Environmental Science and Pollution Research

, Volume 25, Issue 16, pp 15449–15461 | Cite as

Hematological and histopathological effects of silver nanoparticles in rainbow trout (Oncorhynchus mykiss)—how about increase of salinity?

  • Hamid Salari Joo
  • Mohammad Reza Kalbassi
  • Seyed Ali Johari
Research Article


Hematological and histopathological toxicities of silver nanoparticles (Ag-NPs) to rainbow trout were assessed in three water salinities: 0.4 ppt (low salinity), 6 ± 0.3 ppt (moderate salinity), and 12 ± 0.2 ppt (high salinity). The concentrations of Ag-NPs in the low salinity were 0.032, 0.1, 0.32, and 1 ppm, and in the moderate and high salinities were 3.2, 10, 32, and 100 ppm. The results indicated a concentration-dependently increased (thrombocyte, monocyte, and large lymphocyte) and decreased (neutrophil and small lymphocyte) white blood cell count in the Ag-NP treatments in the low salinity than the other ones in the moderate and high salinities. Red blood cell volume significantly increased in all of the experimental groups exposed to higher Ag-NP concentrations, especially those in the low salinity. In the moderate and high salinities, blood plasma total protein decreased in 10 and 32 ppm Ag-NP treatments, but albumin increased in the groups in the low salinity. Blood plasma ions (Cl, Na+, K+, Ca2+, and Mg2+) showed high changes in the higher Ag-NP treatments. In all treatments, gill histological analysis demonstrated a time- and Ag-NP concentration-dependent extent of abnormalities, with the highest epithelial lifting in 1 ppm Ag-NPs in the low salinity and also the highest necrosis and aneurism in the 32 ppm treatments in other salinities. Lower Ag-NP concentrations in the low salinity led to fibrosis, villus fusion, inflammation, vacuolization, and microvillus hyperplasia in the gut, yet villi lifting and necrosis in 0.32 and 1 ppm of Ag-NPs were the main anomalies. In addition to the mentioned alterations, villi abolitions predominantly occurred in 32 ppm Ag-NP concentrations in the moderate and high salinities. Overall, despite exposing to lower Ag-NP concentrations, the fish kept in the low salinity demonstrated more vulnerability to Ag-NPs than those in the other salinities.


Blood cells Plasma ions Total protein Albumin Intestine Gill 



The authors gratefully acknowledge the support of the Tarbiat Modares University, who funded this research through a M.Sc. thesis project.

Supplementary material

11356_2018_1663_MOESM1_ESM.docx (31.5 mb)
ESM 1 (DOCX 32283 kb)


  1. Andreasen P (1985) Free and total calcium concentrations in the blood of rainbow trout, Salmo gairdneri, during ‘stress’ conditions. J Exp Biol 118:111–120Google Scholar
  2. Asghari S, Johari SA, Lee JH, Kim YS, Jeon YB, Choi HJ, Moon MC, Yu IJ (2012) Toxicity of various silver nanoparticles compared to silver ions in Daphnia magna. Journal of Nanobiotechnology 10:14CrossRefGoogle Scholar
  3. Baldisserotto B, Romero JMM, Kapoor B (2007) Fish osmoregulation. CRC Press/ Taylor and Francis Group, Boca Raton, p 540Google Scholar
  4. Beer C, Foldbjerg R, Hayashi Y, Sutherland DS, Autrup H (2012) Toxicity of silver nanoparticles—nanoparticle or silver ion? Toxicol Lett 208:286–292 Google Scholar
  5. Behra R, Sigg L, Clift MJ, Herzog F, Minghetti M, Johnston B, Petri-Fink A, Rothen-Rutishauser B (2013): Bioavailability of silver nanoparticles and ions: from a chemical and biochemical perspective. J R Soc Interface. 
  6. Bilberg K, Hovgaard MB, Besenbacher F, Baatrup E (2012) In Vivo Toxicity of Silver Nanoparticles and Silver Ions in Zebrafish (Danio rerio). J Toxicol.
  7. Boge G, Roche H (2004) In vitro effects of wastewater treatment plant effluent on sea bass red blood cells. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 139:17–22Google Scholar
  8. Choi O, Clevenger TE, Deng B, Surampalli RY, Ross L, Hu Z (2009) Role of sulfide and ligand strength in controlling nanosilver toxicity. Water Res 43:1879–1886CrossRefGoogle Scholar
  9. Clark VL, Kruse JA (1990) Clinical methods: the history, physical, and laboratory examinations. JAMA 264:2808–2809CrossRefGoogle Scholar
  10. De Smet H, Blust R, Moens L (1998) Absence of albumin in the plasma of the common carp Cyprinus carpio: binding of fatty acids to high density lipoprotein. Fish Physiol Biochem 19:71–81CrossRefGoogle Scholar
  11. Di Giulio RT, Hinton DE (2008) The toxicology of fishes. CRC Press/ Taylor and Francis Group, Boca Raton, pp 1096.
  12. Emam HE, Ahmed HB (2016) Polysaccharides templates for assembly of nanosilver. Carbohydr Polym 135:300–307CrossRefGoogle Scholar
  13. Fabrega J, Luoma SN, Tyler CR, Galloway TS, Lead JR (2011) Silver nanoparticles: behaviour and effects in the aquatic environment. Environ Int 37:517–531CrossRefGoogle Scholar
  14. Farmen E, Mikkelsen H, Evensen Ø, Einset J, Heier L, Rosseland B, Salbu B, Tollefsen K, Oughton D (2012) Acute and sub-lethal effects in juvenile Atlantic salmon exposed to low μg/L concentrations of Ag nanoparticles. Aquat Toxicol 108:78–84 Google Scholar
  15. 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 84:415–430CrossRefGoogle Scholar
  16. Felip A, Carrillo M, Herráez M, Zanuy S, Basurco B (2009) Advances in fish reproduction and their application to broodstock management: a practical manual for sea bass. Options Méditerranéennes. Série B, Études et Recherches, Paris, pp 1-95 Google Scholar
  17. Griffitt RJ, Lavelle CM, Kane AS, Denslow ND, Barber DS (2013) Chronic nanoparticulate silver exposure results in tissue accumulation and transcriptomic changes in zebrafish. Aquat Toxicol 130:192-200. 
  18. Harris J, Bird DJ (2000) Modulation of the fish immune system by hormones. Vet Immunol Immunopathol 77:163–176CrossRefGoogle Scholar
  19. Hogstrand C, Wood CM (1998) Toward a better understanding of the bioavailability, physiology, and toxicity of silver in fish: implications for water quality criteria. Environ Toxicol Chem 17:547–561CrossRefGoogle Scholar
  20. Jiang L, Yu Y, Li Y, Yu Y, Duan J, Zou Y, Li Q, Sun Z (2016) Oxidative damage and energy metabolism disorder contribute to the hemolytic effect of amorphous silica nanoparticles. Nanoscale Res Lett 11:1–12CrossRefGoogle Scholar
  21. Johari S, Kalbassi M, Soltani M, Yu I (2013) Toxicity comparison of colloidal silver nanoparticles in various life stages of rainbow trout (Oncorhynchus mykiss). Iran J Fish Sci 12:76–95Google Scholar
  22. 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 Pathol 24:995–1007CrossRefGoogle Scholar
  23. Joo HS, Kalbassi MR, Yu IJ, Lee JH, Johari SA (2013) Bioaccumulation of silver nanoparticles in rainbow trout (Oncorhynchus mykiss): influence of concentration and salinity. Aquat Toxicol 140:398–406 Google Scholar
  24. Kalbassi MR, Salari-joo H, Johari A (2011) Toxicity of silver nanoparticles in aquatic ecosystems: salinity as the main cause in reducing toxicity. Iranian Journal of Toxicology 5:436–443Google Scholar
  25. Kumar CSSR (2009) Metallic nanomaterials. Wiley-VCH, Strauss GmbH, Morlenbach, pp 598Google Scholar
  26. Lawrence AJ, Hemingway KL (2008) Effects of pollution on fish: molecular effects and population responses. Wiley, Blackwell, pp 376Google Scholar
  27. Li S-Q, Zhu R-R, Zhu H, Xue M, Sun X-Y, Yao S-D, Wang S-L (2008) Nanotoxicity of TiO2 nanoparticles to erythrocyte in vitro. Food Chem Toxicol 46:3626–3631CrossRefGoogle Scholar
  28. Lourtioz J-M, Lahmani M, Dupas-Haeberlin C, Hesto P (2016) Nanosciences and nanotechnology: evolution or revolution? Springer International Publishing, Cham.Google Scholar
  29. Massarsky A, Abraham R, Nguyen KC, Rippstein P, Tayabali AF, Trudeau VL, Moon TW (2014a) Nanosilver cytotoxicity in rainbow trout (Oncorhynchus mykiss) erythrocytes and hepatocytes. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 159:10–21Google Scholar
  30. Massarsky A, Trudeau VL, Moon TW (2014b) Predicting the environmental impact of nanosilver. Environ Toxicol Pharmacol 38:861–873CrossRefGoogle Scholar
  31. Mazon A, Monteiro E, Pinheiro G, Fernadez M (2002) Hematological and physiological changes induced by short-term exposure to copper in the freshwater fish, Prochilodus scrofa. Braz J Biol 62:621–631CrossRefGoogle Scholar
  32. Modesto KA, Martinez CB (2010) Effects of roundup transorb on fish: hematology, antioxidant defenses and acetylcholinesterase activity. Chemosphere 81:781–787CrossRefGoogle Scholar
  33. Nair PMG, Park SY, Lee S-W, Choi J (2011) Differential expression of ribosomal protein gene, gonadotrophin releasing hormone gene and Balbiani ring protein gene in silver nanoparticles exposed Chironomus riparius. Aquat Toxicol 101:31–37CrossRefGoogle Scholar
  34. Nia JR (2011) Preparation of colloidal nanosilver. In: Google Patents US7892317B2Google Scholar
  35. Nowack B, Krug HF, Height M (2011) 120 years of nanosilver history: implications for policy makers. Environmental Science & Technology 45:1177–1183CrossRefGoogle Scholar
  36. OECD (1998) OECD Guidelines for Testing of Chemicals. OECD Publishing, ParisGoogle Scholar
  37. Powers CM, Slotkin TA, Seidler FJ, Badireddy AR, Padilla S (2011) Silver nanoparticles alter zebrafish development and larval behavior: distinct roles for particle size, coating and composition. Neurotoxicol Teratol 33:708–714CrossRefGoogle Scholar
  38. Roberts RJ (2012) Fish pathology. John Wiley and Sons, Hoboken, p 592 Google Scholar
  39. Sancho E, Ceron J, Ferrando M (2000) Cholinesterase activity and hematological parameters as biomarkers of sublethal molinate exposure in Anguilla anguilla. Ecotoxicol Environ Saf 46:81–86CrossRefGoogle Scholar
  40. Schiavo S, Duroudier N, Bilbao E, Mikolaczyk M, Schäfer J, Cajaraville M, Manzo S (2017) Effects of PVP/PEI coated and uncoated silver NPs and PVP/PEI coating agent on three species of marine microalgae. Sci Total Environ 577:45–53CrossRefGoogle Scholar
  41. Sekar D, Falcioni ML, Barucca G, Falcioni G (2014) DNA damage and repair following in vitro exposure to two different forms of titanium dioxide nanoparticles on trout erythrocyte. Environ Toxicol 29:117–127CrossRefGoogle Scholar
  42. Sendra M, Moreno-Garrido I, Yeste M, Gatica J, Blasco J (2017a) Toxicity of TiO2, in nanoparticle or bulk form to freshwater and marine microalgae under visible light and UV-A radiation. Environ Pollut 227:39–48CrossRefGoogle Scholar
  43. Sendra M, Yeste M, Gatica J, Moreno-Garrido I, Blasco J (2017b) Direct and indirect effects of silver nanoparticles on freshwater and marine microalgae (Chlamydomonas reinhardtii and Phaeodactylum tricornutum). Chemosphere 179:279–289CrossRefGoogle Scholar
  44. Shaw BJ, Handy RD (2011) Physiological effects of nanoparticles on fish: a comparison of nanometals versus metal ions. Environ Int 37:1083–1097CrossRefGoogle Scholar
  45. Shirdel I, Kalbassi MR (2016) Effects of nonylphenol on key hormonal balances and histopathology of the endangered Caspian brown trout (Salmo trutta caspius). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 183:28–35Google Scholar
  46. Šiller L, Lemloh M-L, Piticharoenphun S, Mendis BG, Horrocks BR, Brümmer F, Medaković D (2013) Silver nanoparticle toxicity in sea urchin Paracentrotus. Environ Pollut 178:498-502 Google Scholar
  47. Smith CJ, Shaw BJ, Handy RD (2007) Toxicity of single walled carbon nanotubes to rainbow trout (Oncorhynchus mykiss): respiratory toxicity, organ pathologies, and other physiological effects. Aquat Toxicol 82:94–109CrossRefGoogle Scholar
  48. Thomas S, Egée S (1998) Fish red blood cells: characteristics and physiological role of the membrane ion transporters. Comp Biochem Physiol A Mol Integr Physiol 119:79–86CrossRefGoogle Scholar
  49. Varner K, El-Badaway A, Feldhake D, Venkatapathy R (2010) State of the science literature review: everything nanosilver and more. US Environmental Protection Agency, Washington DC, p 363Google Scholar
  50. Wang J, Zhou G, Chen C, Yu H, Wang T, Ma Y, Jia G, Gao Y, Li B, Sun J (2007) Acute toxicity and biodistribution of different sized titanium dioxide particles in mice after oral administration. Toxicol Lett 168:176–185CrossRefGoogle Scholar
  51. Wiwanitkit V, Sereemaspun A, Rojanathanes R (2008) Visualization of gold nanoparticle on the microscopic picture of red blood cell: implication for possible risk of nanoparticle exposure. Stoch Env Res Risk A 22:583–585CrossRefGoogle Scholar
  52. Yakhnenko V, Klimenkov I, Sudakov N, Belyshenko AY, Glyzina OY, Mamontov A, Sapozhnikova YP, Sukhanova L (2016) Morphofunctional peculiarities of erythrocytes in wild and farmed Coregonid fishes from Lake Baikal. Contemp Probl Ecol 9:219–228CrossRefGoogle Scholar
  53. Zonn IS, Kosarev AN, Glantz MH (2010) The Caspian Sea Encyclopedia. Springer, Heidelberg.

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Hamid Salari Joo
    • 1
  • Mohammad Reza Kalbassi
    • 1
  • Seyed Ali Johari
    • 2
  1. 1.Department of Marine SciencesTarbiat Modares UniversityMazandaranIran
  2. 2.Aquaculture Department, Natural Resources FacultyUniversity of KurdistanSanandajIran

Personalised recommendations