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Evaluation of coexposure to inorganic arsenic and titanium dioxide nanoparticles in the marine shrimp Litopenaeus vannamei

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Abstract

The acute toxicity of titanium dioxide nanoparticles (nTiO2) that occur concomitantly in the aquatic environment with other contaminants such as arsenic (As) is little known in crustaceans. The objective of the present study is to evaluate whether coexposure to nTiO2 can influence the accumulation, metabolism, and oxidative stress parameters induced by arsenic exposure in the gills and hepatopancreas of the shrimp Litopenaeus vannamei. Organisms were exposed by dissolving chemicals in seawater (salinity = 30) at nominal concentrations of 10 μg/L nTiO2 or AsIII, dosed alone and in combination. Results showed that there was not a significant accumulation of As in either tissue type, but the coexposure altered the pattern of the metabolism. In the hepatopancreas, no changes were observed in the biochemical response, while in the gills, an increase in the glutamate-cysteine-ligase (GCL) activity was observed upon exposure to As or nTiO2 alone, an increase in the reduced glutathione (GSH) levels was observed upon exposure to As alone, and an increase in the total antioxidant capacity was observed upon exposure to nTiO2 or nTiO2 + As. However, these modulations were not sufficient enough to prevent the lipid damage induced by nTiO2 exposure. Our results suggest that coexposure to nTiO2 and As does not alter the toxicity of this metalloid in the gills and hepatopancreas of L. vannamei but does alter its metabolism, favoring its accumulation of organic As species considered moderately toxic.

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References

  • Abedin MJ, Cresser MS, Meharg AA, Feldmann J, Cotter-Howells J (2002) Arsenic accumulation and metabolism in rice (Oryza sativa L.). Environ Sci Technol 36:962–968

    Article  CAS  Google Scholar 

  • Aitken RJ, Chaudhry MQ, Boxall ABA, Hull M (2006) Manufacture and use of nanomaterials: current status in the UK and global trends. Occup Med 56:300–306. doi:10.1093/occmed/kql051

    Article  CAS  Google Scholar 

  • Akter KF, Owens G, Davey DE, Naidu R (2005) As speciation and toxicity in biological systems. Rev environ contamt 184:97–149

    CAS  Google Scholar 

  • Amado LL, Garcia ML, Ramos PB, Freitas RF, Zafalon B, Ferreira JLR, Yunes JS, Monserrat JM (2009) A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: Application to evaluate microcystins toxicity. Sci Total Environ 407:2115–2123. doi:10.1016/j.scitotenv.2008.11.038

    Article  CAS  Google Scholar 

  • Aposhian HV (1997) Enzymatic methylation of As species and other new approaches to As toxicity. Annu Rev Pharmacol 37:397–419

    Article  CAS  Google Scholar 

  • Baan RA (2007) Carcinogenic Hazards from Inhaled Carbon Black, Titanium Dioxide, and Talc not Containing Asbestos or Asbestiform Fibers: Recent Evaluations by an IARC Monographs Working Group. Inhal Toxicol 19:213–228. doi:10.1080/08958370701497903

    Article  CAS  Google Scholar 

  • Bagnyuokova TV, Luzha LI, Pogribny IP, Lushchak VI (2007) Oxidative stress and antioxidant defenses in goldfish liver in response to short-term exposure to arsenite. Environ Mol Mutagen 48:658–665

    Article  CAS  Google Scholar 

  • Benhima H, Chiban M, Sinan F, Seta P, Persin M (2008) Removal of lead and cadmium ions from aqueous solution by adsorption onto micro-particles of dry plants. Colloids Surf B Biointerfaces 61:10–16. doi:10.1016/j.colsurfb.2007.06.024

    Article  CAS  Google Scholar 

  • Boado RJ, Hui EK-W, Lu JZ, Sumbria RK, Pardridge WM (2013) Blood-brain Barrier Molecular Trojan Horse Enables Imaging of Brain Uptake of Radioiodinated Recombinant Protein in the Rhesus Monkey. Bioconjug Chem 24:1741–1749. doi:10.1021/bc400319d

    Article  CAS  Google Scholar 

  • Borm PJA, Schins RPF, Albrecht C (2004) Inhaled particles and lung cancer, part B: Paradigms and risk assessment. Int J Cancer 110:3–14. doi:10.1002/ijc.20064

    Article  CAS  Google Scholar 

  • Briggs M, Funge-Smith S, Subasinghe R, Phillips M (2004) Introductions and movement of Penaeus vannamei and Penaeus stylirostris in Asia and the Pacific. RAP Publ 10:92

    Google Scholar 

  • Canesi L, Ciacci C, Fabbri R, Marcomini A, Pojana G, Gallo G (2012) Bivalve molluscs as a unique target group for nanoparticle toxicity. Mar Environ Res Emerging and persistent impacts on Marine Organisms: Detection methods and action mechanisms 76:16–21. doi:10.1016/j.marenvres.2011.06.005

    CAS  Google Scholar 

  • Chiban M, Zerbet M, Carja G, Sinan F (2012) Application of low-cost adsorbents for arsenic removal: A review. J Environ Chem Ecotoxicol 4. doi:10.5897/JECE11.013

  • Clemente Z, Castro VL, Jonsson CM, Fraceto LF (2011) Ecotoxicology of nano-TiO2 – an evaluation of its toxicity to organisms of aquatic ecosystems. Int J Environ Res 6:33–50

    Google Scholar 

  • Conselho Nacional do Meio Ambiente (2005) Resolução do Conama, N° 357. Brasília: Diário Oficial da União (www.mma.gov.br/port/conama/res/res05/res35705.pdf). Accessed 20 Sep 2014

  • Costa CLA, Chaves IS, Ventura-Lima J, Ferreira JLR, Ferraz L, Carvalho LM, Monserrat JM (2012) In vitro evaluation of co-exposure of arsenium and organical nanomaterial (fullerene; C60) in zebrafish hepatocyte. Comp Biochem Phys C 155:206–212

    Google Scholar 

  • Dabeka RW, McKenzie AD, Lacroix GM, Cleroux C, Bowe S, Graham RA, Conacher HB, Verdier P (1993) Survey of arsenic in total diet food composites and estimation of the dietary intake of arsenic by Canadian adults and children. J AOAC Int 76:14–25

    CAS  Google Scholar 

  • Dankovic D, Kuempel E, Wheeler M (2007) An Approach to Risk Assessment for TiO2. Inhal Toxicol 19:205–212. doi:10.1080/08958370701497754

    Article  CAS  Google Scholar 

  • Fan W, Cui M, Liu H, Wang C, Shi Z, Tan C, Yan X (2011) Nano-TiO2 enhances the toxicity of copper in natural water to Daphnia magna. Environ Pollut 159:729–734

    Article  CAS  Google Scholar 

  • Fattorini D, Regoli F (2004) Arsenic speciation in tissues of the Mediterranean polychaete Sabella spalanzanii. Environ Toxicol Chem 23:1881–1887

    Article  CAS  Google Scholar 

  • Fattorini D, Notti A, Halt MN, Gambi MC, Regoli F (2005) Levels and chemical speciation of arsenic in polychaetes: a review. Mar Ecol 26:255–264

    Article  CAS  Google Scholar 

  • Fattorini D, Notti A, Regoli F (2006) Characterization of arsenic content in marine organisms from temperate, tropical, and polar environments. Chem Ecol 22:405–414

    Article  CAS  Google Scholar 

  • Ferreira JLR, Lonné NM, França T, Maximilla NR, Lugokenski T, Costa PG, Filmann G, Soares FAA, de La Torre FR, Monserrat JM (2014) Co-exposure of the organic nanomaterial fullerene C60 with benzo[a]pyrene in Danio rerio (zebrafish) hepatocytes: Evidence of toxicological interactions. Aquat Toxicol 147:76–83

    Article  CAS  Google Scholar 

  • Ferreira-Cravo M, Piedras FR, Moraes TB, Ferreira JLR, de Freitas DPS, Machado MD, Geracitano LA, Monserrat JM (2007) Antioxidant responses and reactive oxygen species generation in different body regions of the estuarine polychaeta Laeonereis acuta (Nereididae). Chemosphere 66:1367–1374. doi:10.1016/j.chemosphere.2006.06.050

    Article  CAS  Google Scholar 

  • French RA, Jacobson AR, Kim B, Isley SL, Penn RL, Baveye PC (2009) Influence of Ionic Strength, pH, and Cation Valence on Aggregation Kinetics of Titanium Dioxide Nanoparticles. Environ Sci Technol 43:1354–1359. doi:10.1021/es802628n

    Article  CAS  Google Scholar 

  • Gallagher SR (1992) GUS Protocols: using the GUS gene as a reporter of gene expression. Academic Press

  • Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine. Oxford University Press

  • 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). J Environ Sci 21:1459–1466. doi:10.1016/S1001-0742(08)62440-7

    Article  CAS  Google Scholar 

  • Hristovski K, Baumgardner A, Westerhoff P (2007) Selecting metal oxide nanomaterials for arsenic removal in fixed bed columns: From nanopowders to aggregated nanoparticle media. J Hazard Mater 147:265–274. doi:10.1016/j.jhazmat.2007.01.017

    Article  CAS  Google Scholar 

  • Huang Y-K, Lin K-H, Chen H-W, Chang C-C, Liu C-W, Yang M-H, Hsueh Y-M (2003) Arsenic species contents at aquaculture farm and in farmed mouthbreeder (Oreochromis mossambicus) in blackfoot disease hyperendemic areas. Food Chem Toxicol 41:1491–1500. doi:10.1016/S0278-6915(03)00165-0

    Article  CAS  Google Scholar 

  • Järup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182. doi:10.1093/bmb/ldg032

    Article  Google Scholar 

  • Jegadeesan G, Al-Abed SR, Sundaram V, Choi H, Scheckel KG, Dionysiou DD (2010) Arsenic sorption on TiO2 nanoparticles: Size and crystallinity effects. Water Res 44:965–973. doi:10.1016/j.watres.2009.10.047

    Article  CAS  Google Scholar 

  • Kanwar JR, Samarasinghe RM, Sehgal R, Kanwar RK (2012) Nano-lactoferrin in diagnostic, imaging and targeted delivery for cancer and infectious diseases. J Cancer Sci Ther 4:31–42

    CAS  Google Scholar 

  • Kim J-H, Kang J-C (2015) The arsenic accumulation and its effect on oxidative stress responses in juvenile rockfish, Sebastes schlegelii, exposed to waterborn arsenic (As+3). Environ Toxicol Phar 39:668–672

    Article  CAS  Google Scholar 

  • Klaine SJ, Alvarez PJJ, Batley GE, Fernandes TF, Handy RD, Lyon DY, Mahendra S, McLaughlin MJ, Lead JR (2008) Nanomaterials in the Environment: behavior, fate, bioavailability and effects. Environ Toxicol Chem 27:1825–1851

    Article  CAS  Google Scholar 

  • Kubota R, Kunito T, Tanabe S (2001) Arsenic accumulation in the liver tissue of marine mammals. Environ Pollut 115:303–312. doi:10.1016/S0269-7491(01)00099-9

    Article  CAS  Google Scholar 

  • Larsen EH, Moseholm L, Nielsen MM (1992) Atmospheric deposition of trace elements around point sources and human health risk assessment. II: Uptake of arsenic and chromium by vegetables grown near a wood preservation factory. Sci Total Environ 126:263–275. doi:10.1016/0048-9697(92)90201-3

    Article  CAS  Google Scholar 

  • Li B, Li X, Zhu B, Zhang X, Wang Y, Xu Y, Wang H, Hou Y, Zheng Q, Sun G (2011) Sodium arsenite induced reactive oxygen species generation, nuclear factor (erythroid-2 related) factor 2 activation, heme-oxygenase-1 expression, and glutathione elevation in Chang human hepatocytes. Environ Toxicol 1:401–410

    Google Scholar 

  • Limbach KL, Wich P, Manser P, Grass RN, Bruinink A, Stark WI (2007) Exposure of Engineered Nanoparticles to Human Lung Epithelial Cells: Influence of Chemical Composition and Catalytic Activity on Oxidative Stress. Environ Sci Technol 41:4158–4163

    Article  CAS  Google Scholar 

  • Linhua H, Zhenyu W, Baoshan X (2009) Effect of sub-acute exposure to TiO2 nanoparticles on oxidative stress and histopathological changes in Juvenile Carp (Cyprinus carpio). J Environ Sci 21:1459–1466

    Article  CAS  Google Scholar 

  • Llobet JM, Falcó G, Casas C, Teixidó A., Domingo JL (2003) Concentrations of arsenic, cadmium, mercury, and lead in common foods and estimated daily intake by children, adolescents, adults, and seniors of Catalonia, Spain. J Agric Food Chem. 51:838–842.

  • Lobato RO, Manske SN, Wasielesky W, Fattorini D, Regoli F, Monserrat JM, Ventura-Lima J (2013) The role of lipoic acid against of metallic pollutant effect in the shrimp Litopenaeus vannamei (Crustacea; Decapoda). Comp Biochem Phys A 491–497

  • Ma L, Tu SX (2011) Removal of arsenic from aqueous solution by two types of nano TiO2 crystals. Environ Chem Lett 9:464–472

    Article  CAS  Google Scholar 

  • Masserini M (2013) Nanoparticles for brain drug delivery. Int Sch Res 2013:18 ID:e238428. doi:10.1155/2013/238428

  • Meharg AA, Rahman MM (2003) Arsenic Contamination of Bangladesh Paddy Field Soils: Implications for Rice Contribution to Arsenic Consumption. Environ Sci Technol 37:229–234. doi:10.1021/es0259842

    Article  CAS  Google Scholar 

  • Menard A, Drobne D, Jemec A (2011) Ecotoxicity of nanosized TiO2. Review of in vivo data. Environ Pollut 159:677–684

    Article  CAS  Google Scholar 

  • Mirlean N, Roseiberg A (2006) The effect of emissions of fertilizer production on the environment contamination by cadmium and arsenic in southern Brazil. Environ Pollut 143:335–340

    Article  CAS  Google Scholar 

  • Mueller NC, Nowack B (2008) Exposure modeling of engineered nanoparticles in the environment. Environ Sci Technol 42:4447–4453

    Article  CAS  Google Scholar 

  • Nabi D, Aslam I, Qazi IA (2009) Evaluation of the adsorption potential of titanium dioxide nanoparticles for arsenic removal. J Environ Sci 21:402–408. doi:10.1016/S1001-0742(08)62283-4

    Article  CAS  Google Scholar 

  • Nasreddine L, Parent-Massin D (2002) Food contamination by metals and pesticides in the European Union. Should we worry? Toxicol Lett 127:29–41. doi:10.1016/S0378-4274(01)00480-5

    Article  CAS  Google Scholar 

  • Oakes KD, Van Der Kraak GJ (2003) Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquat Toxicol 63:447–463. doi:10.1016/S0166-445X(02)00204-7

    Article  CAS  Google Scholar 

  • Olivo M, Lucky SS, Bhuvaneswari R, Dendukuri N (2011) Nano-sensitizers for multi-modality optical diagnostic imaging and therapy of cancer. SPIE Proc.;8087:8087T

  • Olmedo P, Pla A, Hernández AF, Barbier F, Ayouni L, Gil F (2013) Determination of toxic elements (mercury, cadmium, lead, tin and arsenic) in fish and shellfish samples. Risk assessment for the consumers. Environ Int 59:63–72.

  • Park E-H, Yi J, Kim Y, Choi K, Park K (2010) Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism. Toxicol In Vitro 24:872–878

    Article  CAS  Google Scholar 

  • Pena ME, Korfiatis GP, Patel M, Lippinott L, Ming X (2005) Adsorption of As(V) and As(III) by nanocrystalline titanium dioxide. Water Res 2327–2337

  • Pena M, Meng X, Korfiatis GP, Jing C (2006) Adsorption Mechanism of Arsenic on Nanocrystalline Titanium Dioxide. Environ Sci Technol 40:1257–1262. doi:10.1021/es052040e

    Article  CAS  Google Scholar 

  • Petković J, Žegura B, Filipić M (2011) Influence of titanium dioxide nanoparticles on cellular antioxidant defense and its involvement in genotoxicity in HepG2 cells. J Phys 304:1–8

    Google Scholar 

  • Reeves JF, Davies SJ, Dodd NJF, Jha AN (2008) Hydroxyl radicals (OH) are associated with titanium dioxide (TiO2) nanoparticle-induced cytotoxicity and oxidative DNA damage in fish cells. Mutat Res Mol Mech Mutagen 640:113–122. doi:10.1016/j.mrfmmm.2007.12.010

    Article  CAS  Google Scholar 

  • Ren X, Gaile DP, Gong Z, Qiu W, Ge Y, Zhang C, Huang C, Yan H, Olson JR, Kavanagh TI, Wu H (2015) Arsenic response to microRNAs in vivo in their potential involvement in arsenic-induced oxidative stress. Toxicol Appl Pharm 283:198–205

    Article  CAS  Google Scholar 

  • Schuliga M, Chouchane S, Snow ET (2002) Upregulation of glutathione-related genes and enzyme activities in cultured of human cells by sublethal concentrations of inorganic arsenic. Toxicol Sci 70:183–192

    Article  CAS  Google Scholar 

  • Shaw JR, Glaholt SP, Greenberg NS, Sierra-Alvarez R, Folt CL (2007) Acute toxicity of arsenic to Daphnia pulex: influence of organic functional groups and oxidation state. Environ Toxicol Chem 26:1532–1537

    Article  CAS  Google Scholar 

  • Smedley PL, Kinniburgh DG (2002) A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem 17:517–568. doi:10.1016/S0883-2927(02)00018-5

    Article  CAS  Google Scholar 

  • Stenehjem DD, Hartz AM, Bauer B, Anderson GW (2009) Novel and emerging strategies in drug delivery for overcoming the blood–brain barrier. Future Med Chem 1:1623–1641. doi:10.4155/fmc.09.137

    Article  CAS  Google Scholar 

  • Sun H, Zhang X, Niu Q, Chen Y, Crittenden JC (2007) Enhanced Accumulation of Arsenate in Carp in the Presence of Titanium Dioxide Nanoparticles. Water Air Soil Poll 178:245–254

    Article  CAS  Google Scholar 

  • Sun Q, Tan D, Zhou Q, Liu X, Cheng Z, Liu G, Zhu M, Sang X, Gui S, Cheng J, Hu R, Tang M, Hong F (2012) Oxidative damage of lung and its protective mechanism in mice caused by long-term exposure to titanium dioxide nanoparticles. J Biomed Mater Res-A 100A:2554–2562

    Article  CAS  Google Scholar 

  • Trouiller B, Reliene R, Westbrook A, Solaimani P, Schiestl RH (2009) Titanium Dioxide Nanoparticles Induce DNA Damage and Genetic Instability In vivo in Mice. Cancer Res 69:8784–8789. doi:10.1158/0008-5472.CAN-09-2496

    Article  CAS  Google Scholar 

  • Tu HT, Silvestre F, Wang N, Thome J-P, Phuong NT, Kestemont P (2010) A multi-biomarker approach to assess the impact of farming systems on black tiger shrimp (Penaeus monodon). Chemosphere 81:1204–1211. doi:10.1016/j.chemosphere.2010.09.039

    Article  CAS  Google Scholar 

  • Ventura-Lima J, Fattorini D, Regoli F, Monserrat JM (2009a) Effects of different inorganic arsenic species in Cyprinus carpio (Cyprinidae) tissues after short-time exposure: bioaccumulation, biotransformation and biological responses. Environ Poll 157:3479–3484

    Article  CAS  Google Scholar 

  • Ventura-Lima J, Castro MR, Acosta D, Fattorini D, Regoli F, Carvalho LM, Bohrer D, Geracitano LA, Barros DM, Silva RS, Bonan CD, Bogo MR, Monserrat JM (2009b) Effects of arsenic (As) exposure on the antioxidant status of gills of the zebrafish Danio rerio (Cypridinae). Comp Biochem Physiol 149C:538–543

    CAS  Google Scholar 

  • Ventura-Lima J, Bogo MR, Monserrat JM (2011) Arsenic toxicity in mammals and aquatic animals: A comparative biochemical approach. Ecotoxicol Environ Saf 74:211–218. doi:10.1016/j.ecoenv.2010.11.002

    Article  CAS  Google Scholar 

  • White CC, Viernes H, Krejsa CM, Botta D, Kavanagh TJ (2003) Fluorescencebased microtiter plate assay for glutamate-cysteine ligase activity. Anal Biochem 318:175–180

    Article  CAS  Google Scholar 

  • Winston GW, Regoli F, Dugas AJ Jr, Fong JH, Blanchard KA (1998) A Rapid Gas Chromatographic Assay for Determining Oxyradical Scavenging Capacity of Antioxidants and Biological Fluids. Free Radic Biol Med 24:480–493. doi:10.1016/S0891-5849(97)00277-3

    Article  CAS  Google Scholar 

  • Wu X, Gao M, Wang L, Luo Y, Bi R, Li L, Xie L (2014) The arsenic content in marketed seafood and associated health risks for the residents of Shandong, China. Ecotoxicol Environ Saf 102:168–173. doi:10.1016/j.ecoenv.2014.01.028

    Article  CAS  Google Scholar 

  • Yamanaka K, Hasegawa A, Sawamura R, Okada S (1991) Cellular response to oxidative damage in lung induced by administration of dimethylarsinic acid, a major metabolite of inorganic arsenics, in mice. Toxicol Appl Pharm 108:205–213

    Article  CAS  Google Scholar 

  • Yamanaka K, Katsumata K, Ikuma K, Hasegawa A, Nakano M, Okada S (2000) The role of orally administered dimethylarsinic acid, a main metabolite of inorganic arsenics in the promotion and progression of UVB-induced skin tumorogenesis in hairless mice. Cancer Lett 152:79–85

    Article  CAS  Google Scholar 

  • Zar JH (1984) Biostatistical Analysis. Prentice Hall, New Jersey

    Google Scholar 

  • Zhang R, Niu Y, Li Y, Zhao C, Song B, Li Y, Zhou Y (2010) Acute toxicity study of the interaction between titanium dioxide nanoparticles and lead acetate in mice. Environ Toxicol Pharmacol 30:52–60. doi:10.1016/j.etap.2010.03.015

    Article  CAS  Google Scholar 

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Acknowledgments

The authors wish to thank CNPq for financial support (MCTI/CNPq process no 17/2011). Lucas Cordeiro is a graduate fellow at Fundação de Amparo à Pesquisa do Rio Grande do Sul (FAPERGS). Larissa Müller is an undergraduate at FAPERGS. José M. Monserrat and Wilson Wasielesky are research fellows at CNPq. Juliane Ventura-Lima and José M. Monserrat are members of the nanotoxicology network “Nanotoxicologia ocupacional e ambiental: subsídios científicos para estabelecer marcos regulatórios e avaliação de riscos” (CNPq, Proc. 552131/2011-3).

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Authors and Affiliations

  1. Instituto de Ciências Biológicas (ICB), Universidade Federal do Rio Grande - FURG, Rio Grande, RS, Brazil

    Lucas Cordeiro, Larissa Müller, José Marìa Monserrat & Juliane Ventura-Lima

  2. Programa de Pós-Graduação em Ciências Fisiológicas-Fisiologia Animal Comparada-FURG, Rio Grande, RS, Brazil

    Lucas Cordeiro, José Marìa Monserrat & Juliane Ventura-Lima

  3. Programa de Pós-Graduação em Química Tecnológica e Ambiental-FURG, Rio Grande, RS, Brazil

    Marcos A. Gelesky

  4. Programa de Pós-Graduação em Aquacultura-FURG, Rio Grande, RS, Brazil

    Wilson Wasielesky & José Marìa Monserrat

  5. Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche, 60131, Ancona, Italy

    Daniele Fattorini & Francesco Regoli

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  1. Lucas Cordeiro
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Cordeiro, L., Müller, L., Gelesky, M.A. et al. Evaluation of coexposure to inorganic arsenic and titanium dioxide nanoparticles in the marine shrimp Litopenaeus vannamei . Environ Sci Pollut Res 23, 1214–1223 (2016). https://doi.org/10.1007/s11356-015-5200-5

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