1 mg/l (96 h-LC50/40), 0.2 mg/l (96 h-LC50/20) and 0.4 mg/l (96 h-LC50/10)]. Physico chemical parameters of the test medium, such as pH, temperature, hardness, alkalinity, and dissolved oxygen, were observed throughout the experiment, and all values were within the ranges necessary for the fish's survival. At intervals of 7, 14, 21, and 28 days, the control (without any test chemical) and copper sulphate exposed Groups' blood, liver, kidney, and gill tissues were taken to evaluate changes in genotoxic and histological parameters. Micronuclei (MN) induction and nuclear abnormalities (NAs) were observed at regular intervals. After 28 days, the MN frequency in Groups 1, 2, 3, and 4 was 0.78±0.006, 8.40±0.052, 10.37±0.098 and 10.90±0.024 respectively. A significant (P< 0.05) rise in MN frequencies and NAs indicated fish erythrocytes' DNA damage. Histological analysis of the liver, kidney, and gills revealed serious tissue injury such as necrosis, vacuolization, and degeneration after 28 days in the exposed Groups. The present study observed changes due to genotoxicity and histology, giving the most comprehensive understanding of CuSO4 stress on the fish C. punctatus and its risks to human health.
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Keywords
Channa punctatus, Copper, Micronuclei, Necrosis, Nuclear abnormalities
References
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Abdel-Latif, H. M., Dawood, M. A., Mahmoud, S. F., Shukry, M., Noreldin, A. E., Ghetas, H. A. & Khallaf, M. A. (2021). Copper oxide nanoparticles alter serum biochemical indices, induce histopathological alterations, and modulate transcription of cytokines, HSP70, and oxidative stress genes in Oreochromis niloticus. Animals, 11(3), 652. https://doi.org/10.3390/ani11030652
Aghamirkarimi, S., Mashinchian Moradi, A., Sharifpour, I., Jamili, S. & GhavamMostafavi, P. (2017). Sublethal effects of copper nanoparticles on the histology of gill, liver and kidney of the Caspian roach, Rutilus rutilus caspicus.Global Journal of Environmental Science and Management. DOI 10.22034/gjesm.2017.03.03.009Ale, A., Bacchetta, C., Rossi, A. S., Galdopórpora, J., Desimone, M. F., de la Torre, F. R., ... & Cazenave, J. (2018). Nanosilver toxicity in gills of a neotropical fish: Metal accumulation, oxidative stress, histopathology and other physiological effects. Ecotoxicology and Environmental Safety, 148, 976-984. https://doi.org/10.1016/j.ecoenv.2017.11.072Alimba, C. G. & Laide, A. W. (2019). Genotoxic and cytotoxic assessment of individual and composite mixture of cadmium, lead and manganese in Clarias gariepinus (Burchell 1822) using micronucleus assay. The Nucleus, 62(3), 191-202.https://doi.org/10.1007/s13237-019-00289-w
Anbumani, S. & Mohankumar, M. N. (2011). Nuclear and cytoplasmic abnormalities in the fish Catlacatla (Hamilton) exposed to chemicals and ionizing radiation. Research Journal of Environmental Sciences, 5(12), 867-877.
APHA, AWWA &WEF (2017). In: Rice EW, Baird RB, Eaton AD, Clesceri LS, editors. Standard methods for the examination of water and wastewater. 23rd ed. Washington, DC: APHA; 2017.
Canalejo, A., Diaz-de-Alba, M., Granado-Castro, M. D., Cordoba, F., Espada-Bellido, E., Galindo-Riaño, M. D. & Torronteras, R. (2016). Early genotoxic response and accumulation induced by waterborne copper, lead, and arsenic in European seabass, Dicentrarchuslabrax. Environmental Science and Pollution Research, 23, 3256-3266.https://doi.org/10.1007/s11356-015-5435-1
Chowdhary, P., Bharagava, R. N., Mishra, S. & Khan, N. (2020). Role of industries in water scarcity and its adverse effects on environment and human health. Environmental Concerns and Sustainable Development: Volume 1: Air, Water and Energy Resources, 235-256. https://doi.org/10.1007/978-981-13-5889-0_12
De Zwart, D., Adams, W., Galay Burgos, M., Hollender, J., Junghans, M., Merrington, G., ... & Williams, R. (2018). Aquatic exposures of chemical mixtures in urban environments: Approaches to impact assessment. Environmental Toxicology and Chemistry, 37(3), 703-714.https://doi.org/10.1002/etc.3975
Elalfy, M. M., Abomosallam, M. S., Sleem, F. & Elhadidy, M. (2021). Copper and copper containing pesticide as copper oxychloride toxicity and its adverse effects on animal and human health. MedicoResearch Chronicles, 8(2),89-98.https://doi.org/10.26838 MEDRECH. 2021.8.2. 486
Francisco, C. D. M., Bertolino, S. M., De Oliveira Junior, R. J., Morelli, S. & Pereira, B. B. (2019). Genotoxicity assessment of polluted urban streams using a native fish Astyanax altiparanae. Journal of Toxicology and Environmental Health, Part A, 82(8), 514-523. https://doi.org/10.1080/15287394.2019.1624235
Javed, M. & Usmani, N. (2019). An overview of the adverse effects of heavy metal contamination on fish health. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 89, 389-403.https://doi.org/10.1007/s40011-017-0875-7
Jomova, K., Makova, M., Alomar, S. Y., Alwasel, S. H., Nepovimova, E., Kuca, K., & Valko, M. (2022). Essential metals in health and disease. Chemico-biological interactions, 110173.)https://doi.org/10.1016/j.cbi.2022.110173
Karim, N. (2018). Copper and human health-a review. Journal of Bahria University Medical and Dental College, 8(2), 117-122.).
Kaur, S., Khera, K. S. & Kondal, J. K. (2018). Heavy metal induced histopathological alterations in liver, muscle and kidney of freshwater cyprinid, Labeorohita (Hamilton). Journal of Entomology and Zoology Studies, 6(2), 2137-2144.
Kumar, M., Gupta, N., Ratn, A., Awasthi, Y., Prasad, R., Trivedi, A. & Trivedi, S. P. (2020). Biomonitoring of heavy metals in river ganga water, sediments, plant, and fishes of different trophic levels. Biological trace element research, 193, 536-547.https://doi.org/10.1007/s12011-019-01736-0
Kumar, M., Kumar, P. & Devi, S. (2015). To study the histopathological changes in the gills of Clarias batrachus, an air-breathing teleost after short term exposure of copper sulphate. J Aquac Res Develop, 6(10). DOI: 10.4172/2155-9546.1000369
Kumar, M., Singh, S., Dwivedi, S., Trivedi, A., Dubey, I. & Trivedi, S. P. (2023). Copper-induced genotoxicity, oxidative stress, and alteration in transcriptional level of autophagy-associated genes in snakehead fish Channa punctatus. Biological Trace Element Research, 201(4), 2022-2035. https://doi.org/10.1007/s12011-022-03301-8
Lawrence, A. J. & Hemingway, K. L. (Eds.). (2008). Effects of pollution on fish: molecular effects and population responses. John Wiley & Sons.).
Lieke, T., Meinelt, T., Hoseinifar, S. H., Pan, B., Straus, D. L. & Steinberg, C. E. (2020). Sustainable aquaculture requires environmental‐friendly treatment strategies for fish diseases. Reviews in Aquaculture, 12(2), 943-965.https://doi.org/10.1111/raq.12365
Malhotra, N., Ger, T. R., Uapipatanakul, B., Huang, J. C., Chen, K. H. C. & Hsiao, C. D. (2020). Review of copper and copper nanoparticle toxicity in fish. Nanomaterials, 10(6), 1126.https://doi.org/10.3390/nano10061126
Mansouri, B., Maleki, A., Johari, S. A., Shahmoradi, B., Mohammadi, E. & Davari, B. (2017). Histopathological effects of copper oxide nanoparticles on the gill and intestine of common carp (Cyprinus carpio) in the presence of titanium dioxide nanoparticles. Chemistry and Ecology, 33(4), 295-308.https://doi.org/10.1080/ 02757540.2017. 1301436
Maurya, P. K., Malik, D. S., Yadav, K. K., Kumar, A., Kumar, S. & Kamyab, H. (2019). Bioaccumulation and potential sources of heavy metal contamination in fish species in River Ganga basin: Possible human health risks evaluation. Toxicology Reports, 6, 472-481.https://doi.org/10.1016/j.toxrep.2019.05.012
Mhaske, A., Sharma, S. & Shukla, R. (2023). Nanotheranostic: The futuristic therapy for copper mediated neurological sequelae. Journal of Drug Delivery Science and Technology, 104193.).https://doi.org/10.1016/j.jddst.2023.104193
Mitra, S., Chakraborty, A. J., Tareq, A. M., Emran, T. B., Nainu, F., Khusro, A., ... & Simal-Gandara, J. (2022). Impact of heavy metals on the environment and human health: Novel therapeutic insights to counter toxicity. Journal of King Saud University-Science, 34(3), 101865.https://doi.org/10.1016/j.jksus.2022.101865
Murali, M., Athif, P., Suganthi, P., Bukhari, A. S., Mohamed, H. S., Basu, H. & Singhal, R. K. (2018). Toxicological effect of Al2O3 nanoparticles on histoarchitecture of the freshwater fish Oreochromis mossambicus. Environmental Toxicology and Pharmacology, 59, 74-81.https://doi.org/10.1016/j.etap.2018.03.004
Nagpure, N. S., Srivastava, R., Kumar, R., Dabas, A., Kushwaha, B. & Kumar, P. (2015). Assessment of pollution of river Ganges by tannery effluents using genotoxicity biomarkers in murrel fish, Channa punctatus (Bloch).
Noureen, A., Jabeen, F., Tabish, T. A., Yaqub, S., Ali, M. & Chaudhry, A. S. (2018). Assessment of copper nanoparticles (Cu-NPs) and copper (II) oxide (CuO) induced hemato-and hepatotoxicity in Cyprinus carpio. Nanotechnology, 29(14), 144003.10.1088/1361-6528/aaaaa7
OECD. Test no. 203: fish, acute toxicity testing, section 2: Effects on biotic systems. Guidelines for the testing of chemicals. 2019;10.
Rehman, M., Liu, L., Wang, Q., Saleem, M. H., Bashir, S., Ullah, S. & Peng, D. (2019). Copper environmental toxicology, recent advances, and future outlook: a review. Environmental science and pollution research, 26, 18003-18016. https://doi.org/10.1007/s11356-019-05073-6
Sangeetha, P. & Aruljothi, B. (2019). The toxic effect of heavy metals (nickel, copper, and mixture) on histological parameters of the common carp (fingerlings) Cyprinus carpio. Plant Arch, 19(2), 4534-4542.
Sarangi, P. K. (2021). Cytogenotoxic Effect of Pesticides Induces Variability in Micronu-cleus and Nucleo-Cytoplasmic Abnormalities in Channa punctatus in vivo. Journal of Zoological Research| Volume, 3(04).
Shah, N., Khan, A., Habib Khan, N. & Khisroon, M. (2021). Genotoxi consequences in common grass carp (Ctenopharyngodon idella Valenciennes, 1844) exposed to selected toxic metals. Biological Trace Element Research, 199, 305-314. https://doi.org/10.1007/s12011-020-02122-x
Shahjahan, M., Khatun, M. S., Mun, M. M., Islam, S. M., Uddin, M. H., Badruzzaman, M. & Khan, S. (2020). Nuclear and cellular abnormalities of erythrocytes in response to thermal stress in common carp Cyprinus carpio. Frontiers in Physiology, 11, 543.https://doi.org/10.3389/fphys.2020.00543
Stankevičiūtė, M., Butrimavičienė, L., Valskienė, R., Greiciūnaitė, J., Baršienė, J., Vosylienė, M. Z. & Svecevičius, G. (2016). Analysis of nuclear abnormalities in erythrocytes of rainbow trout (Oncorhynchus mykiss) treated with Cu and Zn and after 4-, 8-, and 12-day depuration (post-treatment recovery). Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 797, 26-35.https://doi.org/10.1016/j.mrgentox.2016.01.003
Tavares-Dias, M. (2021). Toxic, physiological, histomorphological, growth performance and antiparasitic effects of copper sulphate in fish aquaculture. Aquaculture, 535, 736350.). https://doi.org/10.1016/j.aquaculture.2021.73 6350
Trivedi, S. P., Singh, S., Trivedi, A. & Kumar, M. (2022). Mercuric chloride‐induced oxidative stress, genotoxicity, haematological changes, and histopathological alterations in fish Channa punctatus (B loch, 1793). Journal of Fish Biology, 100(4), 868-883.https://doi.org/10.1111/jfb.15019
Wu, L., Yu, Q., Zhang, G., Wu, F., Zhang, Y., Yuan, C., ... & Wang, Z. (2019). Single and combined exposures of waterborne Cu and Cd induced oxidative stress responses and tissue injury in female rare minnow (Gobiocypris rarus). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 222, 90-99.https://doi.org/10.1016/j.cbpc.2019.04.013
Yu, Z., Zheng, Y. G., Du, H. L., Li, H. J. & Wu, L. F. (2020). Bioflocs protects copper-induced inflammatory response and oxidative stress in Rhynchocypris lagowski Dybowski through inhibiting NF-κB and Nrf2 signaling pathways. Fish & shellfish immunology, 98, 466-476. https://doi.org/10.1016/j.fsi.2020.01.048
Zebral, Y. D., Roza, M., da Silva Fonseca, J., Costa, P. G., de Oliveira, C. S., Zocke, T. G., ... & Bianchini, A. (2019). Waterborne copper is more toxic to the killifish Poecilia vivipara in elevated temperatures: Linking oxidative stress in the liver with reduced organismal thermal performance. Aquatic Toxicology, 209, 142-149. https://doi.org/10.1016/j.aquatox.2019.02.005
Zeng, L., Ai, C. X., Zhang, J. S. & Li, W. C. (2020). Pre-hypoxia exposure inhibited copper toxicity by improving energy metabolism, antioxidant defence and mitophagy in the liver of the large yellow croaker Larimichthys crocea. Science of the Total Environment, 708, 134961. https://doi.org/10.1016/j.scitotenv.2019.134961
Abdel-Latif, H. M., Dawood, M. A., Mahmoud, S. F., Shukry, M., Noreldin, A. E., Ghetas, H. A. & Khallaf, M. A. (2021). Copper oxide nanoparticles alter serum biochemical indices, induce histopathological alterations, and modulate transcription of cytokines, HSP70, and oxidative stress genes in Oreochromis niloticus. Animals, 11(3), 652. https://doi.org/10.3390/ani11030652
Aghamirkarimi, S., Mashinchian Moradi, A., Sharifpour, I., Jamili, S. & GhavamMostafavi, P. (2017). Sublethal effects of copper nanoparticles on the histology of gill, liver and kidney of the Caspian roach, Rutilus rutilus caspicus.Global Journal of Environmental Science and Management. DOI 10.22034/gjesm.2017.03.03.009Ale, A., Bacchetta, C., Rossi, A. S., Galdopórpora, J., Desimone, M. F., de la Torre, F. R., ... & Cazenave, J. (2018). Nanosilver toxicity in gills of a neotropical fish: Metal accumulation, oxidative stress, histopathology and other physiological effects. Ecotoxicology and Environmental Safety, 148, 976-984. https://doi.org/10.1016/j.ecoenv.2017.11.072Alimba, C. G. & Laide, A. W. (2019). Genotoxic and cytotoxic assessment of individual and composite mixture of cadmium, lead and manganese in Clarias gariepinus (Burchell 1822) using micronucleus assay. The Nucleus, 62(3), 191-202.https://doi.org/10.1007/s13237-019-00289-w
Anbumani, S. & Mohankumar, M. N. (2011). Nuclear and cytoplasmic abnormalities in the fish Catlacatla (Hamilton) exposed to chemicals and ionizing radiation. Research Journal of Environmental Sciences, 5(12), 867-877.
APHA, AWWA &WEF (2017). In: Rice EW, Baird RB, Eaton AD, Clesceri LS, editors. Standard methods for the examination of water and wastewater. 23rd ed. Washington, DC: APHA; 2017.
Canalejo, A., Diaz-de-Alba, M., Granado-Castro, M. D., Cordoba, F., Espada-Bellido, E., Galindo-Riaño, M. D. & Torronteras, R. (2016). Early genotoxic response and accumulation induced by waterborne copper, lead, and arsenic in European seabass, Dicentrarchuslabrax. Environmental Science and Pollution Research, 23, 3256-3266.https://doi.org/10.1007/s11356-015-5435-1
Chowdhary, P., Bharagava, R. N., Mishra, S. & Khan, N. (2020). Role of industries in water scarcity and its adverse effects on environment and human health. Environmental Concerns and Sustainable Development: Volume 1: Air, Water and Energy Resources, 235-256. https://doi.org/10.1007/978-981-13-5889-0_12
De Zwart, D., Adams, W., Galay Burgos, M., Hollender, J., Junghans, M., Merrington, G., ... & Williams, R. (2018). Aquatic exposures of chemical mixtures in urban environments: Approaches to impact assessment. Environmental Toxicology and Chemistry, 37(3), 703-714.https://doi.org/10.1002/etc.3975
Elalfy, M. M., Abomosallam, M. S., Sleem, F. & Elhadidy, M. (2021). Copper and copper containing pesticide as copper oxychloride toxicity and its adverse effects on animal and human health. MedicoResearch Chronicles, 8(2),89-98.https://doi.org/10.26838 MEDRECH. 2021.8.2. 486
Francisco, C. D. M., Bertolino, S. M., De Oliveira Junior, R. J., Morelli, S. & Pereira, B. B. (2019). Genotoxicity assessment of polluted urban streams using a native fish Astyanax altiparanae. Journal of Toxicology and Environmental Health, Part A, 82(8), 514-523. https://doi.org/10.1080/15287394.2019.1624235
Javed, M. & Usmani, N. (2019). An overview of the adverse effects of heavy metal contamination on fish health. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 89, 389-403.https://doi.org/10.1007/s40011-017-0875-7
Jomova, K., Makova, M., Alomar, S. Y., Alwasel, S. H., Nepovimova, E., Kuca, K., & Valko, M. (2022). Essential metals in health and disease. Chemico-biological interactions, 110173.)https://doi.org/10.1016/j.cbi.2022.110173
Karim, N. (2018). Copper and human health-a review. Journal of Bahria University Medical and Dental College, 8(2), 117-122.).
Kaur, S., Khera, K. S. & Kondal, J. K. (2018). Heavy metal induced histopathological alterations in liver, muscle and kidney of freshwater cyprinid, Labeorohita (Hamilton). Journal of Entomology and Zoology Studies, 6(2), 2137-2144.
Kumar, M., Gupta, N., Ratn, A., Awasthi, Y., Prasad, R., Trivedi, A. & Trivedi, S. P. (2020). Biomonitoring of heavy metals in river ganga water, sediments, plant, and fishes of different trophic levels. Biological trace element research, 193, 536-547.https://doi.org/10.1007/s12011-019-01736-0
Kumar, M., Kumar, P. & Devi, S. (2015). To study the histopathological changes in the gills of Clarias batrachus, an air-breathing teleost after short term exposure of copper sulphate. J Aquac Res Develop, 6(10). DOI: 10.4172/2155-9546.1000369
Kumar, M., Singh, S., Dwivedi, S., Trivedi, A., Dubey, I. & Trivedi, S. P. (2023). Copper-induced genotoxicity, oxidative stress, and alteration in transcriptional level of autophagy-associated genes in snakehead fish Channa punctatus. Biological Trace Element Research, 201(4), 2022-2035. https://doi.org/10.1007/s12011-022-03301-8
Lawrence, A. J. & Hemingway, K. L. (Eds.). (2008). Effects of pollution on fish: molecular effects and population responses. John Wiley & Sons.).
Lieke, T., Meinelt, T., Hoseinifar, S. H., Pan, B., Straus, D. L. & Steinberg, C. E. (2020). Sustainable aquaculture requires environmental‐friendly treatment strategies for fish diseases. Reviews in Aquaculture, 12(2), 943-965.https://doi.org/10.1111/raq.12365
Malhotra, N., Ger, T. R., Uapipatanakul, B., Huang, J. C., Chen, K. H. C. & Hsiao, C. D. (2020). Review of copper and copper nanoparticle toxicity in fish. Nanomaterials, 10(6), 1126.https://doi.org/10.3390/nano10061126
Mansouri, B., Maleki, A., Johari, S. A., Shahmoradi, B., Mohammadi, E. & Davari, B. (2017). Histopathological effects of copper oxide nanoparticles on the gill and intestine of common carp (Cyprinus carpio) in the presence of titanium dioxide nanoparticles. Chemistry and Ecology, 33(4), 295-308.https://doi.org/10.1080/ 02757540.2017. 1301436
Maurya, P. K., Malik, D. S., Yadav, K. K., Kumar, A., Kumar, S. & Kamyab, H. (2019). Bioaccumulation and potential sources of heavy metal contamination in fish species in River Ganga basin: Possible human health risks evaluation. Toxicology Reports, 6, 472-481.https://doi.org/10.1016/j.toxrep.2019.05.012
Mhaske, A., Sharma, S. & Shukla, R. (2023). Nanotheranostic: The futuristic therapy for copper mediated neurological sequelae. Journal of Drug Delivery Science and Technology, 104193.).https://doi.org/10.1016/j.jddst.2023.104193
Mitra, S., Chakraborty, A. J., Tareq, A. M., Emran, T. B., Nainu, F., Khusro, A., ... & Simal-Gandara, J. (2022). Impact of heavy metals on the environment and human health: Novel therapeutic insights to counter toxicity. Journal of King Saud University-Science, 34(3), 101865.https://doi.org/10.1016/j.jksus.2022.101865
Murali, M., Athif, P., Suganthi, P., Bukhari, A. S., Mohamed, H. S., Basu, H. & Singhal, R. K. (2018). Toxicological effect of Al2O3 nanoparticles on histoarchitecture of the freshwater fish Oreochromis mossambicus. Environmental Toxicology and Pharmacology, 59, 74-81.https://doi.org/10.1016/j.etap.2018.03.004
Nagpure, N. S., Srivastava, R., Kumar, R., Dabas, A., Kushwaha, B. & Kumar, P. (2015). Assessment of pollution of river Ganges by tannery effluents using genotoxicity biomarkers in murrel fish, Channa punctatus (Bloch).
Noureen, A., Jabeen, F., Tabish, T. A., Yaqub, S., Ali, M. & Chaudhry, A. S. (2018). Assessment of copper nanoparticles (Cu-NPs) and copper (II) oxide (CuO) induced hemato-and hepatotoxicity in Cyprinus carpio. Nanotechnology, 29(14), 144003.10.1088/1361-6528/aaaaa7
OECD. Test no. 203: fish, acute toxicity testing, section 2: Effects on biotic systems. Guidelines for the testing of chemicals. 2019;10.
Rehman, M., Liu, L., Wang, Q., Saleem, M. H., Bashir, S., Ullah, S. & Peng, D. (2019). Copper environmental toxicology, recent advances, and future outlook: a review. Environmental science and pollution research, 26, 18003-18016. https://doi.org/10.1007/s11356-019-05073-6
Sangeetha, P. & Aruljothi, B. (2019). The toxic effect of heavy metals (nickel, copper, and mixture) on histological parameters of the common carp (fingerlings) Cyprinus carpio. Plant Arch, 19(2), 4534-4542.
Sarangi, P. K. (2021). Cytogenotoxic Effect of Pesticides Induces Variability in Micronu-cleus and Nucleo-Cytoplasmic Abnormalities in Channa punctatus in vivo. Journal of Zoological Research| Volume, 3(04).
Shah, N., Khan, A., Habib Khan, N. & Khisroon, M. (2021). Genotoxi consequences in common grass carp (Ctenopharyngodon idella Valenciennes, 1844) exposed to selected toxic metals. Biological Trace Element Research, 199, 305-314. https://doi.org/10.1007/s12011-020-02122-x
Shahjahan, M., Khatun, M. S., Mun, M. M., Islam, S. M., Uddin, M. H., Badruzzaman, M. & Khan, S. (2020). Nuclear and cellular abnormalities of erythrocytes in response to thermal stress in common carp Cyprinus carpio. Frontiers in Physiology, 11, 543.https://doi.org/10.3389/fphys.2020.00543
Stankevičiūtė, M., Butrimavičienė, L., Valskienė, R., Greiciūnaitė, J., Baršienė, J., Vosylienė, M. Z. & Svecevičius, G. (2016). Analysis of nuclear abnormalities in erythrocytes of rainbow trout (Oncorhynchus mykiss) treated with Cu and Zn and after 4-, 8-, and 12-day depuration (post-treatment recovery). Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 797, 26-35.https://doi.org/10.1016/j.mrgentox.2016.01.003
Tavares-Dias, M. (2021). Toxic, physiological, histomorphological, growth performance and antiparasitic effects of copper sulphate in fish aquaculture. Aquaculture, 535, 736350.). https://doi.org/10.1016/j.aquaculture.2021.73 6350
Trivedi, S. P., Singh, S., Trivedi, A. & Kumar, M. (2022). Mercuric chloride‐induced oxidative stress, genotoxicity, haematological changes, and histopathological alterations in fish Channa punctatus (B loch, 1793). Journal of Fish Biology, 100(4), 868-883.https://doi.org/10.1111/jfb.15019
Wu, L., Yu, Q., Zhang, G., Wu, F., Zhang, Y., Yuan, C., ... & Wang, Z. (2019). Single and combined exposures of waterborne Cu and Cd induced oxidative stress responses and tissue injury in female rare minnow (Gobiocypris rarus). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 222, 90-99.https://doi.org/10.1016/j.cbpc.2019.04.013
Yu, Z., Zheng, Y. G., Du, H. L., Li, H. J. & Wu, L. F. (2020). Bioflocs protects copper-induced inflammatory response and oxidative stress in Rhynchocypris lagowski Dybowski through inhibiting NF-κB and Nrf2 signaling pathways. Fish & shellfish immunology, 98, 466-476. https://doi.org/10.1016/j.fsi.2020.01.048
Zebral, Y. D., Roza, M., da Silva Fonseca, J., Costa, P. G., de Oliveira, C. S., Zocke, T. G., ... & Bianchini, A. (2019). Waterborne copper is more toxic to the killifish Poecilia vivipara in elevated temperatures: Linking oxidative stress in the liver with reduced organismal thermal performance. Aquatic Toxicology, 209, 142-149. https://doi.org/10.1016/j.aquatox.2019.02.005
Zeng, L., Ai, C. X., Zhang, J. S. & Li, W. C. (2020). Pre-hypoxia exposure inhibited copper toxicity by improving energy metabolism, antioxidant defence and mitophagy in the liver of the large yellow croaker Larimichthys crocea. Science of the Total Environment, 708, 134961. https://doi.org/10.1016/j.scitotenv.2019.134961
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Induction of micronuclei in blood and histopathological alterations in gill, kidney and liver of Channa punctatus (Bloch, 1793) exposed to copper sulphate. (2024). Journal of Applied and Natural Science, 16(1), 17-26. https://doi.org/10.31018/jans.v16i1.5172
