Titanium dioxide nanoparticles alters routine metabolism and causes histopathological alterations in Oreochromis niloticus


  • Karina Fernandes Oliveira REZENDE
  • Elisa BERGAMI
  • Kelison Venício Brito ALVES
  • Ilaria CORSI
  • Edison BARBIERI




Nile tilapia, nanoparticles, oxygen consumption, ammonia excretion, gills, liver


Titanium Dioxide Nanoparticles (TiO2 NPs) could cause alterations in exposed aquatic species, in terms of oxygen consumption, ammonia excretion and tissues functionality therefore, the aim of the present study is to evaluate the effects of acute exposure to different concentrations of TiO2 NPs (0.1, 0.5, 1.0 and 2.5 mgL-1) on routine metabolism (oxygen consumption and ammonia excretion) and histological parameters (branchial and hepatic) in Oreochromis niloticus. After 24 hours, we observed an increase in oxygen consumption of 2.36 and 3.23 times in groups exposed to 1.0 and 2.5 mgL-1 of TiO2 NPs respectively, as well as an increase in ammonia excretion of 3.54, 4.0 and 4.82 times higher in groups exposed to 0.5, 1.0 and 2.5 mgL-1 of TiO2 NPs respectively, compared to the control group. Histological analysis showed, after 72 hours, moderate to severe alterations in both gills and liver of TiO2  exposed fish at concentrations 1.0 and 2.5 mgL-1, the severity and occurrence of the alteration observed was grade 3 (severe and extensive pathological alterations). We concluded that waterborne exposure of Nile tilapia to TiO2 NPs caused alteration in routine metabolism and histological parameters in a dose-dependent manner.

Nanoparticulas de Dióxido de Tití­¢nio (TiO2NPs) podem causar alterações nas espécies aquáticas expostas, em termos de consumo de oxigênio, excreção de amônia e funcionalidade de tecidos, portanto, o objetivo do presente estudo é avaliar os efeitos da exposição aguda a diferentes concentrações de TiO2NPs (0,1, 0,5, 1,0 e 2,5 mgL-1) sobre o metabolismo de rotina (consumo de oxigênio e excreção de amônia) e parí­¢metros histológicos (branquiais e hepáticos) em Oreochromis niloticus. Após 24 horas, observamos um aumento no consumo de oxigênio de 2,36 e 3,23 vezes em grupos expostos a 1,0 e 2,5 mgL-1 de TiO2NPs respectivamente, bem como um aumento na excreção de amônia de 3,54, 4,0 e 4,82 vezes maior nos grupos expostos a 0,5, 1,0 e 2,5 mgL-1 de TiO2NPs respectivamente, em comparação com o grupo controle. A análise histológica mostrou, após 72 horas, alterações moderadas a severas tanto nas brí­¢nquias quanto no fí­­gado de peixes expostos a TiO2NPs em concentrações de 1,0 e 2,5 mgL-1, a gravidade e a ocorrência da alteração observada foram de grau 3 (alterações patológicas graves e extensas). Concluí­­mos que a exposição í­Â  TiO2NPs da tilápia do Nilo causaram alteração no metabolismo de rotina e nos parí­¢metros histológicos de uma maneira dose-dependente.


ADAM, V.; LOYAUX-LAWNICZAK, S.; LABILLE, J.; GALINDO, C.; DEL NERO, M.; GANGLOFF, S.; WEBER, T.; QUARANTA, G. 2016 Aggregation behaviour of TiO2 nanoparticles in natural river water. Journal of Nanoparticle Research, 18(1): 13. http://dx.doi.org/10.1007/s11051-015-3319-4.

BARBER, D.S.; DENSLOW, N.D.; GRIFFITT, R.J.; MARTYNIUK, C.J. 2009 Sources, fate and effects of engineered nanomaterials in the aquatic environment. In: SAHU, S.C.; CASCIANO, D.A. Nanotoxicity, from in vitro models to health risks. Chichester: John Wiley & Sons. p. 227-245. http://dx.doi.org/10.1002/9780470747803.ch12.

BARBIERI, E.; CAMPOS-GARCIA, J.; MARTINEZ, D.S.T.; 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. http://dx.doi.org/10.1017/S1431927616012009. PMid:27998365.

BARBIERI, E.; FERREIRA, L.A.A. 2011 Effects of the organophosphate pesticide Folidol 600® on the freshwater fish, Nile Tilapia (Oreochromis niloticus). Pesticide Biochemistry and Physiology, 99(3): 209-214.

BARBIERI, E.; FERREIRA, A.C.; REZENDE, K.F.O. 2017a Cadmium effects on shrimp ammonia exetion (Farfantepenaeus paulensis) at differents temperatures and levels. Pan-American Journal of Aquatic Sciences, 12(3): 176-183.

BARBIERI, E.; RUIZ-HIDALGO, K.; REZENDE, K.F.O.; LEONARDO, A.F.G.; SABINO, F.P. 2017b Efectos del carbofuran en juveniles de Oreochromis niloticus en la toxicidad, metabólica de rutina y los parámetros hematológicos. Boletim do Instituto de Pesca, 43(4): 513-526. http://dx.doi.org/10.20950/1678-2305.2017v43n4p513.

CAMPOS-GARCIA, J.; MARTINEZ, D.S.T.; REZENDE, K.F.O.; 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(1): 481-488. http://dx.doi.org/10.1016/j.ecoenv.2016.07.041. PMid:27543744.

CERQUEIRA, C.C.; FERNANDES, M.N. 2002 Gill tissue recovery after copper exposure and blood parameter responses in the tropical fish, Prochilodus scrofa. Ecotoxicology and Environmental Safety, 52(2): 83-91. http://dx.doi.org/10.1006/eesa.2002.2164. PMid:12061823.CHEN, G.X.; LIU, X.Y.; SU, C.M. 2012 Distinct effects of humic acid on transport and retention of TiO2 rutile nanoparticles in saturated sand columns. Environmental Science & Technology, 46(13): 7142-7150. http://dx.doi.org/10.1021/es204010g. PMid:22681399.

CHEN, J.; DONG, X.; XIN, Y.; ZHAO, M. 2011 Effects of titanium dioxide nano-particles on growth and some histological parameters of zebrafish (Danio rerio) after a long-term exposure. Aquatic Toxicology, 101(3-4): 493-499. http://dx.doi.org/10.1016/j.aquatox.2010.12.004. PMid:21276475.DAMATO, M.;

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): 574-581.

DINIZ, M.S.; DE MATOS, A.P.A.; LOURENí­"¡O, J.; CASTRO, L.; PERES, I.; MENDONí­"¡A, E.; PICADO, A. 2013 Liver alterations in two freshwater fish species (Carassius auratus and Danio rerio) following exposure to different TiO2 nanoparticle concentrations. Microscopy and Microanalysis, 19(5): 1131-1140. http://dx.doi.org/10.1017/S1431927613013238. PMid:23931156.

DOI, S.A.; COLLAí­"¡O, 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 í­Â  salinidade. O Mundo da Saúde, 36(4): 594-601.

EVANS, D.H.; PIERMARINI, P.M.; CHOE, K.P. 2005 The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acidí base regulation, and excretion of nitrogenous waste. Physiological Reviews, 85(1): 97-177. http://dx.doi.org/10.1152/physrev.00050.2003. PMid:15618479.

FRY, F.E.J. 1971 The effect of environmental factors on the physiology of fish. In: HOAR, W.S.; RANDALL, D.J. Fish physiology. New York: Academic Press. p. 1-98. http://dx.doi.org/10.1016/S1546-5098(08)60146-6.

GARCIA-SANTOS, S.; FONTAÍNHAS-FERNANDES, A.; WILSON, J.M. 2006 Cadmium tolerance in the Nile tilapia (Oreochromis niloticus) following acute exposure: assessment of some ionoregulatory parameters. Environmental Toxicology, 21(1): 33-46. http://dx.doi.org/10.1002/tox.20152. PMid:16463259.

GIRARDELLO, F.; CUSTÓDIO LEITE, C.; VIANNA VILLELA, I.; SILVA MACHADO, M.; LUIZ MENDES JUCHEM, A.; ROESCH-ELY, M.; NEVES FERNANDES, A.; SALVADOR, M.; ANTONIO Pí­Å GAS HENRIQUES, J. 2016 Titanium dioxide nanoparticles induce genotoxicity but not mutagenicity in golden mussel Limnoperna fortunei. Aquatic Toxicology, 170(1): 223-228. http://dx.doi.org/10.1016/j.aquatox.2015.11.030. PMid:26675368.

GONDIKAS, A.P.; KAMMER, F.; REED, R.B.; WAGNER, S.; RANVILLE, J.F.; HOFMANN, T. 2014 Release of TiO2 nanoparticles from sunscreens into surface waters: a one-year survey at the old Danube recreational Lake. Environmental Science & Technology, 48(10): 5415-5422. http://dx.doi.org/10.1021/es405596y. PMid:24689731.

GOTTSCHALK, F.; SUN, T.; NOWACK, B. 2013 Environmental concentrations of engineered nanomaterials: review of modeling and analytical studies. Environmental Pollution, 181(1): 287-300. http://dx.doi.org/10.1016/j.envpol.2013.06.003. PMid:23856352.

HANAOR, D.; MICHELAZZI, M.; LEONELLI, C.; SORRELL, C.C. 2012 The effects of carboxylic acids on aqueous dispersion and eletroforetic deposition of ZrO2. Journal of the European Ceramic Society, 32(1): 235-244. http://dx.doi.org/10.1016/j.jeurceramsoc.2011.08.015.HANDY, R.D.;

HENRY, T.B.; SCOWN, T.M.; JOHNSTON, B.D.; TYLER, C.R. 2008a Manufactured nanoparticles: their uptake and effects on fish - a mechanistic analysis. Ecotoxicology, 17(5): 396-409. http://dx.doi.org/10.1007/s10646-008-0205-1. PMid:18408995.

HANDY, R.D.; OWEN, R.; VALSAMI-JONES, E. 2008b The ecotoxicology of nanoparticles and nanomaterials: current status, knowledge gaps, challenges, and future needs. Ecotoxicology, 17(5): 315-325. http://dx.doi.org/10.1007/s10646-008-0206-0. PMid:18408994.

HAO, L.; WANG, Z.; XING, B. 2009 Effect of sub-acute exposure to TiO2 nanoparticles on oxidative stress and histopathological changes in juvenile carp (Cyprinus carpio). Journal of Environmental Sciences, 21(10): 1459-1466. http://dx.doi.org/10.1016/S1001-0742(08)62440-7. PMid:20000003.

JAYASEELAN, C.; ABDUL RAHUMAN, A.; RAMKUMAR, R.; PERUMAL, P.; RAJAKUMAR, G.; VISHNU KIRTHI, A.; SANTHOSHKUMAR, T.; MARIMUTHU, S. 2014 Effect of sub-acute exposure to nickel nanoparticles on oxidative stress and histopathological changes in Mozambique tilapia, Oreochromis mossambicus. Ecotoxicology and Environmental Safety, 107(1): 220-228. http://dx.doi.org/10.1016/j.ecoenv.2014.06.012. PMid:25011118.

KAYA, H.; AYDIN, F.; Gí­Å“RKAN, M.; YILMAZ, S.; ATES, M.; DEMIR, V.; ARSLAN, Z. 2016 A comparative toxicity study between small and large size zinc oxide nanoparticles in tilapia (Oreochromis niloticus): Organ pathologies, osmoregulatory responses and immunological parameters. Chemosphere, 144(1): 571-582. http://dx.doi.org/10.1016/j.chemosphere.2015.09.024. PMid:26398925.

KLOTH, T.C.; WOHLSCHIAG, D.E. 1972 Size-related metabolic responses of the pinfish, Lagodon rhomboides, to salinity variations and sublethal petrochemical pollution. Marketing Science, 16(1): 125-137.LEMAIRE, P.; STURVE, J.; FORLIN, L.;

LIVINGSTONE, D.R. 1996 Studies on aromatic hydrocarbon quinone metabolism and DT-diaphorase function in liver of fish species. Marine Environmental Research, 2(1-4): 317-321. http://dx.doi.org/10.1016/0141-1136(95)00042-9.

MACHADO, M.R.; FANTA, E. 2003 Effects of the organophosphorous methyl parathion on the branchial epithelium of a freshwater fish Metynnis roosevelti. Brazilian Archives of Biology and Technology, 46(3): 361-372. http://dx.doi.org/10.1590/S1516-89132003000300008.

MENARD, A.; DROBNE, D.; JEMEC, A. 2011 Exotoxicity of nanosized TiO2- Review of in vivo data. Environmental Pollution, 159(3): 677-684. http://dx.doi.org/10.1016/j.envpol.2010.11.027. PMid:21186069.

MILLER, R.; LENIHAN, H.; MULLER, E.; TSENG, N.; HANNA, S.; KELLER, A. 2010 Impacts of metal oxide nanoparticles on marine phytoplankton. Environmental Science & Technology, 44(19): 7329-7334. http://dx.doi.org/10.1021/es100247x. PMid:20469893.

MIRANDA, R.R.; DAMASO DA SILVEIRA, A.L.R.; JESUS, I.P.; GRí­–TZNER, S.R.; VOIGT, C.L.; CAMPOS, S.X.; GARCIA, J.R.E.; RANDI, M.A.F.; RIBEIRO, C.A.O.; FILIPAK NETO, F. 2016 Effects of realistic concentrations of TiO2 and ZnO nanoparticles in Prochilodus lineatus juvenile fish. Environmental Science and Pollution Research International, 23(6): 5179-5188. http://dx.doi.org/10.1007/s11356-015-5732-8. PMid:26555884.

MONTEIRO, K.M.; CARVALHO, M.O.; ZAHA, A.; FERREIRA, H.B. 2010 Proteomic analysis of the Echinococcus granulosus metacestode during infection of its intermediate host. Proteomics, 10(10): 1985-1999. http://dx.doi.org/10.1002/pmic.200900506. PMid:20217864.

NIGRO, M.; BERNARDESCHI, M.; COSTAGLIOLA, D.; DELLA-TORRE, C.; FRENZILLI, G.; GUIDI, P. ; LUCCHESI, P.; MOTTOLA, F.; SANTONASTASO, M.; SCARCELLI, V.; MONACI, F.; CORSI, I.; STINGO, V. ; ROCCO, L. 2015 n-TiO 2 and CdCl 2 co-exposure to titanium dioxide nanoparticles and cadmium: genomic, DNA and chromosomal damage evaluation in the marine fish European sea bass (Dicentrarchus labrax). Aquatic Toxicology (Amsterdam, Netherlands), 168(1): 72-77. http://dx.doi.org/10.1016/j.aquatox.2015.09.013. PMid:26448269.

PATHIRATNE, A.; GEORGE, S.G. 1998 Toxicity of malathion to Nile tilapia, Oreochromis niloticus and modulation by other environmental contaminants. Aquatic Toxicology (Amsterdam, Netherlands), 43(4): 261-271. http://dx.doi.org/10.1016/S0166-445X(98)00059-9.

POLEKSIC, V.; MITROVIC-TUTUNDZIC, V. 1994 Fish gills as a monitor of sublethal and chronic effects of pollution. In: MULLER, R.; LLOYD, R. Suletha and chronic effects of pollutants on freshwater fish. Rome: FAO. p. 339-352.

REZENDE, K.F.O.; SANTOS, R.M.; BORGES, J.C.S.; SALVO, L.M.; SILVA, J.R.M.C. 2014 Histopathological and genotoxic effects of pollution on Nile Tilapia (Oreochromis niloticus, Linnaeus, 1758) in the Billings Reservoir (Brazil). Toxicology Mechanisms and Methods, 24(6): 404-411. http://dx.doi.org/10.3109/15376516.2014.925020. PMid:24835316.

REZENDE, K.F.O.; SILVA-NETO, G.M.; PINTO, J.M.; SALVO, L.M.; SEVERINO, D.; MORAES, J.C.T.; SILVA, J.R.M.C. 2016 Hepatic parameters of marine fish Rachycentron canadum (Linnaeus, 1766) exposed to sublethal concentrations of water-soluble fraction of petroleum. Journal of Marine Biology and Oceanography, 5(2): 1-6.

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): 16-23.

SCHLENK, D.; HANDY, R.; STEINERT, S.; DEPLEDGE, M.H.; BENSON, W. 2008 Biomarkers. In: GIULIO, R.T.; HINTON, D. The toxicology of fishes. Boca Raton: CRC Press. p. 683-731. http://dx.doi.org/10.1201/9780203647295.ch16.

SCHWAIGER, J.; WANKE, R.; ADAM, S.; PAWERT, M.; HONNEN, W.; TRIEBSKORN, R. 1997 The use of histopathological indicators to evaluate contaminant-related stress in fish. Journal of Aquatic Ecosystem Stress and Recovery, 6(1): 75-86. http://dx.doi.org/10.1023/A:1008212000208.

SHEPHARD, K.L. 1994 Functions for fish mucus. Reviews in Fish Biology and Fisheries, 4(4): 401-429. http://dx.doi.org/10.1007/BF00042888.

SHI, H.; MAGAYE, R.; CASTRANOVA, V.; ZHAO, J. 2013 Titanium dioxide nanoparticles: a review of current toxicological data. Particle and Fibre Toxicology, 10(1): 15. http://dx.doi.org/10.1186/1743-8977-10-15. PMid:23587290.

SUGANTHI, P.; MURALI, M.; HE, S.M.; BASU, H.; SINGHAL, R.K. 2015 Morphological and liver histological effects of ZnO nanoparticles on mozambique tilapia. Journal of Advanced Applied Scientific Research, 1(1): 68-83.

TAKASHIMA, F.; HIBYA, T. 1995 An atlas of fish histology: normal and pathological features. 1ª ed. Tokyo: Kodansha. 213 p.

TAWEEL, A.; SHUHAIMI-O, M.; AHMAD, A.K. 2013 In vivo acute toxicity tests of some heavy metals to tilapia ï¬Âsh (Oreochromis niloticus). The Journal of Biological Sciences, 13(5): 365-371. http://dx.doi.org/10.3923/jbs.2013.365.371.

USPHA í  United States Public Health Association 1980. Standard Methods for the Examination of Water and Wastewater - 4500-NH3. 15th ed. Washington: USPHA.

WESTERS, H. 2001 Fish hatchery management. Bethesda: American Fisheries Society. 733p.

WINKLER, L. 1888 Die Bestimmung des im Wasser gelí­¶sten Sauerstoffes. Berichte der Deutschen Chemischen Gesellschaft, 21(1): 2843-2854. http://dx.doi.org/10.1002/cber.188802102122.

XIONG, D.W.; FANG, T.; YU, L.P.; SIMA, X.F.; ZHU, W.T. 2011 Effects of nano-scale TiO2, ZnO and their bulk counterparts on zebrafish: acute toxicity, oxidative stress and oxidative damage. The Science of the Total Environment, 409(8): 1444-1452. http://dx.doi.org/10.1016/j.scitotenv.2011.01.015. PMid:21296382.

XIONG, S.; GEORGE, S.; JI, Z.; LIN, S.; YU, H.; DAMOISEAUX, R.; FRANCE, B.; NG, K.W.; LOO, S.C.J. 2013 Size of TiO2 nanoparticles influences their phototoxicity: an in vitro investigation. Archives of Toxicology, 87(1): 99-109. http://dx.doi.org/10.1007/s00204-012-0912-5. PMid:22885792.



Most read articles by the same author(s)

1 2 > >>