Abstract
We assessed the acute toxicity effects (96 h) of silver nanoparticles (Ag NPs) and zinc oxide nanoparticles (ZnO NPs) and chronic (28 d) exposure to Ag NPs, including in combination with ZnO NPs. In the chronic studies, we further assessed the toxicokinetics and bioaccumulation of Ag and the resulting histopathological effects in the gill, intestine, and liver of zebrafish. Co-exposures with ZnO NPs reduced the toxicity of Ag NPs for acute (lethality) but enhanced the toxicity effects (tissue histopathology) for chronic exposures. The histological lesions for both NPs exposures in the gill included necrosis and fusion of lamellae, for the intestine necrosis and degeneration, and in the liver, mainly necrosis. The severity of the histological lesions induced by the Ag NPs was related to the amount of accumulated Ag in the zebrafish organs. The Ag accumulation in different organs was higher in the presence of ZnO NPs in the order of the gill > intestine > liver. Depuration kinetics illustrated the lowest half-life for Ag occurred in the gill and for the combined exposure of Ag with ZnO NPs. Our findings illustrate that in addition to tissue, time, and exposure concentration dependencies, the Ag NPs toxicity can also be influenced by the co-exposure to other NPs (here ZnO NPs), emphasizing the need for more combination exposure effects studies for NPs to more fully understand their potential environmental health risks.
Graphical Abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The datasets generated during the current study are available from the corresponding author on reasonable request.
Code Availability
Not applicable.
References
Abdel-Khalek AA (2015) Risk assessment, bioaccumulation of metals and histopathological alterations in Nile tilapia (Oreochromis niloticus) facing degraded aquatic conditions. Bull Environ Contam Toxicol 94:77–83. https://doi.org/10.1007/s00128-014-1400-9
Ale A, Bacchetta C, Rossi AS, Galdopórpora J, Desimone MF, Fernando RD, Gervasio S, Cazenave J (2018) Nanosilver toxicity in gills of a neotropical fish: metal accumulation, oxidative stress, histopathology and other physiological effects. Ecotoxicol Environ Saf 1:976–984. https://doi.org/10.1016/j.ecoenv.2017.11.072
Afifi M, Abdelazim AM (2015) Ameliorative effect of zinc oxide and silver nanoparticles on antioxidant system in the brain of diabetic rats. Asian Pac J Trop Biomed 5:874–877. https://doi.org/10.1016/j.apjtb.2015.06.010
Baek MJ, Son J, Park J, Seol Y, Sung B, Kim YJ (2020) Quantitative prediction of mixture toxicity of AgNO3 and ZnO nanoparticles on Daphnia magna. Sci Technol Adv Mat 21:333–345. https://doi.org/10.3390/nano11010124
Baramaki R, Ebrahimpour M, Mansouri B, Rezaei MR, Babaei H (2012) Contamination of metals in tissues of Ctenopharyngodon idella and Perca fluviatilis, from Anzali Wetland. Iran Bull Environ Contam Toxicol 89:831–835. https://doi.org/10.1007/s00128-012-0795-4
Benavides M, Fernández-Lodeiro J, Coelho P, Lodeiro C, Diniz MS (2016) Single and combined effects of aluminum (Al2O3) and zinc (ZnO) oxide nanoparticles in a freshwater fish, Carassius auratus. Environ Sci Pollut Res 23:24578–24591. https://doi.org/10.1007/s11356-016-7915-3
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. https://doi.org/10.1016/j.aquatox.2009.10.019
Bondarenko O, Juganson K, Ivask A, Kasemets K, Mortimer M, Kahru A (2013) Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: a critical review. Arch Toxicol 87:1181–1200. https://doi.org/10.1007/s00204-013-1079-4
Boran H, Şaffak S (2018) Comparison of dissolved nickel and nickel nanoparticles toxicity in larval zebrafish in terms of gene expression and DNA damage. Arch Environ Contam Toxicol 74:193–202. https://doi.org/10.1007/s00244-017-0468-8
Boxall A, Tiede K, Chaudhry Q, Aitken R, Jones A, Jefferson B, Lewis J (2007) Current and future predicted exposure to engineered nanoparticles. Safety of Nanomaterials Interdisciplinary Research Centre Report, pp 1–3
Beer C, Foldbjerg R, Hayashi Y, Sutherland DS, Autrup H (2012) Toxicity of silver nanoparticles—nanoparticle or silver ion? Toxicol Lett 208:286–292. https://doi.org/10.1016/j.toxlet.2011.11.002
Carvalho JC, Keita H, Santana GR, de Souza GC, Dos Santos IV, Amado JR, Kourouma A, Prada AL, de Oliveira CH, Silva ML (2018) Effects of Bothrops alternatus venom in zebrafish: a histopathological study. Inflammopharmacology 26:273–284. https://doi.org/10.1007/s10787-017-0362-z
Clogston JD, Patri AK (2011) Zeta potential measurement. Characterization of nanoparticles intended for drug delivery. Humana Press, pp 63–70
Das P, Xenopoulos MA, Williams CJ, Hoque ME, Metcalfe CD (2012) Effects of silver nanoparticles on bacterial activity in natural waters. Environ Toxicol Chem 31:122–130. https://doi.org/10.1002/etc.716
Farkas J, Christian P, Gallego-Urrea JA, Roos N, Hassellöv M, Tollefsen KE, Thomas KV (2011) Uptake and effects of manufactured silver nanoparticles in rainbow trout (Oncorhynchus mykiss) gill cells. Aquat Toxicol 101:117–125. https://doi.org/10.1016/j.aquatox.2010.09.010
Forouhar Vajargah M, Mohamadi Yalsuyi A, Hedayati A, Faggio C (2018) Histopathological lesions and toxicity in common carp (Cyprinus carpio L. 1758) induced by copper nanoparticles. Microsc Res Tech 81:724–729. https://doi.org/10.1002/jemt.23028
Forouhar Vajargah M, Mohamadi Yalsuyi A, Sattari M, Prokić MD, Faggio C (2020) Effects of copper oxide nanoparticles (CuO-NPs) on parturition time, survival rate and reproductive success of guppy fish, Poecilia reticulata. J Clust Sci 31:499–506. https://doi.org/10.1007/s10876-019-01664-y
Forouhar Vajargah M, Imanpoor MR, Shabani A, Hedayati A, Faggio C (2019) Effect of long-term exposure of silver nanoparticles on growth indices, hematological and biochemical parameters and gonad histology of male goldfish (Carassius auratus gibelio). Microsc Res Tech 82:1224–1230. https://doi.org/10.1002/jemt.23271
George S, Lin S, Ji Z, Thomas CR, Li L, Mecklenburg M, Meng H, Wang X, Zhang H, XiaT HJN (2012) Surface defects on plate-shaped silver nanoparticles contribute to its hazard potential in a fish gill cell line and zebrafish embryos. ACS Nano 6:3745–3759. https://doi.org/10.1021/nn204671v
Ghosh M, Sinha S, Jothiramajayam M, Jana A, Nag A, Mukherjee A (2016) Cytogenotoxicity and oxidative stress induced by zinc oxide nanoparticle in human lymphocyte cells in-vitro and Swiss albino male mice in-vivo. Food Chem Toxicol 97:286–296. https://doi.org/10.1016/j.fct.2016.09.025
Hadi AA, Alwan SF (2012) Histopathological changes in gills, liver and kidney of fresh water fish, Tilapia zillii, exposed to aluminum. Int J Pharm Res Allied Sci 3:2071–2081. https://doi.org/10.1590/S0100-736X2007000300004
Haghighat F, Kim Y, Sourinejad I, Yu IJ, Johari SA (2021) Titanium dioxide nanoparticles affect the toxicity of silver nanoparticles in common carp (Cyprinus carpio). Chemosphere 262:127805. https://doi.org/10.1016/j.chemosphere.2020.127805
Handy RD, Maunder RJ (2009) The biological roles of mucus: importance for osmoregulation and osmoregulatory disorders of fish health. Osmoregulation and ion transport: integrating physiological, molecular and environmental aspects. Ess Rev J Exp Biol 1:1203–1235. https://doi.org/10.3390/fishes3040041
Hao L, Chen L (2012) Oxidative stress responses in different organs of carp (Cyprinus carpio) with exposure to ZnO nanoparticles. Ecotoxicol Environ Saf 80:103–110. https://doi.org/10.1016/j.ecoenv.2012.02.017
Hartmann NB, Baun A (2010) The nano cocktail: ecotoxicological effects of engineered nanoparticles in chemical mixtures. Integr Environ Assess Manag 6:311–313. https://doi.org/10.1002/ieam.39
Hasnidawani JN, Azlina HN, Norita H, Bonnia NN, Ratim S, Ali ES (2016) Synthesis of ZnO nanostructures using sol-gel method. Procedia Chem 19:211–216. https://doi.org/10.1016/j.proche.2016.03.095
Hayhurst LD, Martin JD, Wallace SJ, Langlois VS, Xenopoulos MA, Metcalfe CD, Rennie (2020) Multi-level responses of yellow perch (Perca flavescens) to a whole-lake nanosilver addition study. Arch Environ Contam Toxicol 79:283–297. https://doi.org/10.1007/s00244-020-00764-5
Hossain Z, Mustafa G, Komatsu S (2015) Plant responses to nanoparticle stress. Int J Mol Sci 16(11):26644–26653. https://doi.org/10.3390/ijms161125980
Hernández-Moreno D, Valdehita A, Conde E, Rucandio I, Navas JM, Fernández-Cruz ML (2019) Acute toxic effects caused by the co-exposure of nanoparticles of ZnO and Cu in rainbow trout. Sci Total Environ 687:24–33. https://doi.org/10.1016/j.scitotenv.2019.06.084
Hua J, Peijnenburg WJ, Vijver MG (2016) TiO2 nanoparticles reduce the effects of ZnO nanoparticles and Zn ions on zebrafish embryos (Danio rerio). NanoImpact 2:45–53. https://doi.org/10.1016/j.impact.2016.06.005
Jang MH, Kim WK, Lee SK, Henry TB, Park JW (2014) Uptake, tissue distribution, and depuration of total silver in common carp (Cyprinus carpio) after aqueous exposure to silver nanoparticles. Environ Sci Technol 48:11568–11574. https://doi.org/10.1021/es5022813
Jebali J, Sabbagh M, Banni M, Kamel N, Ben-Khedher S, M’hamdi N, Boussetta H (2013) Multiple biomarkers of pollution effects in Solea solea fish on the Tunisia coastline. Environ Sci Pollut Res 20:3812–3821. https://doi.org/10.1007/s11356-012-1321-2
Johari SA, Kalbassi MR, Yu IJ, Lee JH (2015) Chronic effect of waterborne silver nanoparticles on rainbow trout (Oncorhynchus mykiss): histopathology and bioaccumulation. Comp Clin Path 24:995–1007. https://doi.org/10.1007/s00580-014-2019-2
Ju-Nam Y, Lead JR (2008) Manufactured nanoparticles: an overview of their chemistry, interactions and potential environmental implications. Sci Total Environ 400:396–414. https://doi.org/10.1016/j.scitotenv.2008.06.042
Kalman J, Riba I, DelValls TÁ, Blasco J (2010) Comparative toxicity of cadmium in the commercial fish species Sparus aurata and Solea senegalensis. Ecotoxicol Environ Saf 73:306–311. https://doi.org/10.1016/j.ecoenv.2009.10.013
Kaviani EF, Naeemi AS, Salehzadeh A (2019) Influence of copper oxide nanoparticle on hematology and plasma biochemistry of Caspian trout (Salmo trutta caspius), following acute and chronic exposure. Pollution 5:225–234. https://doi.org/10.22059/poll.2018.251034.383
Kaviani FE, Naeemi AS, Salehzadeh A (2020) Acute toxicity and effects of titanium dioxide nanoparticles (TiO2 NPs) on some metabolic enzymes and hematological indices of the endangered Caspian trout juveniles (Salmo trutta caspius Kessler, 1877). Iran J Fish Sci 19:1253–1267. https://doi.org/10.22092/ijfs.2019.119319
Kaya H, Aydın F, Gürkan M, Yılmaz S, Ates M, Demir V, Arslan Z (2016) A comparative toxicity study between small and large size zinc oxide nanoparticles in tilapia (Oreochromis niloticus): Organ pathologies, osmoregulatory responses and immunological parameters. Chemosphere 144:571–582. https://doi.org/10.1016/j.chemosphere.2015.09.024
Kelly JM, Janz DM (2009) Assessment of oxidative stress and histopathology in juvenile northern pike (Esox lucius) inhabiting lakes downstream of a uranium mill. Aquat Toxicol 92:240–249. https://doi.org/10.1016/j.aquatox.2009.02.007
Khosravi-Katuli K, Lofrano G, Nezhad HP, Giorgio A, Guida M, Aliberti F, Siciliano A, Carotenuto M, Galdiero E, Rahimi E, Libralato G (2018) Effects of ZnO nanoparticles in the Caspian roach (Rutilus rutilus caspicus). Sci Total Environ 626:30–41. https://doi.org/10.1016/j.scitotenv.2018.01.085
Kim J, Kim S, Lee S (2011) Differentiation of the toxicities of silver nanoparticles and silver ions to the Japanese medaka (Oryzias latipes) and the cladoceran Daphnia magna. Nanotoxicology 5:208–214. https://doi.org/10.3109/17435390.2010.508137
Kumar N, Chandan NK, Wakchaure GC, Singh NP (2020) Synergistic effect of zinc nanoparticles and temperature on acute toxicity with response to biochemical markers and histopathological attributes in fish. Comp Biochem Physiol C Toxicol Pharmacol 229:108678. https://doi.org/10.1016/j.cbpc.2019.108678
Kwok KW, 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 120:59–66. https://doi.org/10.1016/j.aquatox.2012.04.012
Liu J, Feng X, Wei L, Chen L, Song B, Shao L (2016) The toxicology of ion-shedding zinc oxide nanoparticles. Crit Rev Toxicol 46:348–384. https://doi.org/10.3109/10408444.2015.1137864
Mahjoubian M, Naeemi AS, Sheykhan M (2021) Toxicological effects of Ag2O and Ag2CO3 doped TiO2 nanoparticles and pure TiO2 particles on Zebrafish (Danio rerio). Chemosphere 263:128182. https://doi.org/10.1016/j.chemosphere.2020.128182
Mohsenpour R, Mousavi-Sabet H, Hedayati A, Rezaei A, Yalsuyi AM, Faggio C (2020) In vitro effects of silver nanoparticles on gills morphology of female Guppy (Poecilia reticulate) after a short-term exposure. Microsc Res Tech 83:1552–1557. https://doi.org/10.1002/jemt.23549
Maurer-Jones MA, Mousavi MPS, Chen LD, Buhlmann P, Haynes CL (2013) Characterization of silver ion dissolution from silver nanoparticles using fluorous-phase ion-selective electrodes and assessment of resultant toxicity to Shewanella oneidensis. Chem Sci 4(6):2564–2572. https://doi.org/10.1039/C3SC50320H
Manjunatha B, Park SH, Kim K, Kundapur RR, Lee SJ (2018) In vivo toxicity evaluation of pristine graphene in developing zebrafish (Danio rerio) embryos. Environ Sci Pollut Res Int 25:12821–12829. https://doi.org/10.1007/s11356-018-1420-9
Manjunatha B, Park SH, Kundapur RR, Lee SJ (2019) Graphene oxide induces cardiovascular defects in developing zebrafish (Danio rerio) embryo model: in-vivo toxicity assessment. Sci Total Environ 673:810–820. https://doi.org/10.1016/j.scitotenv.2019.04.082
Mansouri B, Ebrahimpour M, Babaei H (2012) Bioaccumulation and elimination of nickel in the organs of black fish (Capoeta fusca). Toxicol Ind Health 28:361–368. https://doi.org/10.1177/0748233711412425
Mansouri B, Maleki A, Johari SA, Shahmoradi B, Mohammadi E, Shahsavari S, Davari B (2016a) Copper bioaccumulation and depuration in common carp (Cyprinus carpio) following co-exposure to TiO2 and CuO nanoparticles. Arch Environ Contam Toxicol 71:541–552. https://doi.org/10.1007/s00244-016-0313-5
Mansouri B, Maleki A, Davari B, Johari SA, Shahmoradi B, Mohammadi E, Shahsavari S (2016b) Histopathological effects following short-term co-exposure of Cyprinus carpio to nanoparticles of TiO2 and CuO. Environ Monit Assess 188:1–12. https://doi.org/10.1007/s10661-016-5579-6
Mansouri B, Maleki A, Johari SA, Reshahmanish N (2015) Effects of cobalt oxide nanoparticles and cobalt ions on gill histopathology of zebrafish (Danio rerio). Aquac Aquar Conserv Legis 8:438–444
Mansouri B, Maleki A, Johari SA, Shahmoradi B, Mohammadi E, Davari B (2017) Histopathological effects of copper oxide nanoparticles on the gill and intestine of common carp (Cyprinus carpio) in the presence of titanium dioxide nanoparticles. Chem Ecol 33:295–308. https://doi.org/10.1080/02757540.2017.1301436
Mohammadi G, Rashidian G, Hoseinifar SH, Naserabad SS, Van Doan H (2020) Ginger (Zingiber officinale) extract affects growth performance, body composition, haematology, serum and mucosal immune parameters in common carp (Cyprinus carpio). Fish Shellfish Immunol 99:267–273. https://doi.org/10.1016/j.fsi.2020.01.032
Naeemi AS, Elmi F, Vaezi G, Ghorbankhah M (2020) Copper oxide nanoparticles induce oxidative stress mediated apoptosis in carp (Cyprinus carpio) larva. Gene Rep 19:100676. https://doi.org/10.1016/j.genrep.2020.100676
Naasz S, Altenburger R, Kühnel D (2018) Environmental mixtures of nanomaterials and chemicals: the Trojan-horse phenomenon and its relevance for ecotoxicity. Sci Total Environ 635:1170–1181. https://doi.org/10.1016/j.scitotenv.2018.04.180
Nidya M, Umadevi M, Sankar P, Rajkumar BJ (2015) L-Glutamic acid functionalized silver nanoparticles and its nonlinear optical applications. J Mater Sci Mater Electron 26:4124–4131. https://doi.org/10.1007/s10854-015-2956-9
Nowrouzi M, Mansouri B, Hamidian AH, Zarei I, Mansouri A (2012) Metal contents in tissues of two fish species from Qeshm Island. Iran Bull Environ Contam Toxicol 89:1004–1008. https://doi.org/10.1007/s00128-012-0809-2
OECD (2006) OECD guidelines for the testing of chemicals. Test No. 221: Lemna sp. growth inhibition test. 1: 1–22. https://doi.org/10.1787/20745761
OECD (2012) OECD guidelines for the testing of chemicals. In: Section 3: Degradation and accumulation test No. 305: Bioaccumulation in Fish: aqueous and dietary exposure. OECD Publishing. https://doi.org/10.1787/2074577x
Omar WA, Saleh YS, Marie MAS (2014) Integrating multiple fish biomarkers and risk assessment as indicators of metal pollution along the Red Sea coast of Hodeida, Yemen Republic. Ecotoxicol Environ Saf 110:221–231. https://doi.org/10.1016/j.ecoenv.2014.09.004
Osborne OJ, Lin S, Chang CH, Ji Z, Yu X, Wang X, Lin S, Xia T, Nel AE (2015) Organ-specific and size-dependent Ag nanoparticle toxicity in gills and intestines of adult zebrafish. ACS Nano 9:9573–9584. https://doi.org/10.1021/acsnano.5b04583
Pandurangan M, Kim DH (2015) In vitro toxicity of zinc oxide nanoparticles: a review. J Nanoparticle Res 17:1–8. https://doi.org/10.1007/s11051-015-2958-9
Paulpandian P, Beevi IS, Somanath B, Kamatchi RK, Paulraj B, Faggio C (2022) Impact of Camellia sinensis iron oxide nanoparticle on growth, hemato-biochemical and antioxidant capacity of blue gourami (Trichogaster trichopterus) fingerlings. Biol Trace Elem Res. https://doi.org/10.1007/s12011-022-03145-2
Pulit-Prociak J, Banach M (2016) Silver nanoparticles—a material of the future? Open Chem 14:76–91. https://doi.org/10.1515/chem-2016-0005
Park CB, Jung JW, Baek M, Sung B, Park JW, Seol Y, Yeom DH, Park JW, Kim YJ (2019) Mixture toxicity of metal oxide nanoparticles and silver ions on Daphnia magna. J Nanopart Res 21:1–3. https://doi.org/10.1007/s11051-019-4606-2
Pavlaki MD, Morgado RG, van Gestel CA, Calado R, Soares AM, Loureiro S (2017) Influence of environmental conditions on the toxicokinetics of cadmium in the marine copepod Acartia tonsa. Ecotoxicol Environ Saf 145:142–149. https://doi.org/10.1016/j.ecoenv.2017.07.008
Peijnenburg WJ, Baalousha M, Chen J, Chaudry Q, Von der Kammer F, Kuhlbusch TA, Lead J, Nickel C, Quik JT, Renker M, Wang Z (2015) A review of the properties and processes determining the fate of engineered nanomaterials in the aquatic environment. Crit Rev Environ Sci Technol 45:2084–2134. https://doi.org/10.1080/10643389.2015.1010430
Piccinno F, Gottschalk F, Seeger S, Nowack B (2012) Industrial production quantities and uses of ten engineered nanomaterials in Europe and the world. J Nanoparticle Res 14:1–11. https://doi.org/10.1007/s11051-012-1109-9
Pirsaheb M, Azadi NA, Miglietta ML, Sayadi MH, Blahova J, Fathi M, Mansouri B (2019) Toxicological effects of transition metal-doped titanium dioxide nanoparticles on goldfish (Carassius auratus) and common carp (Cyprinus carpio). Chemosphere 215:904–915. https://doi.org/10.1016/j.chemosphere.2018.10.111
Prabhu S, Poulose EK (2012) Silver nanoparticles: mechanism of anti-microbial action, synthesis, medical applications, and toxicity effects. Int Nano Lett 2:1–10. https://doi.org/10.1186/2228-5326-2-32
Rahmani R, Hamesadeghi Y, Mansouri A (2019) Toxicity effects of mercury and silver nanoparticles on common carp (Cyprinus carpio). Comp Clin Pat 28:811–816. https://doi.org/10.1007/s00580-019-02933-y
Rajaei G, Mansouri B, Jahantigh H, Hamidian AH (2012) Heavy metal concentrations in the water of the Chah nimeh reservoirs from Zabol. Iran Bull Environ Contam Toxicol 89:495–500. https://doi.org/10.1007/s00128-012-0738-0
Sayadi MH, Mansouri B, Shahri E, Tyler CR, Shekari H, Kharkan J (2020) Exposure effects of iron oxide nanoparticles and iron salts in blackfish (Capoeta fusca): acute toxicity, bioaccumulation, depuration, and tissue histopathology. Chemosphere 247:125900. https://doi.org/10.1016/j.chemosphere.2020.125900
Sayed AEDH, Mekkawy IA, Mahmoud UM, Nagiub M (2020) Histopathological and histochemical effects of silver nanoparticles on the gills and muscles of African catfish (Clarias garepinus). Sci Afr 7:e00230. https://doi.org/10.1016/j.sciaf.2019.e00230
Shaluei F, Hedayati A, Jahanbakhshi A, Kolangi H, Fotovat M (2013) Effect of subacute exposure to silver nanoparticle on some hematological and plasma biochemical indices in silver carp (Hypophthalmichthys molitrix). Hum Exp Toxicol 32:1270–1277. https://doi.org/10.1177/0960327113485258
Shehata AM, Salem FM, El-Saied EM, Abd El-Rahman SS, Mahmoud MY, Noshy PA (2021) Zinc nanoparticles ameliorate the reproductive toxicity induced by silver nanoparticles in male rats. Int J Nanomedicine 16:2555–2568. https://doi.org/10.2147/IJN.S307189
Song L, Connolly M, Fernández-Cruz ML, Vijver MG, Fernández M, Conde E, de Snoo GR, Peijnenburg WJ, Navas JM (2014) Species-specific toxicity of copper nanoparticles among mammalian and piscine cell lines. Nanotoxicology 8:383–393. https://doi.org/10.3109/17435390.2013.790997
Taherian SMR, Hosseini SA, Jafari A, Etminan A, Birjandi M (2019) Acute toxicity of zinc oxide nanoparticles from Satureja hortensis on Rainbow Trout (Oncorhynchus mykiss). Turk J Fish Aquat Sci 20:481–489. https://doi.org/10.4194/1303-2712-v20_6_06
Tong T, Wilke CM, Wu J, Binh CTT, Kelly JJ, Gaillard JF, Gray KA (2015) Combined toxicity of nano-ZnO and nano-TiO2: from single-to multinanomaterial systems. Environ Sci Technol 49:8113–8123. https://doi.org/10.1021/acs.est.5b02148
Vale G, Mehennaoui K, Cambier S, Libralato G, Jomini S, Domingos RF (2016) Manufactured nanoparticles in the aquatic environment-biochemical responses on freshwater organisms: a critical overview. Aquat Toxicol 170:162–174. https://doi.org/10.1016/j.aquatox.2015.11.019
Venkatachalam P, Jayaraj M, Manikandan R, Geetha N, Rene ER, Sharma NC, Sahi SV (2017) Zinc oxide nanoparticles (ZnO NPs) alleviate heavy metal-induced toxicity in Leucaena leucocephala seedlings: a physiochemical analysis. Plant Physiol Biochem 110:59–69. https://doi.org/10.1016/j.plaphy.2016.08.022
Vali S, Majidiyan N, Yalsuyi AM, Vajargah MF, Prokić MD, Faggio C (2022) Ecotoxicological effects of silver nanoparticles (Ag-NPs) on parturition time, survival rate, reproductive success and blood parameters of adult common molly (Poecilia sphenops) and their larvae. Water 14:144. https://doi.org/10.3390/w14020144
Wu Y, Zhou Q (2013) Silver nanoparticles cause oxidative damage and histological changes in medaka (Oryzias latipes) after 14 days of exposure. Environ Toxicol Chem 32(1):165–173. https://doi.org/10.1002/etc.2038
Xiao B, Wang X, Yang J, Wang K, Zhang Y, Sun B, Zhang T, Zhu L (2020) Bioaccumulation kinetics and tissue distribution of silver nanoparticles in zebrafish: the mechanisms and influence of natural organic matter. Ecotoxicol Environ Saf 194:110454. https://doi.org/10.1016/j.ecoenv.2020.110454
Xiong D, Fang T, Yu L, Sima X, Zhu W (2011) Effects of nano-scale TiO2, ZnO and their bulk counterparts on zebrafish: acute toxicity, oxidative stress and oxidative damage. Sci Total Environ 409:1444–1452. https://doi.org/10.1016/j.scitotenv.2011.01.015
Ye N, Wang Z, Wang S, Peijnenburg WJ (2018) Toxicity of mixtures of zinc oxide and graphene oxide nanoparticles to aquatic organisms of different trophic level: particles outperform dissolved ions. Nanotoxicology 12:423–438. https://doi.org/10.1080/17435390.2018.1458342
Yecheskel Y, Dror I, Berkowitz B (2018) Silver nanoparticle (Ag-NP) retention and release in partially saturated soil: column experiments and modelling. Environ Sci Nano 5:422–435. https://doi.org/10.1039/C7EN00990A
Yu R, Wu J, Liu M, Zhu G, Chen L, Chang Y, Lu H (2016) Toxicity of binary mixtures of metal oxide nanoparticles to Nitrosomonas europaea. Chemosphere 153:187–197. https://doi.org/10.1016/j.chemosphere.2016.03.065
Zhang L, Wang WX (2007) Size-dependence of the potential for metal biomagnification in early life stages of marine fish. Environ Toxicol Chem Int J 26:787–794. https://doi.org/10.1897/06-348R.1
Acknowledgements
The data provided in this study were taken from the first author's Ph.D. Dissertation project. The authors of this study gratefully acknowledge Guilan University of Medical Science, Langrud paramedical faculty for their contribution to tissue analysis.
Funding
The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Investigation: MM; Resources: MM; Formal Analysis: MM, ASN, and ZM-S; Writing original draft: MM; Supervision: ASN; Conceptualization: ASN, BM, and ZM-S; Methodology: ASN and BM; Writing—reviewing and editing: ASN, BM, and CRT; Validation: CRT.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Ethics Approval
This study was conducted by the World Medical Association Declaration of Helsinki. This study was approved by the Research and Ethics Committee of Kermanshah University of Medical Sciences (IR.KUMS.REC.1400.479).
Consent to Participate
Not applicable.
Consent for Publication
Not applicable.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Mahjoubian, M., Naeemi, A.S., Moradi-Shoeili, Z. et al. Toxicity of Silver Nanoparticles in the Presence of Zinc Oxide Nanoparticles Differs for Acute and Chronic Exposures in Zebrafish. Arch Environ Contam Toxicol 84, 1–17 (2023). https://doi.org/10.1007/s00244-022-00965-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00244-022-00965-0