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Histopathological Effects on Gills of Nile Tilapia (Oreochromis niloticus, Linnaeus, 1758) Exposed to Pb and Carbon Nanotubes

  • Edison Barbieri (a1), Janaína Campos-Garcia (a1), Diego S. T. Martinez (a2), José Roberto M. C. da Silva (a3), Oswaldo Luiz Alves (a4) and Karina F. O. Rezende (a3)...


The effect of heavy metal in fish has been the focus of extensive research for many years. However, the combined effect of heavy metals and nanomaterials is still a new subject that needs to be studied. The aim of this study was to examine histopathologic alterations in the gills of Nile tilapia (Oreochromis niloticus) to determine possible effects of lead (Pb), carbon nanotubes, and Pb+carbon nanotubes on their histological integrity, and if this biological system can be used as a tool for evaluating water quality in monitoring programs. For this, tilapia were exposed to Pb, carbon nanotubes and Pb+carbon nanotubes for 4 days. The main alterations observed were epithelial structure, hyperplasia and displacement of epithelial cells, and alterations of the structure and occurrence of aneurysms in the secondary lamella. The most severe alterations were related to the Pb+carbon nanotubes. We conclude that the oxidized multi-walled carbon nanotubes enhanced the acute lead toxicity in Nile tilapias. This work draws attention to the implications of carbon nanomaterials released in the aquatic environment and their interaction with classical pollutants.


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Barbieri, E. & Doi, S.A. (2011). The effects of different temperature and salinity levels on the acute toxicity of zinc in the Pink Shrimp. Mar Freshwater Behav Physiol 44(4), 251263.
Barbieri, E., Passos, E.A., Garcia, C.A.B., Souza, K.A. & Santos, D.B. (2010). Assessment of trace metal levels in catfish (Cathorops spixii) from Sal River estuary, Aracaju, state of Sergipe, northeastern Brazil. Water Environ Res 82(12), 23012305.
Britto, R.S., Garcia, M.L., Rocha, A.M., Flores, J.A., Pinheiro, M.V.B., Monserrat, J.M. & Ferreira, J.L.R. (2012). Effects of carbon nanomaterials fullerene C60 and fullerol C60(OH)18–22 on gills of fish Cyprinus carpio (Cyprinidae) exposed to ultraviolet radiation. Aquat Toxicol 114, 8087.
Burkhard-Holm, P. (1997). Lectin histochemistry of rainbow trout (Oncorhynchus mykiss) gill and skin. Histochem J 29(11–12), 893899.
Campos-Garcia, J., Martinez, D.S.T., Alves, O.L. & Barbieri, E. (2015). Ecotoxicological effects of carbofuran and oxidised multiwalled carbon nanotubes on the freshwater fish Nile tilapia: Nanotubes enhance pesticide ecotoxicity. Ecotoxicol Environ Saf 111, 131137.
Campos-Garcia, J., Martinez, D.S.T., Rezende, K.F.O., Silva, J.R.M.C.S., Alves, O.L. & Barbieri, E. (2016). Histopathological alterations in the gills of Nile tilapia exposed to carbofuran and multiwalled carbon nanotubes. Ecotoxicol Environ Saf 133, 481488.
Canesi, L., Ciacci, C., Vallotto, D., Gallo, G., Marcomini, A. & Pojana, G. (2010). In vitro effects of suspensions of selected nanoparticles (C60 fullerene, TiO2, SiO2) on Mytilus hemocytes . Aquat Toxicol 96(2), 151158.
Chae, Y.J., Pham, C.H., Lee, J., Bae, E., Yi, J. & Gu, M.B. (2009). Evaluation of the toxic impact of silver nanoparticles on Japanese medaka (Oryzias latipes). Aquat Toxicol 94(4), 320327.
Cheng, J., Chan, C.M., Veca, L.M., Poon, W.L., Chan, PK, Qu, L., Sun, Y.P. & Cheng, S.H. (2009). Acute and long-term effects after single loading of functionalized multiwalled carbon nanotubes into zebrafish (Danio rerio). Toxicol Appl Pharmacol 235(2), 216225.
Cheng, J.P., Flahaut, E. & Cheng, S.H. (2007). Effect of carbon nanotubes on developing zebrafish (Danio rerio) embryos. Environ Toxicol Chem 26(4), 708716.
Clearwater, S.J., Handy, R.D. & Hogstrand, C. (2005). Interactions of dietborne metals with digestive processes of fishes. In Toxicity of dietborne metals to aquatic organisms, Meyer J.S., Adams W.J., Brix K.V., Luoma S.N., Mount D.R., Stubblefield W.A. & Wood C.M. (Eds.), pp. 205225. Pensacola, FL: SETAC Press.
Damato, M. & Barbieri, E. (2003). Emprego de uma espécie indicadora sul-americana na determinação da toxicidade aguda para Cobre, Zinco, Níquel e Alumínio. O Mundo da Saúde 27(4), 551558.
Damato, M. & Barbieri, E. (2012). Estudo da Toxicidade aguda e alterações metabólicas provocadas pela exposição do Cádmio sobre o peixe Hyphessobrycon callistus utilizado como indicador de saúde ambiental. O Mundo da Saúde 36(4), 574581.
Doi, A.S., Collaço, F.L., Sturaro, L.G.R. & Barbieri, E. (2012). Efeito do chumbo em nível de oxigênio e amônia no camarão rosa (Farfantepeneaus paulensis) em relação à salinidade. O Mundo da Saúde 36(4), 594600.
Erkmen, B. & Kolankaya, D. (2000). Effects of water quality on epithelial morphology in the gills of Capoeta tinca living in two tributaries of Kizilirmak River, Turkey. Bull Environ Contam Toxicol 64(3), 418425.
Griffitt, R.J., Hyndman, K., Denslow, N.D. & Barber, D.S. (2009). Comparison of molecular and histological changes in zebra fish gills exposed to metallic nanomaterials in aquatic organisms. Toxicological Sciences 107(2), 404415.
Griffitt, R.J., Luo, J., Gao, J., Bonzongo, J.C. & Barber, D.S. (2008). Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Toxicol Chem 27(9), 19721978.
Griffitt, R.J., Weil, R., Hyndman, K.A., Denslow, N.D., Powers, K. & Taylor, D. (2007). Exposure to copper nanoparticles causes gill injury and acute lethality in zebrafish (Danio rerio). Environ Sci Technol 41(23), 81788186.
Guerra-Santos, B., Albinati, R.C.B., Moreira, E.L.T., Lima, F.W.M., Azevedo, T.M.P., Costa, D.S.P., Medeiros, S.D.C. & Lira, A.D. (2012). Parameters hematological and histopathologic alterations in cobia (Rachycentron canadum Linnaeus, 1766) com amyloodiniose. Pesquisa Veterinária Brasileira 32(11), 11841190.
Handy, R.D. (1996). Dietary exposure to toxic metals in fish. In Toxicology of Aquatic Pollution: Physiological, Cellular and Molecular Approaches. Society for Experimental Biology Seminar Series, Taylor E.W. (Ed.), pp. 2960. Cambridge: Cambridge University Press.
Handy, R.D., McGeer, J.C., Allen, H.E., Drevnick, P.E., Gorsuch, J.W. & Green, A.S. (2005). Toxic effects of dietborne metals: Laboratory studies. In Toxicity of Dietborne Metals to Aquatic Organisms, Meyer J.S., Adams W.J., Brix K.V, Luoma S.N., Mount D.R, Stubblefield W.A & Wood CM (Eds.), pp. 59112. Pensacola, FL: SETAC Press.
Handy, R.D., Al-Bairuty, G., Al-Jubory, A., Ramsden, C.S., Boyle, D., Shaw, B.J. & Henry, T.B. (2011). Effects of manufactured nanomaterials on fishes: a target organ and body systems physiology approach. J FishBiol 79(4), 821853.
Kamunde, C. & Wood, C.M. (2004). Environmental chemistry, physiological homeostasis, toxicology, and environmental regulation of copper, an essential element in freshwater fish. Australas J Ecotoxicol 10(1), 120.
Klaper, R., Arndt, D., Setyowati, K., Chen, J. & Goetz, F. (2010). Functionalization impacts the effects of carbon nanotubes on the immune system of rainbow trout, Oncorhynchus mykiss . Aquat Toxicol 100(2), 211217.
Klaper, R., Crago, J., Barr, J., Arndt, D., Setyowati, K. & Chen, J. (2009). Toxicity biomarker expression in daphnids exposed to manufactured nanoparticles: Changes in toxicity with functionalization. Environ Pollut 157(4), 11521156.
Laurent, P. & Perry, S.F. (1991). Environmental effects on fish gill morphology. Physiol Zool 64(1), 425.
Mallatti, J. (1985). Fish gill structural changes induced by toxicants and other irritants: A statistical review. Can J Fish Aquat Sci 42(4), 630648.
Martinez, D.S.T., Alves, O.L. & Barbieri, E. (2013). Carbon nanotubes enhanced the lead toxicity on the freshwater fish. J Phys Conf Ser 429(1), 012043.
Maynard, A.D. (2004). Nanotoxicology: Laying a firm foundation for sustainable nanotechnologies. In Nanotoxicology – Characterization, Dosing and Health Effects, Monteiro-Riviere N.A. & Tran C.L. (Eds.), pp. 16. New York: Informa Healthcare USA, Inc.
McDonald, D.G. & Wood, C.M. (1993). Branchial mechanisms of acclimation to metals in freshwater fish. In Fish Ecophysiology, Rankin, J.C. & Jensen, F.B. (Eds.), pp. 297321. London: Chapman & Hall.
McDowell, E.M. & Trump, B.F. (1976). Histologic fixatives suitable for diagnostic light and electron microscopy. Arch Pathol Lab Med 100(8), 405414.
McManus, J.F.A. (1948). Histologica and histochemical uses of periodica acid. Biotech Histochem 23(3), 99108.
Nel, A., Xia, T., Mädler, L. & Li, N. (2006). Toxic potential of materials at the nanolevel. Science 311(5761), 622627.
Newman, M.C. & Clements, W.H. (2008). Fate and transport of contaminants in ecosystems. In Ecotoxicology – A Comprehensive Treatment, Newman, M.C. & Clements, W.H. (Eds.), pp. 737767. Boca Ratón: Taylor & Francis.
Peralta-Videa, J.R., Zhao, L., Lopez-Moreno, M.L., Rosa, G., Hong, J. & Gardea-Torresdey, J.L. (2011). Nanomaterials and the environment: A review for the biennium 2008-2010. J Hazard Mater 186(1), 115.
Poleksic, V. & Mitrovic-Tutundzic, V. (1994). Fish gills as a monitor of sublethal and chronic effects of pollution. In Sublethal and Chronic Effects of Pollutants on Fresh Water Fish, Muller R. & Lloyd R. (Eds.), pp. 339352. Oxford: Fishing News Books.
Rezende, K.F.O., Santos, R.M., Borges, J.C.S., Salvo, L.M. & da Silva, J.R.M.C. (2014). Histopathological and genotoxic effects of pollution on Nile Tilapia (Oreochromis niloticus, Linnaeus, 1758) in the Billings Reservoir (Brazil). Toxicol Mech Methods 24(6), 404411.
Sabóia-Morais, S.M.T., Hernandez-Blasquez, F.J., Mota, D.L. & Bittencourt, A.M. (1996). Mucous cell types in the branchial epithelium of the euryaline fish Poecilia vivípara . J Fish Biol, 49(3), 545548.
Santos, D.B., Barbieri, E., Bondioli, A.C. & Melo, C.B. (2014). Effects of lead in white shrimp (Litopenaeus schmitti) metabolism regarding salinity. O Mundo da Saúde 38(1), 1623.
Schwaiger, J., Wande, R., Adm, S., Pawert, M., Honnen, W. & Triebskorn, R. (1997). The use of histopathologic indicators to evaluate contaminant-related stress in fish. J Aquat Ecosyst Stress Recovery 6(1), 7586.
Shaw, B.J. & Handy, R.D. (2011). Physiological effects of nanoparticles on fish: A comparison of nanometals versus metal ions. Environmental International 37(6), 10831097.
Shaw, B.J. & Handy, R.D. (2006). Dietary copper exposure and recovery in Nile tilapia, Oreochromis niloticus . Aquat Toxicol 76(2), 111121.
Smith, C.J., Shaw, B.J. & Handy, R.D. (2007). Toxicity of single walled carbon nanotubes to rainbow trout, (Oncorhynchus mykiss): Respiratory toxicity, organ pathologies, and other physiological effects. Aquat Toxicol 82(2), 94109.
Spry, D.J. & Wiener, J.G. (1991). Metal bioavailability and toxicity to fish in low-alkalinity lakes: A critical review. Environ Pollut 71(2), 243304.
Thophon, S., Kruatrachue, M. & Upatham, E.S. (2003). Histopathological alterations of white seabass, Lates calcarifer, in acute and subchronic cadmium exposure. Environ Pollut 121(3), 307320.
Vosyliene, M.Z., Kazlauskiene, N. & Svecevicius, G. (2003). Effect of a heavy metal model mixture on biological parameters of rainbow trout Oncorhynchus mykiss . Environ Sci Pollut Res 10(2), 103107.
Wendelaar, B.S.E. & Lock, R.A.C. (1992). Toxicants and osmoregulation in fish. Neth J Zool 42(2), 478493.
Xue, X., Wang, X., Li, Y., Wang, Y. & Wang, Y. (2011). Acute toxicity and synergism of binary mixtures of antifouling biocides with heavy metals to embryos of sea urchin Glyptocidaris crenularis . Hum Exp Toxicol 30(8), 10091021.


Histopathological Effects on Gills of Nile Tilapia (Oreochromis niloticus, Linnaeus, 1758) Exposed to Pb and Carbon Nanotubes

  • Edison Barbieri (a1), Janaína Campos-Garcia (a1), Diego S. T. Martinez (a2), José Roberto M. C. da Silva (a3), Oswaldo Luiz Alves (a4) and Karina F. O. Rezende (a3)...


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