Investigating the histopathology and ultrastructural changes of gill tissue of common carp (Cyprinus carpio) in separate and Co- exposure to silica nanoparticles (SiO2) and zinc oxide nanoparticles (ZnO)

Document Type : Research Paper

Authors

1 Department of Environment, Faculty of Natural Resources and Environment, Malayer University, Malayer, Iran.

2 Drug Abuse Prevention Research Center, Health Research Institute, Kermanshah University of Medical Sciences, Kermanshah, Iran.

10.22059/jne.2024.377728.2682

Abstract

Co- exposure to nanoparticles can cause serious damage to aquatic organisms, including fish. The aim of this study was to investigate the toxic effects of simultaneous exposure to silica and zinc oxide nanoparticles on changes in the gill tissue of common carp (Cyprinus carpio). In this study, common carp were exposed to different concentrations of zinc oxide nanoparticles, silica dioxide, and a combination of these nanoparticles. After 28 days of exposure, the samples were prepared for gill histology. Devices such as XRD, FTIR, and SEM were used in this study. The present study showed that the exposure of common carp to nanoparticles caused various tissue damage, including capillary telangiectasia, hyperplasia, increased mucus secretion, clubbing of the apex of the secondary lamellae, and fusion. Also, the simultaneous exposure of two nanoparticles has more destructive effects than the separate state of nanoparticles, which can be concluded that the presence of silica nanoparticles increases the toxicity of zinc nanoparticles. In addition, different nanoparticles show different effects in different environments. Therefore, it should be noted that the use of different nanoparticles in different amounts requires more detailed and comprehensive studies on the effects of these nanoparticles on living organisms.

Keywords

Banerjee, T.K., 2007. Histopathology of respiratory organs of certain airbreathingfishes of India. Fish Physiology and Biochemistry 33, 441-454.
Barbieri, E., Campos-Garcia, J., Martinez, D.S.T., da Silva, J.R.M.C., Alves, O.L., Rezende, K.F.O., 2016. Histopathological effects on gills of Nile tilapia (Oreochromis niloticus, Linnaeus, 1758) exposed to Pb and carbon nanotubes. Microscopy and Microanalysis 22(6), 1162-1169.
Bathi, J.R., Wright, L., Khan, E., 2022. Critical review of engineered nanoparticles: environmental concentrations and toxicity. Current Pollution Reports 8(4), 498-518.‏
Beegam, A., Lopes, M., Fernandes, T., Jose, J., Barreto, A., Oliveira, M., Soares, A.M.V.M., Trindade, T., Thomas, S., and Pereira, M.L. 2019. Multiorgan histopathological changes in the juvenile seabream Sparus aurata as a biomarker for zinc oxide particles toxicity. Environmental Science and Pollution Research 27, 30907-30917
Bernet, D., Schmidt, H., Meier, W., BurkhardtHolm, P., Wahli, T., 1999. Histopathology in fish: proposal for a protocol to assess aquatic pollution. Journal of fish diseases 22(1), 25-34.
Bhat, I.D., Bhat, B.A., Vishwakarma, S., Verma, A., Saxena, G., 2012. Acute toxicity and behavioural responses of Labeo rohita (Hamilton) to a biopesticide" NEEM-OM, Current World Environment 7 (1), 175-178.
Campos-Garcia, J., Martinez, D. S. T., Rezende, K. F. O., da Silva, J. R. M. C., Alves, O. L., Barbieri, E., 2016. Histopathological alterations in the gills of Nile tilapia exposed to carbofuran and multiwalled carbon nanotubes. Ecotoxicology and environmental safety 133, 481-488.‏
Capaldo, A., Gay, F., and Laforgia, V., 2019. Changes in the gills of the European eel (Anguilla anguilla) after chronic exposure to environmental cocaine concentration. Ecotoxicology and Environmental Safety 169, 112-119.
Correia, J.E., Christofoletti, C.A., Marcato, A.C.C., Marinho, J.F.U., Fontanetti, C.S., 2017. Histopathological analysis of tilapia gills (Oreochromis niloticus Linnaeus, 1758) exposed to sugarcane vinasse. Ecotoxicology and Environmental Safety 135, 319–326.
Eom, I.C., Kim, P.J., and Choi, K.H., 2012. Oxidative stress in juvenile common carp (Cyprinus carpio) exposed to TiO2 nanoparticles. Molecular & cellular toxicology 8, 357-366.
Fathi, M., Binkowski, L.J., Azadi, N.A., Hamesadeghi, U., Mansouri, B., 2018. Co-exposure effects of mercury chloride (HgCl2) and silver nanoparticles (Ag-NPs) on goldfish (Carassius auratus): Histopathological changes, oxidative stress response, and bioaccumulation. Desalination and Water Treatment 105, 264-272.
Fathi, M., Mansouri, B., Azadi, N., Davari, B., Maleki, A., 2017. The effect of silver and mercury nanoparticles on laboratory fish stress index. Zanco Journal of Medical Sciences 18(56), 70-77. In Persian.
Grasso, A., Ferrante, M., Moreda-Pineiro, A., Arena, G., Magarini, R., Conti, G. O., and Copat, C. 2022. Dietary exposure of zinc oxide nanoparticles (ZnO-NPs) from canned seafood by single particle ICP-MS: Balancing of risks and benefits for human health. Ecotoxicology and Environmental Safety 231, 113217.
Griffitt, R. J., Weil, R., Hyndman, K. A., Denslow, N. D., Powers, K., Taylor, D., Barber, D. S., 2007. Exposure to copper nanoparticles causes gill injury and acute lethality in zebrafish (Danio rerio). Environmental science & technology 41(23), 8178-8186.‏
Jaya, K., Shettu, N., 2015. Transmission electron microscopic study of gillsof freshwater fish Channa punctatus (Bloch) exposed to the toxicity of cypermethrin. Journal of Chemical and Pharmaceutical Research 7,698–701.
Kaur, R., Dua, A., 2015. 96 h LC50, behavioural alterations and histopathological effects due 540 to wastewater toxicity in a freshwater fish Channa punctatus. Environmental Science and Pollution Research 22, 5100-5110.
Lee, B.C., Kim, K.T., Cho, J.G., Lee, J.W., Ryu, T.K., Yoon, J.H., Lee, S.H., Duong, C.N., Mansouri, B., Baramaki, .R, Pourkhabbaz, A., Zareh, M., Hamidian, A.H., 2013. Bioaccumulation and depuration of copper in the kidney and liver of freshwater fish Capoeta fusca. Iranian Journal of Toxicology 7, 808-814.in Persian.
Mansouri, B., Johari, S. A., 2016. Effects of short-term exposure to sublethal concentrations of silver nanoparticles on histopathology and electron microscope ultrastructure of zebrafish (Danio rerio) gills. Iranian Journal of Toxicology 10(1), 15-20.‏in Persian.  
Mansouri, B., Johari, S. A., Azadi, N. A., Sarkheil, M., 2018. Effects of waterborne ZnO nanoparticles and Zn2+ ions on the gills of rainbow trout (Oncorhynchus mykiss): bioaccumulation, histopathological and ultrastructural changes. Turkish Journal of Fisheries and Aquatic Sciences 18(5), 739-746. In Persian.
‏Mansouri, B., Maleki, A., Davari, B., Johari, S. A., Shahmoradi, B., Mohammadi, E., 2016. Effect of subchronic exposure of Cuo NPs in presence of TiO2 NPs on fish model. Journal of Mazandaran University of Medical Sciences 26(142), 138-127.‏ in Persian. 
Mansouri, B., Maleki, A., Johari, S. A., Reshahmanish, N., 2015. Effects of cobalt oxide nanoparticles and cobalt ions on gill histopathology of zebrafish (Danio rerio). Aquaculture, Aquarium, Conservation & Legislation 8(3), 438-444. In Persian.‏
Osborne, O.J., Johnston, B.D., Moger, J., Balousha, M., Lead , J.R., Kudoh, T., Tyler, C.R., 2013. Effects of particle size and coating on nanoscale Ag and TiO2 exposure in zebrafish (Danio rerio) embryos. Nanotoxicology 7(8), 1315–1324.
Pirsaheb, M., Azadi, N. A., Miglietta, M. L., Sayadi, M. H., Blahova, J., Fathi, M., Mansouri, B., 2019. Toxicological effects of transition metal-doped titanium dioxide nanoparticles on goldfish (Carassius auratus) and common carp (Cyprinus carpio). Chemosphere 215, 904-915. in Persin.
Pirsaheb, M., Azadi, N.A., Miglietta, M.L., Sayadi, M.H., Blahova, J., Fathi, M., Mansouri, B., 2019. Toxicological effects of transition metal-doped titanium dioxide nanoparticles on goldfish (Carassius auratus) and common carp (Cyprinus carpio). Chemosphere 215, 904-915.
Rezaian, H., Rezaei Funkhes, K., Mir Waqfi, A., 2023. Investigating the separate and simultaneous effects of titanium dioxide nanoparticles (TiO2) and zinc oxide nanoparticles (ZnO) on the gill tissue pathology of common carp (Cyprinus carpio). Aquaculture Science Journal 11(21), 1-13. in Persian.
Sahraei, H., Hosseini, S.A., Hedayati, S.A., Ghorbani, R., 2017. Pathological changes in gill tissue of common carp (Cyprinus carpio) exposed to sub-lethal concentrations of copper oxide nanoparticles. Environmental Science and Technology 20(1) 95-120. in Persian.
Sayadi, M. H., Mansouri, B., Shahri, E., Tyler, C. R., Shekari, H., Kharkan, J., 2020. Exposure effects of iron oxide nanoparticles and iron salts in blackfish (Capoeta fusca): Acute toxicity, bioaccumulation, depuration, and tissue histopathology. Chemosphere, 247, 125900.‏ in Persian.
Sayadi, M. H., Pavlaki, M. D., Loureiro, S., Martins, R., Tyler, C. R., Mansouri, B., and Shekari, H. 2022. Co-exposure of zinc oxide nanoparticles and multi-layer graphenes in blackfish (Capoeta fusca): evaluation of lethal, behavioural, and histopathological effects. Ecotoxicology, 31(3), 425-439.‏ in Persian.
Sayadi, M.H., Mansouri, B., Shahri, E., Tyler, C.R., Shekari, H., Kharkan, J., 2020. Exposure effects of iron oxide nanoparticles and iron salts in blackfish (Capoeta fusca): Acute toxicity, bioaccumulation, depuration, and tissue histopathology. Chemosphere 247, 125900.
Selvarajan, V., Obuobi, S., Ee, P. L. R., 2020. Silica nanoparticles—a versatile tool for the treatment of bacterial infections. Frontiers in Chemistry 8, 602.‏
Vali, S., Mohammadi, G., Tavabe, K. R., Moghadas, F., Naserabad, S. S., 2020. The effects of silver nanoparticles (Ag-NPs) sublethal concentrations on common carp (Cyprinus carpio): Bioaccumulation, hematology, serum biochemistry and immunology, antioxidant enzymes, and skin mucosal responses. Ecotoxicology and environmental safety 194, 110353.‏ in Persian.
Yang, X., Liu, X., Zhang, A., Lu, D., Li, G., Zhang, Q., Jiang, G., 2019. Distinguishing the sources of silica nanoparticles by dual isotopic fingerprinting and machine learning. Nature Communications 10(1), 1620.
Ye, N., Wang, Z., Wang, S., Peijnenburg, W. J., 2018. Toxicity of mixtures of zinc oxide and graphene oxide nanoparticles to aquatic organisms of different trophic level: Particles outperform dissolved ions. Nanotoxicology 12(5), B423-438.