Titanium dioxide nanoparticles promote histopathological and genotoxic effects in Danio rerio after acute and chronic exposures

Authors

DOI:

https://doi.org/10.5902/2179460X67963

Keywords:

Intestine, Liver, Micronucleus test, Nanotoxicology, Zebrafish

Abstract

Titanium dioxide nanoparticles (TiO2-NPs) are among the most used nanomaterials worldwide, but studies evaluating its genotoxicity and histopathological effects are scarce, dealing with short exposure times and low concentrations for human use. The aim was to evaluate TiO2-NPs genotoxicity and histological alterations in the intestine and liver of zebrafish after exposure to human consumption compatible concentrations. Fishes were acutely (96 hours) and chronically (30 days) exposed to 5.0, 20 and 40 mg L-1 of TiO2-NPs and later euthanized for organ and blood analysis through histological procedures and the micronucleus test, respectively. An increase in the thickness of intestinal villi was observed after acute and chronic exposure in the higher concentrations. The liver showed an increase in vacuolated hepatocytes after both exposures, besides an increase in hepatocytes with peripheral nucleus. Genotoxicity was only observed after chronic exposure, demonstrated by the increase in micronucleus and cell buddings. These findings indicate that TiO2-NPs cause histopathological damage even in acute exposures, as the intestine serves as a barrier for NPs and the liver is an organ that accumulates Ti. Genotoxicity was possibly mediated by reactive oxygen species through chronic inflammation, leading to tissue damage and carcinogenesis in longer exposures that represents human exposure time.

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Author Biographies

Juliana Machado Kayser, Universidade Feevale, Novo Hamburgo, RS, Brasil

Graduated in Biomedicine from Feevale University (2020) and Master's Student (CAPES Scholarship) in Toxicology and Toxicological Analysis from the same institution.

Andriéli Carolina Schuster, Universidade Feevale, Novo Hamburgo, RS, Brasil

Master's student in Toxicology and Toxicological Analysis at Feevale University (2021 - 2023). Degree in Nutrition from the same university (2020).

Gabriela Zimmermann Prado Rodrigues, Universidade Feevale, Novo Hamburgo, RS, Brasil

Graduated in Biomedicine from Feevale University (2015), Master and Doctor (CAPES Scholarship) in Environmental Quality from the same institution. Professor in the Biomedicine and Veterinary Medicine courses at Centro Universitário CESUCA, and coordinator of the Ethics Committee on Animal Use (CEUA) of the institution.

Fernando Dal Pont Morisso, Universidade Feevale, Novo Hamburgo, RS, Brasil

Holds a degree in Chemistry and a Licentiate in Chemistry from the Pontifical Catholic University of Rio Grande do Sul (1995), a Master’s in Chemistry from the Federal University of Rio Grande do Sul (1999) and a PhD in Chemistry from the Federal University of Rio Grande do Sul (2003) in the area of organic chemistry, sub-area of organic synthesis. Is currently a professor of Pharmacy and Chemical Engineering at Feevale University and is a permanent professor in the Professional Postgraduate Program in Materials and Industrial Processes Technology.

Günther Gehlen, Universidade Feevale, Novo Hamburgo, RS, Brasil

Holds a degree in Biological Sciences from UFRGS (1998), a Master's degree in Biological Sciences (Biochemistry) from the Federal University of Rio Grande do Sul (2002) and a PhD in Neurosciences from UFRGS (2009). Is currently an adjunct professor at Feevale University and a member of the PPG-Environmental Quality at this University.

References

ABNT - ASSOCIAÇÃO BRASILEIRA DE NORMAS TÉCNICAS. NBR 15088: Ecotoxicologia aquática - toxicidade aguda - método de ensaio com peixes (Cyprinidae). 2016. Available from: https://www.abntcatalogo.com.br/norma.asp-x?ID=364988. Accessed on: 30 nov. 2020.

AMMENDOLIA, M. G. et al. Short-term oral exposure to low doses of nano-sized TiO2 and potential modulatory effects on intestinal cells. Food Chemical Toxicology, [S.L.], v. 102, p. 63-75, abr. 2017. DOI 10.1016/j.fct.2017.01.031.

ANSES - AGENCE NATIONALE DE SÉCURITÉ SANITAIRE L'ALIMENTATION, DE L'ENVIRONNEMENT ET DU TRAVAIL. Opinion of the French Agency for Food, Environmental and Occupational Health & Safety on the risks associated with ingestion of the food additive E171, 2019. Available from: https://www.anses.fr/en/content/anses-opinion-risks-associated-ingestion-food-additive-e171. Accessed on: 20 oct. 2020.

ANVISA - AGÊNCIA NACIONAL DE VIGILÂNCIA SANITÁRIA. RDC Nº 239, de 26 de julho de 2018: Estabelece os aditivos alimentares e coadjuvantes de tecnologia autorizados para uso em suplementos alimentares, 2018. Available from: http://antigo.anvisa.gov.br/documents/10181/3898839/%283%29RDC_239_2018_COMP.pdf/603b8242-989f-41c3-a9ad-0da61dd59b0c. Accessed on: 17 feb. 2021.

ARENZON, A. et al. A determinação da toxicidade crônica para peixes baseada apenas na sobrevivência é suficiente?. Ecotoxicology and Environmental Contamination, Porto Alegre, v. 8, n. 2, p. 65-68, 2013. DOI 10.5132/eec.2013.02.010.

ASZTEMBORSKA, M. et al. Titanium dioxide nanoparticle circulation in an aquatic ecosystem. Water, Air and Soil Pollution, Poland, v. 229, n. 6, Article ID 208, 2018. DOI 10.1007/s11270-018-3852-8.

ATES, M. et al. Bioaccumulation, subacute toxicity, and tissue distribution of engineered titanium dioxide nanoparticles in Goldfish (Carassius auratus). Journal of Nanomaterials, Turkey, v. 2013, 2013. DOI 10.1155/2013/460518

BAALOUSHA, M. Aggregation and disaggregation of iron oxide nanoparticles: Influence of particle concentration, pH and natural organic matter. Science of the Total Environment, Edgbaston, v. 407, n. 6, p. 2093-2101, 2009. DOI 10.1016/j.scitotenv.2008.11.022.

BAR-ILAN, O. et al. Titanium dioxide nanoparticles produce phototoxicity in the developing zebrafish. Nanotoxicology, Madison, v. 6, n. 6, p. 670-679, 2012. DOI 10.3109/17435390.2011.604438

BETTINI, S. et al. Food-grade TiO2 impairs intestinal and systemic immune homeostasis, initiates preneoplastic lesions and promotes aberrant crypt development in the rat colon. Scientific Reports, Grenoble, v. 7, Article ID 40373, p. 1-13, 2017. DOI 10.1038/srep40373.

BIOLA-CLIER, M. et al. Titanium dioxide nanoparticles alter the cellular phosphoproteome in A549 Cells. Nanomaterials (Basel), France, v. 10, n. 185, 2020. DOI 10.3390/nano10020185.

BLEVINS, L. K. et al. Evaluation of immunologic and intestinal effects in rats administered an E 171-containing diet, a food grade titanium dioxide (TiO2). Food and Chemical Toxicology, USA, v. 133, 2019. DOI 10.1016/j.fct.2019.110793.

BOBORI, D. et al. Common mechanisms activated in the tissues of aquatic and terrestrial animal models after TiO2 nanoparticles exposure. Environment International, Thessaloniki, v. 138, e105611, 2020. DOI 10.1016/j.envint.2020.105611.

BOUWMEESTER, H.; ZANDE, M. V. D.; JEPSON, M. A. Effects of food-borne nanomaterials on gastrointestinal tissues and microbiota. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, Wageningen, v. 10, n. 1, e1481, 2017. DOI 10.1002/wnan.1481.

BOVERHOF, D. R. et al. Comparative assessment of nanomaterial definitions and safety evaluation considerations. Regulatory Toxicology and Pharmacology, St. Paul (MN), v. 73, n. 1, p. 137-150, 2015. DOI 10.1016/j.yrtph.2015.06.001.

BOXALL, A. B. A.; TIEDE, K.; CHAUDHRY, Q. Engineered nanomaterials in soils and water: how do they behave and could they pose a risk to human health? Nanomedicine (Lond), v. 2, n. 6, p. 919-927, 2007. DOI 10.2217/17435889.2.6.919.

BRAND, W. et al. Possible effects of titanium dioxide particles on human liver, intestinal tissue, spleen and kidney after oral exposure. Nanotoxicology, the Netherland, v. 14, n. 7, p. 985-1007, 2020. DOI 10.1080/17435390.2020.1778809.

CARMO, T. L. L. et al. Reactive oxygen species and other biochemical and morphological biomarkers in the gills and kidneys of the Neotropical freshwater fish, Prochilodus lineatus, exposed to titanium dioxide (TiO2) nanoparticles. Environmental Science and Pollution Research International, São Carlos (SP), v. 25, n. 23, p. 22963-22976, 2018. DOI 10.1007/s11356-018-2393-4.

CARMO, T. L. L. et al. Overview of the toxic effects of titanium dioxide nanoparticles in blood, liver, muscles, and brain of a Neotropical detritivorous fish. Environmental Toxicology, São Carlos (SP), v. 34, n. 4, p. 457-468, 2019. DOI 10.1002/TOX.22699.

CARRASCO, K. R.; TILBURY, K. L.; MYERS, M. S. Assessment of the piscine micronucleus test as an in situ biological indicator of chemical contaminant effects. Canadian Journal of Fisheries and Aquatic Sciences, USA, v. 47, n. 11, p. 2123-2136, 1990. DOI 10.1139/f90-237.

CHEN, J. et al. Effects of titanium dioxide nano-particles on growth and some histological parameters of zebrafish (Danio rerio) after a long-term exposure. Aquatic Toxicology, China, v. 101, n. 3–4, p. 493–499, 2011. DOI 10.1016/j.aquatox.2010.12.004.

CHEN, X.-X. et al. Characterization and Preliminary Toxicity Assay of Nano-Titanium Dioxide Additive in Sugar-Coated Chewing Gum. Small, China, v. 9, n. 9–10, p. 1765–1774, 2013. DOI 10.1002/smll.201201506.

CHEN, X.; SCHLUESENER, H. J. Nanosilver: A nanoproduct in medical application. Toxicology Letters, Tuebingen, v. 176, n. 1, p. 1–12, jan. 2008. DOI 10.1016/j.toxlet.2007.10.004.

CHEN, Z. et al. Combined effect of titanium dioxide nanoparticles and glucose on the cardiovascular system in young rats after oral administration. Journal of Applied Toxicology: JAT, China, v. 39, n.4, p. 590-602, 2019. DOI 10.1002/jat.3750.

CLEMENTE, Z. et al. Toxicity assessment of TiO2 nanoparticles in zebrafish embryos under different exposure conditions. Aquatic Toxicology, Campinas (SP), v. 147, p. 129–139, 2014. DOI 10.1016/j.aquatox.2013.12.024.

CRANE, M. et al. Ecotoxicity test methods and environmental hazard assessment for engineered nanoparticles. Ecotoxicology, Faringdon, v. 17, n. 5, p. 421–437, 2008. DOI 10.1007/s10646-008-0215-z.

CUNHA, R. L. D.; BRITO-GITIRANA, L. Effects of titanium dioxide nanoparticles on the intestine, liver, and kidney of Danio rerio. Ecotoxicology and Environmental Safety, Brazil, v. 203, e111032, 2020. DOI 10.1016/j.ecoenv.2020.111032.

DALZOCHIO, T. et al. In situ monitoring of the Sinos River, southern Brazil: water quality parameters, biomarkers, and metal bioaccumulation in fish. Environmental Science and Pollution Research, Brazil, v. 25, 9485, 2018. DOI 10.1007/s11356-018-1244-7.

DEMIR, E. et al. Genotoxic and cell-transforming effects of titanium dioxide nanoparticles. Environmental Research, Spain, v. 136, p. 300-308, 2015. DOI 10.1016/j.envres.2014.10.032.

DUDEFOI, W. et al. Impact of food grade and nano-TiO2 particles on a human intestinal community. Food and Chemical Toxicology, Kingston, v. 106, p. 242–249, 2017. DOI 10.1016/j.fct.2017.05.050.

EFSA - European Food Safety Authority. Re-evaluation of titanium dioxide (E 171) as a food additive. Journal European Food Safety Authority, v. 14, n. 9, 2016.

EPA - U. S. Environmental Protection Agency. Nanomaterial case studies: Nanoscale titanium dioxide in water treatment and in topical sunscreen. 2010. Available from: https://cfpub.epa.gov/ncea/risk/recordisplay.cfm?deid=230972. Accessed on: 7 jan. 2021.

EP - European Parliament. Regulation (EU) 2015/647 of 24 April 2015: Amending and correcting Annexes II and III to Regulation (EC) No 1333/2008 of the European Parliament and of the Council as regards the use of certain food additives, 2015. Available from: https://webgate.ec.europa.eu/foods_system/main/?event=document. view&identifier=17071&documentCrossTable=legislation&documentType=legislation&documentTypeIdentifier=-1 Accessed on: 20 jan. 2021.

FDA - U. S. Food and Drug Administration. Code of Federal Regulations Title 21. 2020. Available from: https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFR Search.cfm?fr=73.1575. Accessed on: 9 mar. 2021.

FEDERICI, G.; SHAW, B. J.; HANDY, R. D. Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): Gill injury, oxidative stress, and other physiological effects. Aquatic Toxicology, Plymouth, v. 84, n. 4, p. 415–430, 2007. DOI 10.1016/j.aquatox.2007.07.009.

FENECH, M. et al. HUMN project: Detailed description of the scoring criteria for the cytokinesis-block micronucleus assay using isolated human lymphocyte cultures. Mutation Research, Adelaide (SA), v. 534, n. 1-2, p. 65-75, 2003. DOI 10.1016/s1383-5718(02)00249-8.

FENECH, M. et al. Molecular mechanisms of micronucleus, nucleoplasmic bridge and nuclear bud formation in mammalian and human cells. Mutagenesis, Australia, v. 26, n. 1, p. 125-132, 2011. DOI 10.1093/mutage/geq052.

FILHO, R. S. et al. Genotoxicity of titanium dioxide nanoparticles and triggering of defense mechanisms in Allium cepa. Genetics and Molecular Biology, Brazil, v. 42, n. 2, p. 425-435, 2019. DOI 10.1590/1678-4685-GMB-2018-0205.

GERLOFF, K. et al. Distinctive toxicity of TiO2 rutile/anatase mixed phase nanoparticles on Caco-2 cells. Chemical Research in Toxicology, Germany, v. 25, n. 3, p. 646-655, 2012. DOI 10.1021/tx200334k.

GRILLO, R.; ROSA, A. H.; FRACETO, L. F. Engineered nanoparticles and organic matter: A review of the state-of-the-art. Chemosphere, Campinas (SP), v. 119, p. 608-619, 2015. DOI 10.1016/j.chemosphere.2014.07.049.

GUO, Z. et al. Titanium dioxide nanoparticle ingestion alters nutrient absorption in an in vitro model of the small intestine. NanoImpact, Ithaca (NY), v. 5, p. 70-82, 2017. DOI 10.1016/j.impact.2017.01.002.

GURR, J. et al. Ultrafine titanium dioxide particles in the absence of photoactivation can induce oxidative damage to human bronchial epithelial cells. Toxicology, Taiwan, v. 213 n. 1-2, p. 66-73, 2005. DOI 10.1016/j.tox.2005.05.007.

HAJIREZAEE, S.; MOHAMMADI, G.; NASERABAD, S. S. The protective effects of vitamin C on common carp (Cyprinus carpio) exposed to titanium oxide nanoparticles (TiO2-NPs). Aquaculture, Iran, v. 518, e734734, 2020. DOI 10.1016/j.aquaculture.2019.734734.

HAO, L.; WANG, Z.; XING, B. Effect of sub-acute exposure to TiO2 nanoparticles on oxidative stress and histopathological changes in Juvenile Carp (Cyprinus carpio). Journal of Environmental Sciences (China), China, v. 21, n. 10, p. 1459-1466, 2009. DOI 10.1016/s1001-0742(08)62440-7.

HAYASHI, M. The micronucleus test: Most widely used in vivo genotoxicity test. Genes Environment, Japan, v. 38, Article ID 18, 2016. DOI 10.1186/s41021-016-0044-x.

HAYES, A. W.; SAHU, S. C. Genotoxicity of engineered nanomaterials found in the human environment. Current Opinion in Toxicology, Florida, v. 19, p. 68-71, 2020. DOI 10.1016/j.cotox.2019.12.003.

HERINGA, M. B., et al. Detection of titanium particles in human liver and spleen and possible health implications. Particle and Fibre Toxicology, The Netherlands, v. 15, n. 1, Article ID 15, 2018. DOI 10.1186/s12989-018-0251-7.

HSU, C. et al. The zebrafish model: Use in studying cellular mechanisms for a spectrum of clinical disease entities. Current Neurovascular Research, Kaohisung, v. 4, n. 2, p. 111-120, 2007. DOI 10.2174/156720207780637234.

HUANG, S. et al. Disturbed mitotic progression and genome segregation are involved in cell transformation mediated by nano-TiO2 long-term exposure. Toxicology and Applied Pharmacology, Taiwan, v. 241, n. 2, p. 182-194, 2009. DOI 10.1016/j.taap.2009.08.013.

IARC - INTERNATIONAL AGENCY FOR RESEARCH ON CANCER. Carbon black, titanium dioxide, and talc. IARC monographs on the evaluation of carcinogenic risks to humans. v. 93, 1st ed., Lyon: International Agency for Research on Cancer, 2010.

ISO - INTERNATIONAL ORGANIZATION FOR STANDARDIZATION. ISO 7346-3:1996: Water quality — Determination of the acute lethal toxicity of substances to a freshwater fish [Brachydanio rerio Hamilton-Buchanan (Teleostei, Cyprinidae)] — Part 3: Flow-through method. ISO, 1996. Available from: https://www.iso.org/standard/14030.html. Accessed on: 20 dec. 2020.

ISWARYA, V. et al. Combined toxicity of two crystalline phases (anatase and rutile) of titania nanoparticles towards freshwater microalgae: Chlorella sp. Aquatic Toxicology, India, v. 161, p. 154-169, 2015. DOI 10.1016/j.aquatox.2015.02.006.

JIA, X. et al. The potential liver, brain, and embryo toxicity of titanium dioxide nanoparticles on mice. Nanoscale Research Letters, China, v. 12, Article ID 478, 2017. DOI 10.1186/s11671-017-2242-2.

JOVANOVIĆ, B. Critical review of public health regulations of titanium dioxide, a human food additive. Integrated Environmental Assessment and Management, Turkey, v. 11, n. 1, p. 10-20, 2015. DOI 10.1002/ieam.1571.

JUGAN, M. -L., et al. Titanium dioxide nanoparticles exhibit genotoxicity and impair DNA repair activity in A549 cells. Nanotoxicology, Gif-sur-Yvette, v. 6, n. 5, p. 501-513, 2012. DOI 10.3109/17435390.2011.587903.

KARLSSON, H. L. et al. Can the comet assay be used reliably to detect nanoparticle-induced genotoxicity? Environmental and Molecular Mutagenesis, Sweden, v. 56, n. 2, p. 82-96, 2015. DOI 10.1002/em.21933.

KAWAHARA, T. et al. Photocatalytic activity of rutile-anatase coupled TiO2 particles prepared by a dissolution-reprecipitation method. Journal of Colloid and Interface Science, Tokyo, v. 267, n. 2, p. 377-381, 2003. DOI 10.1016/s0021-9797(03)00755-0.

KHAN, Z. et al. Toxicity assessment of anatase (TiO2) nanoparticles: a pilot study on stress response alterations and DNA damage studies in Lens culinaris Medik. Heliyon, India, v. 5, n. 7, e02069, 2019. DOI 10.1016/j.heliyon.2019.e02069.

KOTIL, T.; AKBULUT, C.; YÖN, N. D. The effects of titanium dioxide nanoparticles on ultrastructure of zebrafish testis (Danio rerio). Micron, Turkey, v. 100, p. 38-44, 2017. DOI 10.1016/j.micron.2017.04.006.

LAI, S. K. et al. Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus. Proceedings of the National Academy of Sciences of the United States of America, USA, v. 104, n. 5, p. 1482-1487, 2007. DOI 10.1073/pnas.0608611104.

LEE, J. et al. Titanium dioxide nanoparticles oral exposure to pregnant rats and its distribution. Particle and Fibre Toxicology, Deajeon, v. 16, n. 31, p. 1-12, 2019. DOI 10.1186/s12989-019-0313-5.

LI, X., et al. Prebiotic protects against anatase titanium dioxide nanoparticles-induced microbiota-mediated colonic barrier defects. NanoImpact, China, v. 14, e100164, 2019. DOI 10.1016/j.impact.2019.100164.

LI, Y. et al. Genotoxicity and gene expression analyses of liver and lung tissues of mice treated with titanium dioxide nanoparticles. Mutagenesis, USA, v. 32, n. 1, p. 33-46, 2017. DOI 10.1093/mutage/gew065.

MAGDOLENOVA, Z. et al. Impact of agglomeration and different dispersions of titanium dioxide nanoparticles on the human related in vitro cytotoxicity and genotoxicity. Journal of Environmental Monitoring: JEM, Norway, v. 14, n. 2, p. 455-464, 2012. DOI 10.1039/c2em10746e.

MAURICE, P. A.; HOCHELLA, M. F. Chapter 5 Nanoscale particles and processes: A new dimension in soil science. Advences in Agronomy, v. 100, p. 123-153, 2008.

MEDINA-REYES, E. I. et al. Cell cycle synchronization reveals greater G2/M-phase accumulation of lung epithelial cells exposed to titanium dioxide nanoparticles. Environmental Science and Pollution Research International, México, v. 22, n. 5, p. 3976-3982, 2015. DOI 10.1007/s11356-014-3871-y.

MENKE, A. L. et al. Normal anatomy and histology of the adult zebrafish. Toxicologic Pathology, The Netherlands, v. 39, n. 5, p. 759-775, 2011. DOI 10.1177/0192623311409597.

MORGAN, A. et al. Innovative perception on using Tiron to modulate the hepatotoxicity induced by titanium dioxide nanoparticles in male rats. Biomedicine & Pharmacotherapy, Egypt, v. 103, p. 553-561, 2018. DOI 10.1016/j.biopha.2018.04.064.

MU, W. et al. Effect of long-term intake of dietary titanium dioxide nanoparticles on intestine inflammation in mice. Journal of Agricultural and Food Chemistry, China, v. 67, n. 33, p. 9382-9389, 2019. DOI 10.1021/acs.jafc.9b02391.

MURUGADOSS, S. et al. Agglomeration of titanium dioxide nanoparticles increases toxicological responses in vitro and in vivo. Particle and Fibre Toxicology, Belgium, v. 17, Article ID 10, 2020. DOI 10.1186/s12989-020-00341-7.

ORAZIZADEH, M. et al. Effect of glycyrrhizic acid on titanium dioxide nanoparticles-induced hepatotoxicity in rats. Chemico-Biological Interactions, Iran, v. 220, p. 214-221, 2014. DOI 10.1016/j.cbi.2014.07.001.

PICCINNO, F. et al. Industrial production quantities and uses of ten engineered nanomaterials in Europe and the world. Journal Nanoparticle Research, Switzerland, v. 14, e1109, 2012. DOI 10.1007/s11051-012-1109-9.

POWELL, J. J. et al. Origin and fate of dietary nanoparticles and microparticles in the gastrointestinal tract. Journal of Autoimmunity, Cambridge, v. 34, n. 3, p. J226-J233, 2010. DOI 10.1016/j.jaut.2009.11.006.

PRASAD, R. Y. et al. Effect of treatment media on the agglomeration of titanium dioxide nanoparticles: Impact on genotoxicity, cellular interaction, and cell cycle. ACS Nano, North Carolina, v. 7, n. 3, p. 1929-1942, 2013. DOI 10.1021/nn302280n.

PURUSHOTHAMAN, S. et al. Acute exposure to titanium dioxide (TiO2) induces oxidative stress in zebrafish gill tissues. Toxicological & Environmental Chemistry, India, v. 96, n. 6, p. 890-905, 2014. DOI 10.1080/02772248.2014.987511.

ROBICHAUD, C. O. et al. Estimates of upper bounds and trends in nano-TiO2 production as a basis for exposure assessment. Environmental Science & Technology, Durham, v. 43, n. 12, p. 4227-4233, 2009. DOI 10.1021/es8032549.

ROCCO, L. et al. Genotoxicity assessment of TiO2 nanoparticles in the teleost Danio rerio. Ecotoxicology and Environmental Safety, Caserta, v. 113, p. 223-230, 2015. DOI 10.1016/j.ecoenv.2014.12.012.

RODRIGUES, G. Z. P. et al. Evaluation of intestinal histological damage in zebrafish exposed to environmentally relevant concentrations of manganese. Ciência e Natura, Brasil, v. 40, e52, 2018. DOI 10.5902/2179460X31681.

RODRIGUES, G. Z. P. et al. Histopathological, genotoxic, and behavioral damages induced by manganese (II) in adult zebrafish. Chemosphere, Brazil, v. 244, e125550, 2020. DOI 10.1016/j.chemosphere.2019.125550.

ROMPELBERG, C. et al. Oral intake of added titanium dioxide and its nanofraction from food products, food supplements and toothpaste by the Dutch population. Nanotoxicology, The Netherlands, v. 10, n. 10, p. 1404-1414, 2016. DOI 10.1080/17435390.2016.1222457.

RYU, B. et al. Development of an alternative zebrafish model for drug-induced intestinal toxicity. Journal of Applied Toxicology, Republic of Korea, v. 38, n. 2, p. 259-273, 2018. DOI 10.1002/jat.3520.

SAYES, C. M. et al. Correlating nanoscale titania structure with toxicity: A cytotoxicity and inflammatory response study with human dermal fibroblasts and human lung epithelial cells. Toxicological Sciences: an official journal of the Society of Toxicology, Houston (TX), v. 92, n. 1, p. 174-185, 2006. DOI 10.1093/toxsci/kfj197.

SIPES, N. S.; PADILLA, S.; KNUDSEN, T. B. Zebrafish: As an integrative model for twenty-first century toxicity testing. Birth Defects Research. Part C, Embryo Today: Reviews, North Carolina, v. 93, n. 3, p. 256-267, 2011. DOI 10.1002/bdrc.20214.

STICE, S. A. et al. Chapter 44 - Genotoxicity biomarkers: Molecular basis of genetic variability and susceptibility. In: GUPTA, R. C. (ed.). Biomarkers in Toxicology, 2019, 2nd ed., p. 807-821. DOI 10.1016/C2017-0-01788-3.

STROBEL, C. et al. Effects of the physicochemical properties of titanium dioxide nanoparticles, commonly used as sun protection agents, on microvascular endothelial cells. Journal of Nanoparticle Research, Germany, v. 16, n. 1, e2130, 2014. DOI 10.1007/s11051-013-2130-3.

TANG, T.; ZHANG, Z.; ZHU, X. Toxic effects of TiO2 NPs on zebrafish. International Journal of Environmental Research and Public Health, China, v. 16, n. 4, e523, p. 1-14, 2019. DOI 10.3390/ijerph16040523.

TAVARES, A. M. et al. Genotoxicity evaluation of nanosized titanium dioxide, synthetic amorphous silica and multi-walled carbon nanotubes in human lymphocytes. Toxicology In Vitro, Portugal, v. 28, n. 1, p. 60-69, 2014. DOI 10.1016/j.tiv.2013.06.009.

TERISSE, H. et al. Monodispersed titanium oxide nanoparticles in N,N-dimethylformamide: Water solutions. Journal of Sol-Gel Science and Technology, France, v. 67, p. 288-296, 2013. DOI 10.1007/s10971-013-3078-6.

THOMAS, C. R. et al. Nanomaterials in the environment: From materials to high-throughput screening to organisms. ACS Nano, United States, v. 5, n. 1, p. 13-20, 2011. DOI 10.1021/nn1034857.

TROUILLER, B. et al. Titanium dioxide nanoparticles induce DNA damage and genetic instability in vivo in mice. Cancer Research, USA, v. 69, n. 22, p. 8784-8789, 2009. DOI 10.1158/0008-5472.CAN-09-2496.

TUNÇSOY, M. Impacts of titanium dioxide nanoparticles on serum parameters and enzyme activities of Clarias gariepinus. Bulletin of Environmental Contamination and Toxicology, Turkey, v. 106, n. 4, p. 629-636, 2021. DOI 10.1007/s00128-020-03100-8.

URRUTIA-ORTEGA, I. M. et al. Food-grade titanium dioxide exposure exacerbates tumor formation in colitis associated cancer model. Food and Chemical Toxicology, Mexico, v. 93, p. 20-31, 2016. DOI 10.1016/j.fct.2016.04.014.

VELZEBOER, I. et al. Nanomaterials in the environment: Aquatic ecotoxicity tests of some nanomaterials. Environmental Toxicology and Chemistry, Bilthoven, v. 27, n. 9, p. 1942-1947, 2008. DOI 10.1897/07-509.1.

VIDYA, P. V.; CHITRA, K. C. Evaluation of genetic damage in Oreochromis mossambicus exposed to selected nanoparticles by using micronucleus and comet bioassays. Croatian Journal of Fisheries, India, v. 76, n. 3, p. 115-124, 2018. DOI 10.2478/cjf-2018-0015.

VIGNARDI, C. P. et al. Genotoxicity, potential cytotoxicity and cell uptake of titanium dioxide nanoparticles in the marine fish Trachinotus carolinus (Linnaeus, 1766). Aquatic Toxicology, São Paulo, v. 158, p. 218-229, 2015. DOI 10.1016/j.aquatox.2014.11.008.

WANG, Z.; LUO, Z.; YAN, Y. Dispersion and sedimentation of titanium dioxide nanoparticles in freshwater algae and daphnia aquatic culture media in the presence of arsenate. Journal of Experimental Nanoscience, China, v. 13, n. 1, p. 119-129, 2018. DOI 10.1080/17458080.2018.1449023.

WANI, M. R.; SHADAB, G. G. H. A. Titanium dioxide nanoparticle genotoxicity: A review of recent in vivo and in vitro studies. Toxicology and Industrial Health, India, v. 36, n. 7, p. 514-530, 2020. DOI 10.1177/0748233720936835.

WEIR, A. et al. Titanium dioxide nanoparticles in food and personal care products. Environmental Science & Technology, Arizona, v. 46, n. 4, p. 2242-2250, 2012. DOI 10.1021/es204168d.

WILSON, J. M.; LAURENT, P. Fish gill morphology: Inside out. Journal of Experimental Zoology, Portugal, v. 293, n. 3, p. 192-213, 2002. DOI 10.1002/jez.10124.

WOLF, J. C.; WHEELER, J. R. A critical review of histopathological findings associated with endocrine and non-endocrine hepatic toxicity in fish models. Aquatic Toxicology, USA, v. 197, p. 60-78, 2018. DOI 10.1016/j.aquatox.2018.01.013.

WOLF, J. C.; WOLFE, M. J. A brief overview of nonneoplastic hepatic toxicity in fish. Toxicologic Pathology, USA, v. 33, n. 1, p. 75-85, 2005. DOI 10.1080/01926230590890187

YANG, Y. et al. Characterization of food-grade titanium dioxide: The presence of nanosized particles. Environmental Science & Technology, Arizona, v. 48, n. 11, p. 6391-6400, 2014. DOI 10.1021/es500436x.

YIN, C. et al. TiO2 particles in seafood and surimi products: Attention should be paid to their exposure and uptake through foods. Chemosphere, China, v. 188, p. 541-547, 2017. DOI 10.1016/j.chemosphere.2017.08.168.

ZHU, X. et al. Trophic transfer of TiO(2) nanoparticles from Daphnia to zebrafish in a simplified freshwater food chain. Chemosphere, Tempe (AZ), v. 79, n. 9, p. 928-933, 2010. DOI 10.1016/j.chemosphere.2010.03.022.

ZHU, X. et al. Long-term exposure to titanium dioxide nanoparticles promotes diet-induced obesity through exacerbating intestinal mucus layer damage and microbiota dysbiosis. Nano Research, China, v. 14, n. 5 p. 1512-1522, 2020. DOI 10.1007/s12274-020-3210-1.

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2022-05-23 — Updated on 2022-05-31

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Machado Kayser, J., Carolina Schuster, A., Zimmermann Prado Rodrigues, G., Dal Pont Morisso, F., & Gehlen, G. (2022). Titanium dioxide nanoparticles promote histopathological and genotoxic effects in Danio rerio after acute and chronic exposures. Ciência E Natura, 44, e19. https://doi.org/10.5902/2179460X67963 (Original work published May 23, 2022)

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Vol. 44 (2022): Continuous Publication

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Environment

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