Salinity modulates biochemical and histopathological changes caused by silver nanoparticles in juvenile Persian sturgeon (Acipenser persicus)

  • Ashkan BananEmail author
  • Mohammad Reza KalbassiEmail author
  • Mahmoud Bahmani
  • Ebrahim Sotoudeh
  • Seyed Ali Johari
  • Jonathan M. Ali
  • Alan S. Kolok
Research Article


The objective of this study was to evaluate the effect of salinity on the acute and sub-chronic toxicity of silver nanoparticles (AgNPs) in Persian sturgeon. This was evaluated by exposing Persian sturgeon to AgNPs in three salinities: freshwater (F: 0.4 ppt), brackish water 1 (B1: 6 ± 0.2 ppt), and brackish water 2 (B2: 12 ± 0.3 ppt) for 14 days, which was followed by analysis of alterations in plasma chemistry and histopathology of the gills, liver, and intestine. Values of 96-h median lethal concentration (LC50) were calculated as 0.89 mg/L in F, 2.07 mg/L in B1, and 1.59 mg/L in B2. After sub-chronic exposures, plasma cortisol, glucose, potassium, and sodium levels illustrated no significant changes within each salinity level. In F, 0.2 mg/L AgNP caused the highest levels of alkaline phosphatase and osmolality levels. In B1, 0.6 mg/L AgNP induced the highest level of alkaline phosphatase and elevated plasma osmolality was recorded in all AgNP-exposed treatments in comparison with the controls. The B2 treatment combined with 0.6 mg/L AgNP significantly reduced plasma chloride level. The results showed elevating salinity significantly increased osmolality, chloride, sodium, and potassium levels of plasma in the fish exposed to AgNPs. The abundance of the tissue lesions was AgNP concentration-dependent, where the highest number of damages was observed in the gills, followed by liver and intestine, respectively. The histopathological study also confirmed alterations such as degeneration of lamella, lifting of lamellar epithelium, hepatic vacuolation, pyknotic nuclei, and cellular infiltration of the lamina propria elicited by AgNPs in the gills, liver, and intestine of Persian sturgeon. In conclusion, the stability of AgNPs in aquatic environments can be regulated by changing the salinity, noting that AgNPs are more stable in low salinity waters.


Metal nanoparticles Nanoecotoxicology Histopathology Colloidal silver Persian sturgeon Gills 



The corresponding authors would like to acknowledge the support of Lorestan University, Tarbiat Modares University, University of Nebraska at Omaha and Iran Nanotechnology Initiative Council.

Funding information

This study was financially supported by Iran’s Ministry of Science, Research and Technology (MSRT, IRAN) (grant number 92-5641).


  1. Abedi S, Sharifpour I, Mozanzadeh MT, Zorriehzahra J, Khodabandeh S, Gisbert E (2015) A histological and ultrastructural study of the skin of rainbow trout (Oncorhynchus mykiss) alevins exposed to different levels of ultraviolet B radiation. J Photochem Photobiol B 147:56–62CrossRefGoogle Scholar
  2. Afshinnia K, Marrone B, Baalousha M (2018) Potential impact of natural organic ligands on the colloidal stability of silver nanoparticles. Sci Total Environ 625:1518–1526CrossRefGoogle Scholar
  3. 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 126:104–115CrossRefGoogle Scholar
  4. Ale A, Rossi AS, Bacchetta C, Gervasio S, de la Torre FR, Cazenave J (2018) Integrative assessment of silver nanoparticles toxicity in Prochilodus lineatus fish. Ecol Indic 93:1190–1198CrossRefGoogle Scholar
  5. APHA, American Public Health Association, American Water Works Association, Water Environment Association (1998) Standard methods for the examination of water and wastewater. 20th edition. American Public Health Association, Washington, D.C., USAGoogle Scholar
  6. Ansar S, Abudawood M, Hamed SS, Aleem MM (2017) Sodium selenite protects against silver nanoparticle-induced testicular toxicity and inflammation. Biol Trace Elem Res 175:161CrossRefGoogle Scholar
  7. 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. J Nanobiotechnol 10:1–14CrossRefGoogle Scholar
  8. Bacchetta C, Ale A, Simoniello MF, Gervasio S, Davico C, Rossi AS, Desimone MF, Poletta G, López G, Monserrat JM, Cazenave J (2017) Genotoxicity and oxidative stress in fish after a short-term exposure to silver nanoparticles. Ecol Indic 76:230–239CrossRefGoogle Scholar
  9. Banan A, Kalbassi Masjed Shahi MR, Bahmani M, Yazdani Sadati MA (2016) Toxicity assessment of silver nanoparticles in Persian sturgeon (Acipenser persicus) and starry sturgeon (Acipenser stellatus) during early life stages. Environ Sci Pollut Res Int 23:10139–10144CrossRefGoogle Scholar
  10. Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34CrossRefGoogle Scholar
  11. Best JH, Eddy FB, Codd GA (2003) Effects of microcystis cells, cell extracts and lipopolysaccharide on drinking and liver function in rainbow trout Oncorhynchus mykiss Walbaum. Aquat Toxicol 64:419–426CrossRefGoogle Scholar
  12. Bronzi P, Rosenthal H, Gessner J (2011) Global sturgeon aquaculture production: an overview. J Appl Ichthyol 27(2):169–175CrossRefGoogle Scholar
  13. Burke J, Handy RD, Roast SD (2003) Effect of low salinity on cadmium accumulation and calcium homeostasis in the shore crab (Carcinus maenas) at fixed free Cd2+ concentrations. Environ Toxicol Chem 22:2761–2767CrossRefGoogle Scholar
  14. Cambier S, Rogeberg M, Georgantzopoulou A, Serchi T, Karlsson C, Verhaegen S, Iversen TG, Guignard C, Kruszewski M, Hoffmann L, Audinot JN, Ropstad E, Gutleb AC (2018) Fate and effects of silver nanoparticles on early life-stage development of zebrafish (Danio rerio) in comparison to silver nitrate. Sci Total Environ 610-611:972–982CrossRefGoogle Scholar
  15. Christensen EAF, Svendsen MBS, Steffensen JF (2017) Plasma osmolality and oxygen consumption of perch Perca fluviatilis in response to different salinities and temperatures. J Fish Biol 90:819–833CrossRefGoogle Scholar
  16. Du J, Tang J, Xu S, Ge J, Dong Y, Li H, Jin M (2018) A review on silver nanoparticles-induced ecotoxicity and the underlying toxicity mechanisms. Regul Toxicol Pharmacol 98:231–239CrossRefGoogle Scholar
  17. Erfan Shahkar, Dae-jung Kim, Mahmoud Mohseni, Hyeonho Yun, Sungchul C. Bai, (2015) Effects of Salinity Changes on Hematological Responses in Juvenile Ship Sturgeon Acipenser nudiventris. Fisheries and aquatic sciences 18 (1):45–50CrossRefGoogle Scholar
  18. Firat Ö, Cogun HY, Yüzereroğlu TA, Gök G, Firat Ö, Kargin F, Kötemen Y (2011) A comparative study on the effects of a pesticide (cypermethrin) and two metals (copper, lead) to serum biochemistry of Nile tilapia, Oreochromis niloticus. Fish Physiol Biochem 37:657–666CrossRefGoogle Scholar
  19. Gambardella C, Costa E, Piazza V, Fabbrocini A, Magi E, Faimali M, Garaventa F (2015) Effect of silver nanoparticles on marine organisms belonging to different trophic levels. Mar Environ Res 111:41–49CrossRefGoogle Scholar
  20. Giese B, Klaessig F, Park B, Kaegi R, Steinfeldt M, Wigger H, von Gleich A, Gottschalk F (2018) Risks, release and concentrations of engineered nanomaterial in the environment. Sci Rep 81:1565CrossRefGoogle Scholar
  21. 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 130-131:192–200CrossRefGoogle Scholar
  22. 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 79:821–853CrossRefGoogle Scholar
  23. Imsland AK, Gunnarsson S, Foss A, Stefansson SO (2003) Gill Na+,K+-ATPase activity, plasma chloride and osmolality in juvenile turbot (Scophthalmus maximus) reared at different temperatures and salinities. Aquaculture 218:671–683CrossRefGoogle Scholar
  24. INIC (2019) Iran Nanotechnology Initiative Council’s website. Accessed 10 Aug 2019
  25. 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(19):11568–11574CrossRefGoogle Scholar
  26. Johari SA, Kalbassi MR, Soltani M, Yu IJ (2013) Toxicity comparison of colloidal silver nanoparticles in various life stages of rainbow trout (Oncorhynchus mykiss). Iran J Fish Sci 12(1):76–95Google Scholar
  27. 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(5):995–1007CrossRefGoogle Scholar
  28. Johari SA, Sarkheil M, Tayemeh MB, Veisi S (2018) Influence of salinity on the toxicity of silver nanoparticles (AgNPs) and silver nitrate (AgNO3) in halophilic microalgae, Dunaliella salina. Chemosphere 209:156–162CrossRefGoogle Scholar
  29. 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 140-141(7):398–406Google Scholar
  30. Joo HS, Kalbassi MR, Johari SA (2018) Hematological and histopathological effects of silver nanoparticles in rainbow trout (Oncorhynchus mykiss)—how about increase of salinity? Environ Sci Pollut Res 25:15449CrossRefGoogle Scholar
  31. Katuli KK, Massarsky A, Hadadi A, Pourmehran Z (2014) Silver nanoparticles inhibit the gill Na+/K+-ATPase and erythrocyte AChE activities and induce the stress response in adult zebrafish (Danio rerio). Ecotoxicol Environ Saf 106:173–180CrossRefGoogle Scholar
  32. Khosravi-Katuli K, Shabani A, Paknejad H, Imanpoor MR (2018) Comparative toxicity of silver nanoparticle and ionic silver in juvenile common carp (Cyprinus carpio): accumulation, physiology and histopathology. J Hazard Mater 359:373–381CrossRefGoogle Scholar
  33. Keller AA, McFerran S, Lazareva A, Suh S (2013) Global life-cycle emissions of engineered nanomaterials. J Nanopart Res 15:1692CrossRefGoogle Scholar
  34. Lacave JM, Vicario-Parés U, Bilbao E, Gilliland D, Mura F, Dini L, Cajaraville MP, Orbea A (2018) Waterborne exposure of adult zebrafish to silver nanoparticles and to ionic silver results in differential silver accumulation and effects at cellular and molecular levels. Sci Total Environ 642:1209–1220CrossRefGoogle Scholar
  35. 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 2012:14Google Scholar
  36. Lee JW, Kim JE, Shin YJ, Ryu JS, Eom IC, Lee JS, Kim Y, Kim PJ, Choi KH, Lee BC (2014) Serum and ultrastructure responses of common carp (Cyprinus carpio L.) during long-term exposure to zinc oxide nanoparticles. Ecotoxicol Environ Saf 104:9–17CrossRefGoogle Scholar
  37. Martínez-Alvarez RM, Hidalgo MC, Domezain A, Morales AE, García-Gallego M, Sanz A (2002) Physiological changes of sturgeon Acipenser naccarii caused by increasing environmental salinity. J Exp Biol 205:3699–3706Google Scholar
  38. Masouleh FF, Amiri BM, Mirvaghefi A, Ghafoori H, Madsen SS (2017) Silver nanoparticles cause osmoregulatory impairment and oxidative stress in Caspian kutum (Rutilus kutum, Kamensky 1901). Environ Monit Assess 189(9):448CrossRefGoogle Scholar
  39. McCarthy MP, Carroll DL, Ringwood AH (2013) Tissue specific responses of oysters, Crassostrea virginica, to silver nanoparticles. Aquat Toxicol 138:123–128CrossRefGoogle Scholar
  40. Murray LM, Rennie MD, Enders EC, Pleskach K, Martin JD (2017) Effect of nanosilver on cortisol release and morphometrics in rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 36:1606–1613CrossRefGoogle Scholar
  41. Nia JR (2011) Preparation of colloidal nanosilver. Google US PatentGoogle Scholar
  42. Nickum JG, Bart HL Jr, Bowser PR, Greer IE, Hubbs C, Jenkins JA, MacMillan JR, Rachlin JW, Rose JD, Sorensen PW, Tomasso JR (2004) Guidelines for the use of fishes in research. American Fisheries Society, Bethesda, 54 pagesGoogle Scholar
  43. NIOSH (National Institute for Occupational Safety and Health) (1999) NIOSH manual of analytical methods, method no. 7300. NIOSH, CincinnatiGoogle Scholar
  44. OECD (1992) OECD guidelines for the testing of chemicals. Guideline No. 203: Acute Toxicity for Fish. Organization for Economic Cooperation and Development, ParisGoogle Scholar
  45. OECD (1984) OECD guidelines for the testing of chemicals. Guideline No. 204: Fish, Prolonged Toxicity Test: 14-Day Study. Organization for Economic Cooperation and Development, Paris, FranceGoogle Scholar
  46. Ostaszewska T, Chojnacki M, Kamaszewski M, Sawosz-Chwalibóg E (2016) Histopathological effects of silver and copper nanoparticles on the epidermis, gills, and liver of Siberian sturgeon. Environ Sci Pollut Res 23(2):1621–1633CrossRefGoogle Scholar
  47. Pulit-Prociak J, Banach M (2016) Silver nanoparticles—a material of the future...? Open Chem 14:76–91CrossRefGoogle Scholar
  48. Redding JM, Schreck CB, Birks EK, Ewing RD (1984) Cortisol and its effect on plasma thyroid hormone and electrolyte concentrations in freshwater and during seawater acclimation in yearling coho salmon, Oncorhynchus kisutch. Gen Comp Endocrinol 56:146–155CrossRefGoogle Scholar
  49. 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 466-467:232–241CrossRefGoogle Scholar
  50. Hischier R (2014) Life cycle assessment of manufactured nanomaterials: inventory modelling rules and application example. The International Journal of Life Cycle Assessment 19 (4):941–943CrossRefGoogle Scholar
  51. Salari Joo H, Kalbassi MR, Johari SA (2012) Effect of water salinity on acute toxicity of colloidal silver nanoparticles in rainbow trout (Oncorhynchus mykiss) larvae. Iran J Health Environ 5(2):121–131Google Scholar
  52. Sendra M, Yeste M, Gatica J, Moreno-Garrido I, Blasco J (2017) Direct and indirect effects of silver nanoparticles on freshwater and marine microalgae (Chlamydomonas reinhardtii and Phaeodactylum tricornutum). Chemosphere 179:279–289CrossRefGoogle Scholar
  53. 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(12):1270–1277CrossRefGoogle Scholar
  54. Shobana C, Rangasamy B, Poopal RK, Renuka S, Ramesh M (2018) Green synthesis of silver nanoparticles using Piper nigrum: tissue-specific bioaccumulation, histopathology, and oxidative stress responses in Indian major carp Labeo rohita. Environ Sci Pollut Res 25(12):11812–11832CrossRefGoogle Scholar
  55. Skeggs L Jr, Hochstrassat J (1964) Colorimetric determination of chloride in serum and plasma. Clin Chem 10:918–936Google Scholar
  56. Sotoudeh E, Mardani F (2018) Antioxidant-related parameters, digestive enzyme activity and intestinal morphology in rainbow trout (Oncorhynchus mykiss) fry fed graded levels of red seaweed, Gracilaria pygmaea. Aquac Nutr 24:777–785CrossRefGoogle Scholar
  57. Vance ME, Kuiken T, Vejerano EP, McGinnis SP, Hochella MF Jr, Rejeski D, Hull MS (2015) Nanotechnology in the real world: redeveloping the nanomaterial consumer products inventory, Beilstein J. Nanotechnol. 6:1769–1780Google Scholar
  58. Wang J, Wang W (2014) Salinity influences on the uptake of silver nanoparticles and silver nitrate by marine medaka (Oryzias melastigma). Environ Toxicol Chem 33(3):632–640CrossRefGoogle Scholar
  59. Wang H, Burgess RM, Cantwell MG, Portis LM, Perron MM, Wu F, Ho KT (2014) Stability and aggregation of silver and titanium dioxide nanoparticles in seawater: role of salinity and dissolved organic carbon. Environ Toxicol Chem 33(5):1023–1029CrossRefGoogle Scholar
  60. 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 32:165–173CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Department of Animal Sciences, Faculty of Agriculture and Natural ResourcesLorestan UniversityKhorramabadIran
  2. 2.Department of Aquaculture, School of Marine SciencesTarbiat Modares UniversityTehranIran
  3. 3.Iranian Fisheries Science and Research InstituteTehranIran
  4. 4.Department of Fisheries, Faculty of Marine Science and TechnologyPersian Gulf UniversityBushehrIran
  5. 5.Fisheries Department, Natural Resources FacultyUniversity of KurdistanSanandajIran
  6. 6.Permitting and Environmental Health BureauNew Hampshire Department of Environmental ServicesConcordUSA
  7. 7.Idaho Water Resources Research InstituteUniversity of IdahoMoscowUSA

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