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A critical evaluation of the fish early-life stage toxicity test for engineered nanomaterials: experimental modifications and recommendations

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Abstract

There are concerns that regulatory toxicity tests are not fit for purpose for engineered nanomaterials (ENMs) or need modifications. The aim of the current study was to evaluate the OECD 210 fish, early-life stage toxicity test for use with TiO2 ENMs, Ag ENMs, and MWCNT. Both TiO2 ENMS (≤160 mg l−1) and MWCNT (≤10 mg l−1) showed limited acute toxicity, whilst Ag ENMs were acutely toxic to zebrafish, though less so than AgNO3 (6-day LC50 values of 58.6 and 5.0 µg l−1, respectively). Evidence of delayed hatching, decreased body length and increased muscle width in the tail was seen in fish exposed to Ag ENMs. Oedema (swollen yolk sacs) was also seen in fish from both Ag treatments with, for example, mean yolk sac volumes of 17, 35 and 39 µm3 for the control, 100 µg l−1 Ag ENMs and 5 µg l−1 AgNO3 treatments, respectively. Among the problems with the standard test guidelines was the inability to maintain the test solutions within ±20 % of nominal concentrations. Pronounced settling of the ENMs in some beakers also made it clear the fish were not being exposed to nominal concentrations. To overcome this, the exposure apparatus was modified with the addition of an exposure chamber that ensured mixing without damaging the delicate embryos/larvae. This allowed more homogeneous ENM exposures, signified by improved measured concentrations in the beakers (up to 85.7 and 88.1 % of the nominal concentrations from 10 mg l−1 TiO2 and 50 µg l−1 Ag ENM exposures, respectively) and reduced variance between measurements compared to the original method. The recommendations include: that the test is conducted using exposure chambers, the use of quantitative measurements for assessing hatching and morphometrics, and where there is increased sensitivity of larvae over embryos to conduct a shorter, larvae-only toxicity test with the ENMs.

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References

  • Al-Bairuty GA, Shaw BJ, Handy RD, Henry TB (2013) Histopathological effects of waterborne copper nanoparticles and copper sulphate on the organs of rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 126:104–115

    Article  CAS  Google Scholar 

  • Al-Jubory AR, Handy RD (2013) Uptake of titanium from TiO2 nanoparticle exposure in the isolated perfused intestine of rainbow trout: nystatin, vanadate and novel CO2-sensitive components. Nanotoxicology 7:1282–1301

    Article  CAS  Google Scholar 

  • Asharani PV, Wu YL, Gong Z, Valiyaveettil S (2008) Toxicity of silver nanoparticles in zebrafish models. Nanotechnology 19:255102

    Article  CAS  Google Scholar 

  • Bai W, Zhang Z, Tian W, He X, Ma Y, Zhao Y, Chai Z (2010) Toxicity of zinc oxide nanoparticles to zebrafish embryo: a physicochemical study of toxicity mechanism. J Nanopart Res 12:1645–1654  

    Article  CAS  Google Scholar 

  • Besinis A, De Peralta T, Handy RD (2014) The antibacterial effects of silver, titanium dioxide and silica dioxide nanoparticles compared to the dental disinfectant chlorhexidine on Streptococcus mutans using a suite of bioassays. Nanotoxicology 8:1–16

    Article  CAS  Google Scholar 

  • Bilberg K, Malte H, Wang T, Baatrup E (2010) Silver nanoparticles and silver nitrate cause respiratory stress in Eurasian perch (Perca fluviatilis). Aquat Toxicol 96:159–165

    Article  CAS  Google Scholar 

  • Bilberg K, Hovgaard MB, Besenbacher F, Baatrup E (2012) In vivo toxicity of silver nanoparticles and silver ions in Zebrafish (Danio rerio). J Toxicol Article ID 293784

  • Bird NC, Mabee PM (2003) Developmental morphology of the axial skeleton of the zebrafish, Danio rerio (Ostariophysi: Cyprinidae). Dev Dyn 228:337–357

    Article  Google Scholar 

  • Boyle D, Boran H, Atfield AJ, Henry TB (2015) Use of an exposure chamber to maintain aqueous phase nanoparticle dispersions for improved toxicity testing in fish. Environ Toxicol Chem 34:583–588

    Article  CAS  Google Scholar 

  • Brinkman SF, Hansen DL (2007) Toxicity of cadmium to early life stages of brown trout (Salmo trutta) at multiple water hardnesses. Environ Toxicol Chem 26:1666–1671

    Article  CAS  Google Scholar 

  • Bryson-Richardson R, Berger S, Currie P (2012) Atlas of zebrafish development. Elsevier, London 232

    Google Scholar 

  • Celá P, Veselá B, Matalová E, Večeřa Z, Buchtová M (2014) Embryonic toxicity of nanoparticles. Cells Tissues Organs 199:1–23

    Article  Google Scholar 

  • Chae YJ, Pham CH, Lee J, Bae E, Yi J, Gu MB (2009) Evaluation of the toxic impact of silver nanoparticles on Japanese medaka (Oryzias latipes). Aquat Toxicol 94:320–327

    Article  CAS  Google Scholar 

  • Chapman PM, Caldwell, RS, Chapman PF (1996) A warning: NOECs are inappropriate for regulatory use. Environ Toxicol Chem 5: 77–79

    Article  CAS  Google Scholar 

  • Cheng J, Cheng SH (2012) Influence of carbon nanotube length on toxicity to zebrafish embryos. Int J Nanomed 7:3731–3739

    Article  Google Scholar 

  • Cheng J, Flahaut E, Cheng SH (2007) Effect of carbon nanotubes on develo** zebrafish (Danio rerio) embryos. Environ Toxicol Chem 26:708–716

    Article  CAS  Google Scholar 

  • Christen V, Capelle M, Fent K (2013) Silver nanoparticles induce endoplasmatic reticulum stress response in zebrafish. Toxicol Appl Pharm 272:519–528

    Article  CAS  Google Scholar 

  • Clemente Z, Castro VL, Feitosa LO, Lima R, Jonsson CM, Maia AH, Fraceto LF (2013) Fish exposure to nano-TiO2 under different experimental conditions: methodological aspects for nanoecotoxicology investigations. Sci Total Environ 463–464:647–656

    Article  Google Scholar 

  • Clemente Z, Castro VLSS, Moura MAM, Jonsson CM, Fraceto LF (2014) Toxicity assessment of TiO2 nanoparticles in zebrafish embryos under different exposure conditions. Aquat Toxicol 147:129–139

    Article  CAS  Google Scholar 

  • Crane M, Newman MC (2000) What level of effect is a no observed effect? Environ Toxicol Chem 19:516–519

    Article  CAS  Google Scholar 

  • Crane M, Handy RD, Garrod J, Owen R (2008) Ecotoxicity test methods and environmental hazard assessment for engineered nanoparticles. Ecotoxicology 17:421–437

    Article  CAS  Google Scholar 

  • Delay M, Dolt T, Woellhaf A, Sembritzki R, Frimmel FH (2011) Interactions and stability of silver nanoparticles in the aqueous phase: influence of natural organic matter (NOM) and ionic strength. J Chromatogr A 1218:4206–4212

    Article  CAS  Google Scholar 

  • Duan J, Yu Y, Shi H, Tian L, Guo C, Huang P, Zhou X, Peng S, Sun Z (2013) Toxic effects of silica nanoparticles on zebrafish embryos and larvae. PLoS ONE 8(9):e74606. doi:10.1371/journal.pone.0074606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eaton JG, McKim JM, Holcombe GW (1978) Metal toxicity to embryos and larvae of seven freshwater fish species. I. Cadmium. Bull Environ Contam Toxicol 19:95–103

    Article  CAS  Google Scholar 

  • Embry MR, Belanger SE, Braunbeck TA, Galay-Burgos M, Halder M, Hinton DE, Léonard MA, Lillicrap A, Norberg-King T, Whale G (2010) The fish embryo toxicity test as an animal alternative method in hazard and risk assessment and scientific research. Aquat Toxicol 97:79–87

    Article  CAS  Google Scholar 

  • European Commission (2011) Commission recommendation of 18 October 2011 on the definition of nanomaterial. Official Journal of the European Union, (2011/696/EU)

  • Federici G, Shaw BJ, Handy RD (2007) Toxicity of titanium dioxide nanoparticles to rainbow trout, (Oncorhynchus mykiss): gill injury, oxidative stress, and other physiological effects. Aquat Toxicol 84:415–430

    Article  CAS  Google Scholar 

  • Fraser TWK, Reinardy HC, Shaw BJ, Henry TB, Handy RD (2011) Dietary toxicity of single-walled carbon nanotubes and fullerenes (C60) in rainbow trout (Oncorhynchus mykiss). Nanotoxicology 5:98–108

    Article  CAS  Google Scholar 

  • Gellert G, Heinrichsdorff J (2001) Effect of age on the susceptibility of zebrafish eggs to industrial wastewater. Water Res 35:3754–3757

    Article  CAS  Google Scholar 

  • Griffitt RJ, Weil R, Hyndman KA, Denslow ND, Powers K, Taylor D, Barber DS (2007) Exposure to copper nanoparticles causes gill injury and acute lethality in zebrafish (Danio rerio). Environ Sci Technol 41:8178–8186

    Article  CAS  Google Scholar 

  • Griffitt RJ, Luo J, Gao J, Bonzongo JC, Barber DS (2008) Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Toxicol Chem 27:1972–1978

    Article  CAS  Google Scholar 

  • Groh KJ, Carvalho RN, Chipman JK, Denslow ND, Halder M, Murphy CA, Roelofs D, Rolaki A, Schirmer K, Watanabe KH (2015) Development and application of the adverse outcome pathway framework for understanding and predicting chronic toxicity: II. A focus on growth impairment in fish. Chemosphere 120:778–792

    Article  CAS  Google Scholar 

  • Guadagnolo CM, Brauner CJ, Wood CM (2001) Chronic effects of silver exposure on ion levels, survival, and silver distribution within develo** rainbow trout (Oncorhynchus mykiss) embryos. Environ Toxicol Chem 20:553–560

    Article  CAS  Google Scholar 

  • Halder M, Léonard M, Iguchi T, Oris JT, Ryder K, Belanger SE, Braunbeck TA, Embry MR, Whale G, Norberg-King T, Lillicrap A (2010) Regulatory aspects on the use of fish embryos in environmental toxicology. Integr Environ Assess Manag 6:484–491

    Article  CAS  Google Scholar 

  • Handy RD, Shaw BJ (2007) Ecotoxicity of nanomaterials to fish: challenges for ecotoxicity testing. Integr Environ Assess Manag 3:458–460

    Article  CAS  Google Scholar 

  • Handy RD, Sims DW, Giles A, Campbell HA, Musonda MM (1999) Metabolic trade-off between locomotion and detoxification for maintenance of blood chemistry and growth parameters by rainbow trout (Oncorhynchus mykiss) during chronic dietary exposure to copper. Aquat Toxicol 47:23–41

    Article  CAS  Google Scholar 

  • Handy RD, von der Kammer F, Lead JR, Hassellöv M, Owen R, Crane M (2008) The ecotoxicology and chemistry of manufactured nanoparticles. Ecotoxicology 17:287–314

    Article  CAS  Google Scholar 

  • Handy RD, Al-Bairuty G, Al-Jubory A, Ramsden CS, Boyle D, Shaw BJ, Henry TB (2011) Effects of manufactured nanomaterials on fishes: a target organ and body systems physiology approach. J Fish Biol 79:821–853

    Article  CAS  Google Scholar 

  • Handy RD, van den Brink N, Chappell M, Mühling M, Behra R, Dušinská M, Simpson P, Ahtiainen J, Jha AN, Seiter J, Bednar A, Kennedy A, Fernandes TF, Riediker M (2012a) Practical considerations for conducting ecotoxicity test methods with manufactured nanomaterials: what have we learnt so far? Ecotoxicology 21:933–972

    Article  CAS  Google Scholar 

  • Handy RD, Cornelis G, Fernandes T, Tsyusko O, Decho A, Sabo-Attwood T, Metcalfe C, Steevens JA, Klaine SJ, Koelmans AA, Horne N (2012b) Ecotoxicity test methods for engineered nanomaterials: practical experiences and recommendations from the bench. Environ Toxicol Chem 31:15–31

    Article  CAS  Google Scholar 

  • Henn K, Braunbeck T (2011) Dechorionation as a tool to improve the fish embryo toxicity test (FET) with the zebrafish (Danio rerio). Comp Biochem Physiol C 153:91–98

    Google Scholar 

  • Holeton GF, Randall DJ (1967) The effect of hypoxia upon the partial pressure of gases in the blood and water afferent and efferent to the gills of rainbow trout. J Exp Biol 46:317–327

    CAS  PubMed  Google Scholar 

  • Jager T (2012) Bad habits die hard: the NOEC’s persistence reflects poorly on ecotoxicology. Environ Toxicol Chem 31:228–229

    Article  CAS  Google Scholar 

  • Johnson A, Carew E, Sloman KA (2007) The effects of copper on the morphological and functional development of zebrafish embryos. Aquat Toxicol 84:431–438

    Article  CAS  Google Scholar 

  • Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:25–310

    Article  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 

  • Klaine SJ, Koelmans AA, Horne N, Carley S, Handy RD, Kapustka L, Nowack B, von der Kammer F (2012) Paradigms to assess the environmental impact of manufactured nanomaterials. Environ Toxicol Chem 31:3–14

    Article  CAS  Google Scholar 

  • Klein CL, Comero S, Stahlmecke B, Romazanov J, Kuhlbusch TAJ, Van Doren E, De Temmerman P-J, Mast J, Wick P, Krug H, Locoro G, Hund-Rinke K, Kördel W, Friedrichs S, Maier G, Werner J, Lingsinger Th, Gawlik BM (2011) NM-series of representative manufactured nanomaterials NM-300 silver characterisation, stability, homogeneity. JRC Scientific and Technical Reports

  • Knöbel M, Busser FJM, Rico-Rico A, Kramer NI, Hermens JLM, Hafner C, Tanneberger K, Schirmer K, Scholz S (2012) Predicting adult fish acute lethality with the zebrafish embryo: Relevance of test duration, endpoints, compound properties, and exposure concentration analysis. Environ Sci Technol 46: 9690–9700

    Article  Google Scholar 

  • Kwok KWH, Auffan M, Badireddy AR, Nelson CM, Wiesner MR, Chilkoti A, Liu J, Marinakos SM, Hinton DE (2012) Uptake of silver nanoparticles and toxicity to early life stages of Japanese medaka (Oryzias latipes): effect of coating materials. Aquat Toxicol 120–121:59–66

    Article  Google Scholar 

  • Laale HW (1977) The biology and use of zebrafish, Brachydanio rerio in fisheries research. A literature review. J Fish Biol 10:121–173

    Article  Google Scholar 

  • Landis WG, Chapman PM (2011) Well past time to stop using NOELs and LOELs. Integr Environ Assess Manag 7:vi–viii

    Article  Google Scholar 

  • Laskowski R (1995) Some good reasons to ban the use of NOEC, LOEC and related concepts in ecotoxicology. Oikos 73:140–144

    Article  Google Scholar 

  • Lee KJ, Nallathamby PD, Browning LM, Osgood CJ, Xu X-HN (2007) In vivo imaging of transport and biocompatibility of single silver nanoparticles in early development of zebrafish embryos. ACS Nano 1:133–143

    Article  CAS  Google Scholar 

  • Lee B, Duong CN, Cho J, Lee J, Kim K, Seo Y, Kim P, Choi K, Yoon J (2012) Toxicity of citrate-capped silver nanoparticles in common carp (Cyprinus carpio). J Biomed Biotechnol vol 2012, Article ID 262670

  • Liu XT, Mu XY, Wu XL, Meng LX, Guan WB, Ma YQ, Sun H, Wang CJ, Li XF (2014) Toxicity of multi-walled carbon nanotubes, graphene oxide, and reduced graphene oxide to zebrafish embryos. Biomed Environ Sci 27:676–683

    PubMed  Google Scholar 

  • Ma H, Diamond SA (2013) Phototoxicity of TiO2 nanoparticles to zebrafish (Danio rerio) is dependent on life stage. Environ Toxicol Chem 2:2139–2143

    Article  Google Scholar 

  • MacCormack TJ, Goss GG, Handy RD (2014) Emerging threats to fishes: Engineered organic nanomaterials. In: Tierney KB, Farrell AP, Brauner CJ (eds) Organic chemical toxicology of fishes. Fish physiology, vol 33. Academic Press, San Diego, pp 439–479

    Chapter  Google Scholar 

  • McKim JM, Eaton JG, Holcombe GW (1978) Metal toxicity to embryos and larvae of eight species of freshwater fish—II: copper. Bull Environ Contam Toxicol 19:608–616

    Article  CAS  Google Scholar 

  • Menke AL, Spitsbergen JM, Wolterbeek APM, Woutersen RA (2011) Normal anatomy and histology of the adult zebrafish. Toxicol Pathol 39:759–775

    Article  Google Scholar 

  • Mitrano DM, Ranville JF, Bednar A, Kazor K, Hering AS, Higgins CP (2014) Tracking dissolution of silver nanoparticles at environmentally relevant concentrations in laboratory, natural, and processed waters using single particle ICP-MS (spICP-MS). Environ Sci Nano 1:248–259

    Article  CAS  Google Scholar 

  • Mizell M, Romig ES (1997) The aquatic vertebrate embryo as a sentinel for toxins: zebrafish embryo dechorionation and perivitelline space microinjection. Int J Dev Biol 41:411–423

    CAS  PubMed  Google Scholar 

  • Müller UK (2008) Swimming and muscle. In: Finn RN, Kapoor BG (eds) Fish larval physiology. Science Publishers, Enfield, pp 523–549

    Google Scholar 

  • OECD (1992a) Test no. 210: test no. 210. OECD guidelines for testing of chemicals. fish, early-life stage test. The Organisation for Economic Co-operation and Development

  • OECD (1992b) Test no. 203. Fish, acute toxicity test. OECD guidelines for the testing of chemicals. http://www.keepeek.com/Digital-Asset-Management/oecd/environment/test-no-203-fish-acute-toxicity-test_9789264069961-en#page6

  • OECD (1998) Test no. 203. Fish, short-term toxicity test on embryo and sac-fry stages. OECD guidelines for the testing of chemicals. http://www.oecd-ilibrary.org/docserver/download/9721201e.pdf?expires=1445776299&id=id&accname=guest&checksum=1DEEEB7D378004012F09C90D548E726D

  • OECD (2000) Guidance document on aquatic toxicity testing of difficult substances and mixtures. OECD series on testing and assessment number 23. http://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono(2000)6&doclanguage=en

  • OECD (2012) Guidance on sample preparation and dosimetry for the safety testing of manufactured nanomaterials. Series on the safety of manufactured nanomaterials no. 36. http://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono(2012)40&doclanguage=en

  • OECD (2013) Test no. 210: fish, early-life stage toxicity test. OECD guidelines for the testing of chemicals, Section 2. http://www.oecd-ilibrary.org/environment/test-no-210-fish-early-life stage-toxicity-test_9789264203785-en. OECD Publishing

  • Oris JT, Belanger SE, Bailer AJ (2012) Baseline characteristics and statistical implications for the OECD 210 fish early-life stage chronic toxicity test. Environ Toxicol Chem 31:370–376

    Article  CAS  Google Scholar 

  • Parichy DM, Elizondo MR, Mills MG, Gordon TN, Engeszer RE (2009) Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish. Dev Dyn 238:2975–3015

    Article  Google Scholar 

  • Petersen EJ, Henry TB, Zhao J, MacCuspie RI, Kirschling TL, Dobrovolskaia MA, Hackley V, **ng B, White JC (2014) Identification and avoidance of potential artifacts and misinterpretations in nanomaterial ecotoxicity measurements. Environ Sci Technol 48:4226–4246

    Article  CAS  Google Scholar 

  • Petersen EJ, Diamond SA, Kennedy AJ, Goss GG, Ho K, Lead J, Hanna SK, Hartmann NB, Hund-Rinke K, Mader B, Manier N, Pandard P, Salinas ER, Sayre P (2015) Adapting OECD aquatic toxicity tests for use with manufactured nanomaterials: key issues and consensus recommendations. Environ Sci Technol 49:9532–9547

    Article  CAS  Google Scholar 

  • Ramsden CS, Smith TJ, Shaw BJ, Handy RD (2009) Dietary exposure to titanium dioxide nanoparticles in rainbow trout, (Oncorhynchus mykiss): no effect on growth, but subtle biochemical disturbances in the brain. Ecotoxicology 18:939–951

    Article  CAS  Google Scholar 

  • Ramsden CS, Henry TB, Handy RD (2013) Sub-lethal effects of titanium dioxide nanoparticles on the physiology and reproduction of zebrafish. Aquat Toxicol 126:404–413

    Article  CAS  Google Scholar 

  • Rand GM, Wells PG, McCarty LS (1995) Introduction to aquatic toxicology. In: Rand GH (ed) Fundamentals of aquatic toxicology, 2nd edn. CRC Press, Boca Raton, pp 3–67

    Google Scholar 

  • Ranville J, Montano M (2015) Physicochemical characterization—size distributions. In: Baalousha M, Lead JR (eds) Characterization of nanomaterials in complex environmental and biological media. Frontiers of nanoscience, vol 8. Elsevier, Amsterdam, p 320

    Google Scholar 

  • Rasmussen K, Mast J, De Temmerman P-J, Verleysen E, Waegeneers N, Van Steen F, Pizzolon JC, De Temmerman L, Van Doren E, Jensen KA, Birkedal R, Levin M, Nielsen SH, Koponen IK, Clausen PA, Kofoed-Sørensen V, Kembouche Y, Thieriet N, Spalla O, Guiot C, Rousset D, Witschger O, Bau S, Bianchi B, Motzkus C, Shivachev B, Dimowa L, Nikolova R, Nihtianova D, Tarassov M, Petrov O, Bakardjieva S, Gilliland D, Pianella F, Ceccone G, Spampinato V, Cotogno G, Gibson N, Gaillard C, Mech A (2014a) Titanium dioxide, NM-100, NM-101, NM-102, NM-103, NM-104, NM-105: characterisation and physico-chemical properties, JRC repository: NM-series of representative manufactured nanomaterials. JRC Science and Policy Reports

  • Rasmussen K, Mast J, De Temmerman P-J, Verleysen E, Waegeneers N, Van Steen F, Pizzolon JC, De Temmerman L, Van Doren E, Jensen KA, Birkedal R, Clausen PA, Kembouche Y, Thieriet N, Spalla O, Guiot C, Rousset D, Witschger O, Bau S, Bianchi B, Shivachev B, Dimowa L, Nikolova R, Nihtianova D, Tarassov M, Petrov O, Bakardjieva S, Motzkus C, Labarraque G, Oster C, Cotogno G, Gailliard C (2014b) Multi-walled carbon nanotubes, NM-400, NM-401, NM-402, NM-403: characterisation and physico-chemical properties. JRC repository: NM-series of representative manufactured nanomaterials. JRC Science and Policy Reports

  • Rawson DM, Zhang T, Kalicharan D, Jongebloed WL (2000) Field emission scanning electron microscopy and transmission electron microscopy studies of the chorion, plasma membrane and syncytial layers of the gastrula-stage embryo of the zebrafish Brachydanio rerio: a consideration of the structural and functional relationships with respect to cryoprotectant penetration. Aquac Res 3:325–336

    Article  Google Scholar 

  • Ribeiro F, Gallego-Urrea JA, Jurkschat K, Crossley A, Hassellöv M, Taylor C, Soares AMVM, Loureiro S (2014) Silver nanoparticles and silver nitrate induce high toxicity to Pseudokirchneriella subcapitata, Daphnia magna and Danio rerio. Sci Total Environ 466–467:232–241

    Article  Google Scholar 

  • Rojo I, Uriate M, Obieta I, Bustero I, Egizabal A, Pardo MA, de Ilárduya M (2007) Toxicogenomics study of nanomaterials on the model organism zebrafish. In: Technical proceedings of the 2007 NSTI nanotechnology conference and trade show, vol 2, pp 655–658

  • Rombough PJ (1985) The influence of the zona radiata on the toxicities of zinc, lead, mercury, copper, and silver ions to embryos of steelhead trout Salmo gairdneri. Comp Biochem Physiol C 82:115–117

    Article  CAS  Google Scholar 

  • Sánchez-Bayo F (2012) Should we forget NOECs? Integr Environ Assess Manag 8:564–565

    Article  Google Scholar 

  • Schilling TF (2002) The morphology of larval and adult zebrafish. In: Nusslein-Volhard C, Ralf-Dahm R (eds) Zebrafish (practical approach series). Oxford University Press, Oxford, pp 59–94

    Google Scholar 

  • Schlenk D, Handy R, Steinert S, Depledge MH, Benson W (2008) Biomarkers. In: Di Giulio RT, Hinton DE (eds) The toxicology of fishes. CRC Press, Boca Raton, p 1071

    Google Scholar 

  • Schwab F, Bucheli TD, Lukhele LP, Magrez A, Nowack B, Sigg L, Knauer K (2011) Are carbon nanotube effects on green algae caused by shading and agglomeration? Environ Sci Technol 45:6136–6144

    Article  CAS  Google Scholar 

  • Shaw BJ, Al-Bairuty G, Handy RD (2012) Effects of waterborne copper nanoparticles and copper sulphate on rainbow trout, (Oncorhynchus mykiss): physiology and accumulation. Aquat Toxicol 116–117:90–101

    Article  Google Scholar 

  • Shaw BJ, Ramsden CS, Turner A, Handy RD (2013) A simplified method for determining titanium from TiO2 nanoparticles in fish tissue with a concomitant multi-element analysis. Chemosphere 92:1136–1144

    Article  CAS  Google Scholar 

  • Simonet BM, Valcárcel M (2009) Monitoring nanoparticles in the environment. Anal Bioanal Chem 393:17–21

    Article  CAS  Google Scholar 

  • Skalski JR (1981) Statistical inconsistencies in the use of no-observed-effect-levels in toxicity testing. In: Branson DR, Dickson KL (eds) Aquatic toxicology and hazard evaluation. American Society for Testing and Materials, Philadelphia, pp 337–387

    Google Scholar 

  • Tiede K, Boxall ABA, Tear SP, Lewis J, David H, Hassellöv M (2008) Detection and characterization of engineered nanoparticles in food and the environment. Food Addit Contam 25:795–821

    Article  CAS  Google Scholar 

  • Truong L, Saili KS, Miller JM, Hutchinson JE, Tanguay RL (2012) Persistent adult zebrafish behavioral deficits results from acute embryonic exposure to gold nanoparticles. Comp Biochem Physiol C 155:269–274

    CAS  Google Scholar 

  • Velasco-Santamaría YM, Handy RD, Sloman KA (2011) Endosulfan affects health variables in adult zebrafish (Danio rerio) and induces alterations in larvae development. Comp Biochem Physiol C Toxicol Pharmacol 153:372–380

    Article  Google Scholar 

  • von der Kammer F, Ferguson PL, Holden PA, Masion A, Rogers KR, Klaine SJ, Koelmans AA, Horne N, Unrine JM (2012) Analysis of engineered nanomaterials in complex matrices (environment and biota): general considerations and conceptual case studies. Environ Toxicol Chem 31:32–49

    Article  Google Scholar 

  • Warne MSJ, van Dam R (2008) NOEC and LOEC data should no longer be generated or used. Australas J Ecotoxicol 14:1–5

    Google Scholar 

  • Welsh PG, Lipton J, Mebane CA, Marr JCA (2008) Influence of flow-through and renewal exposures on the toxicity of copper to rainbow trout. Ecotoxicol Environ Saf 69:199–208

    Article  CAS  Google Scholar 

  • Witeska M, Sarnowski P, Ługowska K, Kowal E (2014) The effects of cadmium and copper on embryonic and larval development of ide Leuciscus idus L. Fish Physiol Biochem 40:151–163

    Article  CAS  Google Scholar 

  • Zhang Y, Chen Y, Paul Westerhoff P, Crittenden J (2009) Impact of natural organic matter and divalent cations on the stability of aqueous nanoparticles. Water Res 43:4249–4257

    Article  CAS  Google Scholar 

  • Zhu X, Zhu L, Duan Z, Qi R, Li Y, Lang Y (2008) Comparative toxicity of several metal oxide nanoparticle aqueous suspensions to Zebrafish (Danio rerio) early developmental stage. J Environ Sci Health A 43:278–284

    Article  CAS  Google Scholar 

  • Zhu B, Liu G-L, Ling F, Song L-S, Wang G-X (2015) Development toxicity of functionalized single-walled carbon nanotubes on rare minnow embryos and larvae. Nanotoxicology 9:579–590

    Article  CAS  Google Scholar 

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Acknowledgments

This work was carried out as part of the E.C. MARINA Project, Call identifier: FP7-NMP-2010-LARGE-4, Grant Agreement No: NMP4-LA-2011-263215 (MARINA). The PI at Plymouth was Professor R. D. Handy. Dr Shaw organised and conducted the experiments at the bench, with assistance at specific times from temporary RAs at the bench, C.C. Liddle and K.M. Windeatt, who contributed equally. Shaw and Handy prepared this critical review and take responsibility for the scientific opinions herein. Thanks go to Dr. Andrew Fisher for help with ICP-OES and ICP-MS.

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  1. Ecotoxicology Research and Innovation Centre, School of Biological Sciences, Plymouth University, Drake Circus, Plymouth, PL4 8AA, UK

    Benjamin J. Shaw, Corin C. Liddle, Kirsten M. Windeatt & Richard D. Handy

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  2. Corin C. Liddle
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  3. Kirsten M. Windeatt
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  4. Richard D. Handy
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Correspondence to Richard D. Handy.

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Shaw, B.J., Liddle, C.C., Windeatt, K.M. et al. A critical evaluation of the fish early-life stage toxicity test for engineered nanomaterials: experimental modifications and recommendations. Arch Toxicol 90, 2077–2107 (2016). https://doi.org/10.1007/s00204-016-1734-7

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  • DOI: https://doi.org/10.1007/s00204-016-1734-7

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