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Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

Postal Subscription Code 80-973

2018 Impact Factor: 3.883

Front. Environ. Sci. Eng.    2015, Vol. 9 Issue (5) : 793-803    https://doi.org/10.1007/s11783-015-0775-0
RESEARCH ARTICLE
A multi-integrated approach on toxicity effects of engineered TiO2 nanoparticles
Ana PICADO1,*(),Susana M. PAIXÃO1,*(),Liliana MOITA1,Luis SILVA1,Mário S. DINIZ2,3,Joana LOURENÇO2,Isabel PERES3,Luisa CASTRO3,José Brito CORREIA1,Joana PEREIRA4,Isabel FERREIRA4,António Pedro Alves MATOS5,6,Pedro BARQUINHA4,Elsa MENDONCA1
1. LNEG-National Laboratory of Energy and Geology, I.P., Lisbon 1649-038, Portugal
2. REQUIMTE, Chemistry Department, Fine Chemistry and Biotechnology Center, Faculty of Sciences and Technology, New University of Lisbon, Caparica 2829-516, Portugal
3. IMAR-Ocean Institute, Department of Sciences and Environmental Engineering, Faculty of Sciences and Technology, New University of Lisbon, Caparica 2829-516, Portugal
4. CENIMAT/I3N and Department of Materials Science, Faculty of Sciences and Technology, New University of Lisbon, Caparica 2829-516, Portugal
5. Pathological Anatomy, Curry Cabral Hospital, Lisbon 1069-166, Portugal
6. CESAM, Faculty of Sciences, Lisbon University, Lisbon 1749-016, Portugal
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Abstract

The new properties of engineered nanoparticles drive the need for new knowledge on the safety, fate, behavior and biologic effects of these particles on organisms and ecosystems. Titanium dioxide nanoparticles have been used extensively for a wide range of applications, e.g, self-cleaning surface coatings, solar cells, water treatment agents, topical sunscreens. Within this scenario increased environmental exposure can be expected but data on the ecotoxicological evaluation of nanoparticles are still scarce. The main purpose of this work was the evaluation of effects of TiO2 nanoparticles in several organisms, covering different trophic levels, using a battery of aquatic assays. Using fish as a vertebrate model organism tissue histological and ultrastructural observations and the stress enzyme activity were also studied. TiO2 nanoparticles (Aeroxide® P25), two phase composition of anatase (65%) and rutile (35%) with an average particle size value of 27.6±11 nm were used. Results on the EC50 for the tested aquatic organisms showed toxicity for the bacteria, the algae and the crustacean, being the algae the most sensitive tested organism. The aquatic plant Lemna minor showed no effect on growth. The fish Carassius auratus showed no effect on a 21 day survival test, though at a biochemical level the cytosolic Glutathione-S-Transferase total activity, in intestines, showed a general significant decrease (p<0.05) after 14 days of exposure for all tested concentrations. The presence of TiO2 nanoparticles aggregates were observed in the intestine lumen but their internalization by intestine cells could not be confirmed.

Keywords ecotoxicity      enzymatic analysis      histology      transmission electron microscopy (TEM)      TiO2-nanoparticles     
Corresponding Author(s): Ana PICADO,Susana M. PAIXÃO   
Online First Date: 13 February 2015    Issue Date: 08 October 2015
 Cite this article:   
Ana PICADO,Susana M. PAIXÃO,Liliana MOITA, et al. A multi-integrated approach on toxicity effects of engineered TiO2 nanoparticles[J]. Front. Environ. Sci. Eng., 2015, 9(5): 793-803.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-015-0775-0
https://academic.hep.com.cn/fese/EN/Y2015/V9/I5/793
Fig.1  TiO2 nanoparticles as observed by TEM
Fig.2  Nanoparticle tracking analysis of TiO2 suspensions. (a) Stock suspension; (b) Daphnia test media; (c) Fish test media
test-exposure time EC10 (mean±s.d.) EC50 (mean±s.d.) NOEC
P. putida −16 h 1.2±0.53 9.9±1.2
V. fischeri −6 h 2.2±0.09 9.2±0.49 1
Microtox −15 min >81.9 >81.9 81.9
algae −72 h* 0.2±0.1 0.89±0.26
Daphnia −48 h 10.7±7.11 29.5±7.22 5.6
Lemna −7 d >90 >90 90
goldfish −21 d >100 >100 100
Tab.1  EC10-t (mg·L−1) and EC50-t (mg·L−1) values calculated for the different tested species exposed to TiO2-NP. Presented values as mean values±s.d. (n = 3)
Fig.3  Intestine of C. auratus. Control fish (a); accumulation of nanoparticles inside intestine lumen of fish exposed to different concentrations of TiO2 ((b) - 10 mg·L−1 for 14 d; (c) and (d) - 100 mg·L−1 for 21 d; (e) - 100 mg·L−1 for 14 d); (f) TEM image of intestine of fish exposed to 100 mg·L−1 (21 days). Legend: In (Intestine epithelium); NPs (nanoparticles aggregates); lu (intestine lumen); arrowheads (epithelium erosion); M (mucous layer)
Fig.4  SEM from nanoparticles aggregates inside intestine lumen and respective EDS spectrum revealing the presence of Ti (arrowhead) among other elements. Legend: In (intestine epithelium); lu (lumen)
Fig.5  GST total activity (mean±s.d.) in intestines of C. auratus exposed to different concentrations of TiO2. Significant differences if letters are different (p<0.05). Significant differences between exposure periods if *(p<0.05)
1 Schmid  G. Nanoparticles: From Theory to Application. Weinheim, Germany: Wiley-VCH, 2010
2 Kalantzi  O I, Biskos  G. Methods for assessing basic particle properties and cytotoxicity of engineered nanoparticles. Toxics, 2014, 2(1): 79–91
https://doi.org/10.3390/toxics2010079
3 Chen  X, Mao  S S. Titanium dioxide nanomaterials: synthesis, properties, modifications, and applications. Chemical Reviews, 2007, 107(7): 2891–2959
https://doi.org/10.1021/cr0500535 pmid: 17590053
4 Dalai  S, Pakrashi  S, Chandrasekaran  N, Mukherjee  A. Acute toxicity of TiO2 nanoparticles to Ceriodaphnia dubia under visible light and dark conditions in a freshwater system. PLoS ONE, 2013, 8(4): e62970
https://doi.org/10.1371/journal.pone.0062970 pmid: 23658658
5 Liu  X, Chen  G, Su  C. Effects of material properties on sedimentation and aggregation of titanium dioxide nanoparticles of anatase and rutile in the aqueous phase. Journal of Colloid and Interface Science, 2011, 363(1): 84–91
https://doi.org/10.1016/j.jcis.2011.06.085 pmid: 21803366
6 Moore  M N. Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environment International, 2006, 32(8): 967–976
https://doi.org/10.1016/j.envint.2006.06.014 pmid: 16859745
7 Kahru  A, Dubourguier  H C. From ecotoxicology to nanoecotoxicology. Toxicology, 2010, 269(2–3): 105–119
https://doi.org/10.1016/j.tox.2009.08.016 pmid: 19732804
8 Warheit  D B, Hoke  R A, Finlay  C, Donner  E M, Reed  K L, Sayes  C M. Development of a base set of toxicity tests using ultrafine TiO2 particles as a component of nanoparticle risk management. Toxicology Letters, 2007, 171(3): 99–110
https://doi.org/10.1016/j.toxlet.2007.04.008 pmid: 17566673
9 Wiench  K, Wohlleben  W, Hisgen  V, Radke  K, Salinas  E, Zok  S, Landsiedel  R. Acute and chronic effects of nano- and non-nano-scale TiO2 and ZnO particles on mobility and reproduction of the freshwater invertebrate Daphnia magna. Chemosphere, 2009, 76(10): 1356–1365
https://doi.org/10.1016/j.chemosphere.2009.06.025 pmid: 19580988
10 Zhu  X, Zhu  L, Chen  Y, Tian  S. Acute toxicities of six manufactured nanomaterial suspensions to Daphnia magna. Journal of Nanoparticle Research, 2009, 11(1): 67–75
https://doi.org/10.1007/s11051-008-9426-8
11 Zhu  X, Chang  Y, Chen  Y. Toxicity and bioaccumulation of TiO2 nanoparticle aggregates in Daphnia magna. Chemosphere, 2010, 78(3): 209–215
https://doi.org/10.1016/j.chemosphere.2009.11.013 pmid: 19963236
12 Heinlaan  M, Ivask  A, Blinova  I, Dubourguier  H C, Kahru  A. Toxicity of nanosized and bulk ZnO, CuO and TiO2 to bacteria Vibrio fischeri and crustaceans Daphnia magna and Thamnocephalus platyurus. Chemosphere, 2008, 71(7): 1308–1316
https://doi.org/10.1016/j.chemosphere.2007.11.047 pmid: 18194809
13 Blaise  C, Gagné  F, Férard  J F, Eullaffroy  P. Ecotoxicity of selected nano-materials to aquatic organisms. Environmental Toxicology, 2008, 23(5): 591–598
https://doi.org/10.1002/tox.20402 pmid: 18528913
14 Aruoja  V, Dubourguier  H C, Kasemets  K, Kahru  A. Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata. Science of the Total Environment, 2009, 407(4): 1461–1468
https://doi.org/10.1016/j.scitotenv.2008.10.053 pmid: 19038417
15 Hund-Rinke  K, Simon  M. Ecotoxic effect of photocatalytic active nanoparticles (TiO2) on algae and daphnids. Environmental Science and Pollution Research International, 2006, 13(4): 225–232
https://doi.org/10.1065/espr2006.06.311 pmid: 16910119
16 Hall  S, Bradley  T, Moore  J T, Kuykindall  T, Minella  L. Acute and chronic toxicity of nano-scale TiO2 particles to freshwater fish, cladocerans, and green algae, and effects of organic and inorganic substrate on TiO2 toxicity. Nanotoxicology, 2009, 3(2): 91–97
https://doi.org/10.1080/17435390902788078
17 Reeves  J F, Davies  S J, Dodd  N J F, Jha  A N. Hydroxyl radicals (﹒OH) are associated with titanium dioxide (TiO2) nanoparticle-induced cytotoxicity and oxidative DNA damage in fish cells. Mutation Research, 2008, 640(1–2): 113–122
https://doi.org/10.1016/j.mrfmmm.2007.12.010 pmid: 18258270
18 Dodd  N J F, Jha  A N. Titanium dioxide induced cell damage: a proposed role of the carboxyl radical. Mutation Research, 2009, 660(1–2): 79–82
https://doi.org/10.1016/j.mrfmmm.2008.10.007 pmid: 19013474
19 Lovern  S B, Klaper  R. Daphnia magna mortality when exposed to titanium dioxide and fullerene (C60) nanoparticles. Environmental Toxicology and Chemistry, 2006, 25(4): 1132–1137
https://doi.org/10.1897/05-278R.1 pmid: 16629153
20 Clemente  Z, Castro  V L, Jonsson  C M, Fraceto  L F. Ecotoxicology of nano-TiO2 —An evaluation of its toxicity to organisms of aquatic ecosystems. International Journal of Environmental of Research, 2012, 6(1): 33–50
21 Paixão  S M, Silva  L, Fernandes  A, O’Rourke  K, Mendonça  E, Picado  A. Performance of a miniaturized algal bioassay in phytotoxicity screening. Ecotoxicology, 2008, 17(3): 165–171
https://doi.org/10.1007/s10646-007-0179-4 pmid: 17978872
22 Martoja  R, Martoja-Pierson  M. Initiation aux techniques de l'histologie animale. R. Martoja et M. Martoja-Pierson, Masson, 1967, Paris
23 Habig  W H, Pabst  M J, Jakoby  W B. Glutathione S-Transferases. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 1974, 249(22): 7130–7139
pmid: 4436300
24 Banan Khojasteh  S M, Sheikhzadeh  F, Mohammadnejad  D, Azami  A. Histological, histochemical and ultrastructural study of the intestine of rainbow trout (Oncorhynchus mykiss). World Applied Sciences Journal, 2009, 6(11): 1525–1531
25 Delashoub  M, Pousty  I, Banan Khojasteh  S M. Histology of bighead carp (Hypophthalmichthys nobilis) intestine. Global Veterinaria, 2010, 5(6): 302–306
26 Clément  L, Hurel  C, Marmier  N. Toxicity of TiO2 nanoparticles to cladocerans, algae, rotifers and plants- effects of size and crystalline structure. Chemosphere, 2013, 90(3): 1083–1090
https://doi.org/10.1016/j.chemosphere.2012.09.013 pmid: 23062945
27 Sharma  V K. Aggregation and toxicity of titanium dioxide nanoparticles in aquatic environment — A review. Journal of Environmental Science and Health, Part A, 2009, 44(14): 1485–1495
28 Menard  A, Drobne  D, Jemec  A. Ecotoxicity of nanosized TiO2. Review of in vivo data. Environmental Pollution, 2011, 159(3): 677–684
https://doi.org/10.1016/j.envpol.2010.11.027 pmid: 21186069
29 Kim  E, Kim  S H, Kim  H C, Lee  S G, Lee  S J, Jeong  S W. Growth inhibition of aquatic plant caused by silver and titanium oxide nanoparticles. Toxicology and Environmental Health Science, 2011, 3(1): 1–6
https://doi.org/10.1007/s13530-011-0071-8
30 Slatinská  I, Smutná  M, Havelková  M, Svobodová  Z. Review article: biochemical markers of aquatic pollution in fish— Glutathione S-Transferase. Folia Veterinaria, 2008, 52(3–4): 129–134
31 Yi  X, Ding  H, Lu  Y, Liu  H, Zhang  M, Jiang  W. Effects of long-term alachlor exposure on hepatic antioxidant defense and detoxifying enzyme activities in crucian carp (Carassius auratus). Chemosphere, 2007, 68(8): 1576–1581
https://doi.org/10.1016/j.chemosphere.2007.02.035 pmid: 17433409
32 Xiong  D, Fang  T, Yu  L, Sima  X, Zhu  W. Effects of nano-scale TiO2, ZnO and their bulk counterparts on zebrafish: acute toxicity, oxidative stress and oxidative damage. Science of the Total Environment, 2011, 409(8): 1444–1452
https://doi.org/10.1016/j.scitotenv.2011.01.015 pmid: 21296382
33 Zhang  X, Sun  H, Zhang  Z, Niu  Q, Chen  Y, Crittenden  J C. Enhanced bioaccumulation of cadmium in carp in the presence of titanium dioxide nanoparticles. Chemosphere, 2007, 67(1): 160–166
https://doi.org/10.1016/j.chemosphere.2006.09.003 pmid: 17166554
34 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, 2007, 84(4): 415–430
https://doi.org/10.1016/j.aquatox.2007.07.009 pmid: 17727975
35 Handy  R D, Owen  R, Valsami-Jones  E. The ecotoxicology of nanoparticles and nanomaterials: current status, knowledge gaps, challenges, and future needs. Ecotoxicology, 2008, 17(5): 315–325
https://doi.org/10.1007/s10646-008-0206-0 pmid: 18408994
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