Effects of Silver Nanoparticles on Hematological Parameters and Hepatorenal Functions in Laying Japanese Quails

  • Ako Rezaei
  • Amjad Farzinpour
  • Asaad Vaziry
  • Ali Jalili


Silver nanoparticles (AgNPs) have recently emerged as a powerful agents for disinfection in the poultry industry. AgNPs are capable of epithelial barriers passing from the route of exposure to the vital organs and cells. This study evaluated the effects of AgNPs on organs weights, blood biochemical, hematological, and coagulation parameters, antioxidant enzyme activities, and histopathological changes and silver concentrations of liver and kidney tissues in laying Japanese quails after exposure to the nanoparticles. The layer quails were randomly assigned to 4 groups, consisting of six replicates, three quails each. The treatments included 0, 4, 8, and 12 mg/L of AgNPs in daily drinking water for 30 weeks. AgNPs decreased the relative weight of liver, ileum and large intestine (P < 0.05). Administration of AgNPs elevated plasma fibrinogen while decreased serum aspartate aminotransferase activity (P < 0.05). The antioxidant status of the liver showed that malondialdehyde level, an end product of lipid peroxidation, was higher (P < 0.05) and catalase activity was lower (P < 0.05) in the quails exposed to AgNPs. The accumulation of silver in the liver and kidney tissues were increased in a dose-dependent manner after exposure to AgNPs (P < 0.05). Histopathological findings showed reduced lipid vacuolization of hepatocytes in the 12 mg/L AgNPs treatment. In conclusion, the results indicated that AgNPs administration to drinking water can lead to oxidative stress and liver damage in laying quails which may be a predisposing for liver dysfunction.


Silver nanoparticles Laying quails Liver Lipid peroxidation Oxidative stress 



The authors would like to appreciate University of Kurdistan and Iranian Nanotechnology Initiative Council for financial supports of this research. This work would not have been completed without the support of the Nano Nasb Pars Company, Tehran, Iran, for TEM and DLS examinations to characterize the applied AgNPs.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.


  1. 1.
    Ahamed M, AlSalhi MS, Siddiqui MKJ (2010) Silver nanoparticle applications and human health. Clin Chim Acta 411:1841–1848. CrossRefPubMedGoogle Scholar
  2. 2.
    Ognik K, Cholewińska E, Czech A, Kozłowski K, Wlazło L, Nowakowicz-Dębek B, Szlązak R, Tutaj K (2016) Effect of silver nanoparticles on the immune, redox, and lipid status of chicken blood. Czech J Anim Sci 61:450–461. CrossRefGoogle Scholar
  3. 3.
    Buzea C, Pacheco II, Robbie K (2007) Nanomaterials and nanoparticles: sources and toxicity. Biointerphases 2:17–172. CrossRefGoogle Scholar
  4. 4.
    Kim YS, Kim JS, Cho HS, Rha DS, Kim JM, Park JD, Choi BS, Lim R, Chang HK, Chung YH, Kwon IH, Jeong J, Han BS, Yu IJ (2008) Twenty-eight-day oral toxicity, genotoxicity, and gender–related tissue distribution of silver nanoparticles in Sprague–Dawley rats. Inhal Toxicol 20:575–583. CrossRefPubMedGoogle Scholar
  5. 5.
    Kim YS, Song MY, Park JD, Song KS, Ryu HR, Chung YH, Chang HK, Lee JH, Oh KH, Kelman BJ, Hwang IK, Yu IJ (2010) Subchronic oral toxicity of silver nanoparticles. Part Fibre Toxicol 7:1–11. CrossRefGoogle Scholar
  6. 6.
    Jun EA, Lim KM, Kim K, Bae ON, Noh JY, Chung KH, Chung JH (2011) Silver nanoparticles enhance thrombus formation through increased platelet aggregation and procoagulant activity. Nanotoxicology 5:157–167. CrossRefPubMedGoogle Scholar
  7. 7.
    Tang J, Xiong L, Wang S, Wang J, Liu L, Li J, Yuan F, Xi T (2009) Distribution, translocation and accumulation of silver nanoparticles in rats. J Nanosci Nanotechnol 9:1–9. CrossRefGoogle Scholar
  8. 8.
    Korani M, Rezayat SM, Gilani K, Arbabi Bidgoli S, Adeli S (2011) Acute and subchronic dermal toxicity of nanosilver in guinea pig. Int J Nanomedicine 6:855–861. CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Ema M, Okuda H, Gamo M, Honda K (2017) A review of reproductive and developmental toxicity of silver nanoparticles in laboratory animals. Reprod Toxicol 67:149–164. CrossRefPubMedGoogle Scholar
  10. 10.
    Hussain MS, Hess KL, Gearhart JM, Geiss KT, Schlager JJ (2005) In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol in Vitro 19:975–983. CrossRefPubMedGoogle Scholar
  11. 11.
    Kim S, Choi JE, Choi J, Chung KH, Park K, Yi J, Ryu DY (2009) Oxidative stress–dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol in Vitro 23:1076–1084. CrossRefPubMedGoogle Scholar
  12. 12.
    Tiwari DK, Jin T, Behari J (2010) Dose–dependent in–vivo toxicity assessment of silver nanoparticle in Wistar rats. Toxicol Mech Methods 21:13–24. CrossRefPubMedGoogle Scholar
  13. 13.
    van der Zende M, Vanderbriel RJ, Van Doren E et al (2012) Distribution, elimination, and toxicity of silver nanoparticles and silver ions in rats after 28–day oral exposure. ACS Nano 6:7427–7442. CrossRefGoogle Scholar
  14. 14.
    Gaiser BK, Hirn S, Kermanizadeh A, Kanase N, Fytianos K, Wenk A, Haberl N, Brunelli A, Kreyling WG, Stone V (2013) Effects of silver nanoparticles on the liver and hepatocytes in vitro. Toxicol Sci 131:537–547. CrossRefPubMedGoogle Scholar
  15. 15.
    Milić M, Leitinger G, Pavičić I, Zebić Avdičević M, Dobrović S, Goessler W, Vinković Vrček I (2014) Cellular uptake and toxicity effects of silver nanoparticles in mammalian kidney cells. J Appl Toxicol 35:581–592. PubMedGoogle Scholar
  16. 16.
    Alarifi A, Ali D, Al Ghurabi MA, Alkahtani S (2016) Determination of nephrotoxicity and genotoxic potential of silver nanoparticles in Swiss albino mice. Toxicol Environ Chem 99:294–301. CrossRefGoogle Scholar
  17. 17.
    AshaRani PV, Low Kah Mun G, Hande MP, Valiyaveettil S (2009) Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3:279–290. CrossRefPubMedGoogle Scholar
  18. 18.
    Wu Y, Zhou Q (2013) Silver nanoparticles caused oxidative damage and histological changes in Medaka (Oryzias Latipes) after 14 days of exposure. Environ Toxicol Chem 32:165–173. CrossRefPubMedGoogle Scholar
  19. 19.
    Adeyemi OS, Adewumi I (2014) Biochemical evaluation of silver nanoparticles in Wistar rats. Int Sch Res Notices 2014:1–8. CrossRefGoogle Scholar
  20. 20.
    Xin L, Wang J, Wu Y, Gue S, Tong J (2014) Increased oxidative stress and activated heat shock proteins in human cell lianes by silver nanoparticles. Hum Exp Toxicol 34:315–323. CrossRefPubMedGoogle Scholar
  21. 21.
    Sawosz E, Binek M, Grodzik M, Zielinska M, Sysa P, Szmidt M, Niemiec T, Chwalibog A (2007) Influence of hydrocolloidal silver nanoparticles on gastrointestinal microflora and morphology of enterocytes of quails. Arch Anim Nutr 61:444–451. CrossRefPubMedGoogle Scholar
  22. 22.
    Sawosz E, Grodzik M, Zielinska M, Niemiec T, Olszanska B, Chwalibog A (2009) Nanoparticles of silver do not affect growth, development and DNA oxidative damage in chicken embryos. Europ Poult Sci 73:208–216. doi:
  23. 23.
    Chmielowiec-Korzeniowska A, Tymczyna L, Dobrowolska M, Banach M, Nowakowicz-Dębek B, Bryl M, Drabik A, Tymczyna-Sobotka M, Kolejko M (2015) Silver (Ag) in tissues and eggshells, biochemical parameters and oxidative stress in chickens. Open Chem 13:1269–1274. CrossRefGoogle Scholar
  24. 24.
    National Research Council (1994) Nutrient requirements of poultry, 9th edn. National Academy Press, Washington DCGoogle Scholar
  25. 25.
    Rahman Nia J (2009) Preparation of colloidal nanosilver. US Patent application docket 20090013825, 15 January 2009Google Scholar
  26. 26.
    Cherian G, Holsonbake TB, Goeger MP, Bildfell R (2002) Dietary CLA alters yolk and tissue FA composition and hepatic histopathology of laying hens. Lipids 37:751–757. CrossRefPubMedGoogle Scholar
  27. 27.
    Wan AT, Conyers RA, Coombos CJ, Masterton JP (1991) Determination of silver in blood, urine, and tissues of volunteers and burn patients. Clin Chem 37:1683–1687. PubMedGoogle Scholar
  28. 28.
    Campbell TW (1988) Avian hematology and cytology. Iowa State University Press, AmesGoogle Scholar
  29. 29.
    Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474. CrossRefPubMedGoogle Scholar
  30. 30.
    Pagila DE, Valentine WNJ (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169Google Scholar
  31. 31.
    Satoh K (1978) Serum lipid peroxide in cerebrovascular disorders determined by a new colorimetric method. Clin Chim Acta 90:37–43. CrossRefPubMedGoogle Scholar
  32. 32.
    Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. CrossRefPubMedGoogle Scholar
  33. 33.
    Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. CrossRefPubMedGoogle Scholar
  34. 34.
    SAS Institute (2003) SAS Users Guide. Version 9.1 reviews. SAS Institute Inc, CaryGoogle Scholar
  35. 35.
    Loeschner K, Hadrup N, Qvortup K, Larsen A, Gao X, Vogel U, Mortensen A, Lam HR, Larsen EH (2011) Distribution of silver in rats following 28 days of repeated oral exposure to silver nanoparticles or silver acetate. Part Fibre Toxicol 8:1–14. CrossRefGoogle Scholar
  36. 36.
    Jeong GN, Jo UB, Ryo HY, Kim YS, Song KS, Yu IJ (2010) Histochemical study of intestinal mucins after administration of silver nanoparticles in Sprague–Dawley rats. Arch Toxicol 84:63–69. CrossRefPubMedGoogle Scholar
  37. 37.
    Williams K, Milner J, Boudreau MD, Gokulan K, Cerniglia CE, Khare S (2014) Effects of subchronic exposure of silver nanoparticles on intestinal microbiota and gut–associated immune responses in the ileum of Sprague–Dawley rats. Nanotoxicology 9:279–289. CrossRefPubMedGoogle Scholar
  38. 38.
    Williams KM, Gokulan K, Cerniglia CE, Khare S (2016) Size and dose dependent effects of silver nanoparticle exposure on intestinal permeability in an in vitro model of the human gut epithelium. J Nanobiotechnology 14:1–13. CrossRefGoogle Scholar
  39. 39.
    Böhmert L, Niemann B, Lichtenstein D, Juling S, Lampen A (2015) Molecular mechanism of silver nanoparticles in human intestinal cells. Nanotoxicology 9:852–860. CrossRefPubMedGoogle Scholar
  40. 40.
    Shahare B, Yashpal M, Singh G (2013) Toxic effects of repeated oral exposure of silver nanoparticles on small intestine mucosa of mice. Toxicol Mech Methods 23:161–167. CrossRefPubMedGoogle Scholar
  41. 41.
    Harr KE (2002) Clinical chemistry of companion avian species: a review. Vet Clin Pathol 31:140–151. CrossRefPubMedGoogle Scholar
  42. 42.
    Sulaiman FA, Adeyemi OS, Akanji MA, Oloyede HOB, Sulaiman AA, Olatunde A, Hoseni AA, Olowolafe YV, Nlebedim RN, Muritala H, Nafiu MO, Salawu MO (2015) Biochemical and morphological alterations caused by silver nanoparticles in Wistar rats. J Acute Med 5:96–102. CrossRefGoogle Scholar
  43. 43.
    Huang H, Lai W, Cui M, Liang L, Lin Y, Fang Q, Liu Y, Xie L (2016) An evaluation of blood compatibility of silver nanoparticles. Sci Rep 6:1–15. CrossRefGoogle Scholar
  44. 44.
    Martínez-Gutierrez F, Thi EP, Silverman JM, de Oliveira CC, Svensson SL, Hoek AV, Sánchez EM, Reiner NE, Gaynor EC, Pryzdial ELG, Conway EM, Orrantia E, Ruiz F, Av-Gay Y, Bach H (2012) Antibacterial activity, inflammatory response, coagulation and cytotoxicity effects of silver nanoparticles. Nanomedicine 8:328–336. CrossRefPubMedGoogle Scholar
  45. 45.
    Laloy J, Minet V, Alpan L, Mullier F, Beken S, Toussaint O, Lucas S, Dogné JM (2014) Impact of silver nanoparticles on haemolysis, platelet function and coagulation. Nano 4:1–9. Google Scholar
  46. 46.
    Ilinskaya AN, Dobrovolskaia MA (2013) Nanoparticles and the blood coagulation system. Part II: safety concerns. Nanomedicine 8:969–981. 13.49Google Scholar
  47. 47.
    Jiang L, Li Y, Li Y, Guo C, Yu Y, Zou Y, Yang Y, Yu Y, Duan J, Geng W, Li Q, Sun Z (2015) Silica nanoparticles induced the pre–thrombotic state in rats via activation of coagulation factor XII and the JNK-NF-κB/AP-1 pathway. Toxicol Res 4:1453–1464. CrossRefGoogle Scholar
  48. 48.
    Julian RJ (2005) Production and growth related disorders and other metabolic diseases of poultry—a review. Vet J 169:350–369. CrossRefPubMedGoogle Scholar
  49. 49.
    Adeyemi OS, Faniyan TO (2014) Antioxidant status of rats administered silver nanoparticles orally. J Taibah Univ Sci 9:182–186. Google Scholar
  50. 50.
    Sung JH, Ji JH, Park JD, Yoon JU, Kim DS, Jeon KS, Song MY, Jeong J, Han BS, Han JH, Chung YH, Chang HK, Lee JH, Cho MH, Kelman BJ, Yu IJ (2009) Subchronic inhalation toxicity of silver nanoparticles. Toxicol Sci 108:452–461. CrossRefPubMedGoogle Scholar
  51. 51.
    Genter MB, Newman NC, Shertzer HG, Ali SF, Bolon B (2012) Distribution and systemic effects of intranasally administered 25 nm silver nanoparticles in adult mice. Toxicol Patol 40:1004–1013. CrossRefGoogle Scholar
  52. 52.
    Riddell C (1987) Avian histopathology. American Association of Avian Pathologists, Philadelphia, PAGoogle Scholar
  53. 53.
    Park EJ, Bae E, Yi J, Kim Y, Choi K, Lee SH, Yoon J, Lee BC, Park K (2010) Repeated–dose toxicity and inflammatory responses in mice by oral administration of silver nanoparticles. Environ Toxicol Pharmacol 30:162–168. CrossRefPubMedGoogle Scholar
  54. 54.
    Jia J, Li F, Zhou H, Bai Y, Liu S, Jiang Y, Jiang G, Yan B (2017) Oral exposure to silver nanoparticles or silver ions may aggravate fatty liver disease in overweight mice. Environ Sci Technol 51:9334–9343. CrossRefPubMedGoogle Scholar
  55. 55.
    Farzinpour A, Karashi N (2013) The effects of nano–silver on egg quality traits in laying Japanese quail. Appl Nanosci 3:95–99. CrossRefGoogle Scholar
  56. 56.
    Fournier E, Peresson P, Guy G, Hermier D (1997) Relationships between storage and secretion of hepatic lipids in two breeds of geese with different susceptibility to liver steatosis. Poult Sci 76:599–607. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Ako Rezaei
    • 1
  • Amjad Farzinpour
    • 1
  • Asaad Vaziry
    • 1
  • Ali Jalili
    • 2
  1. 1.Department of Animal Science, Faculty of AgricultureUniversity of KurdistanSanandajIran
  2. 2.Department of Immunology & HematologyKurdistan University of Medical SciencesSanandajIran

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