Journal of Isfahan Medical School

Journal of Isfahan Medical School

Evaluating the Effects of Prenatal Exposure to Silver Nanoparticles on Development of Some Internal Organs in Mice: Liver Histomorphometry of Offspring

Document Type : Original Article (s)

Authors
Seyed Reza Fatemi-Tabatabaei 1
Naim Erfani-Majd 2
Shahab Ghaderi 3
Masome Rashno 3
Khodabakhsh Rashidi 4
Mohammad Mehdi Shamsi 5
Mohammad Bahrami-Tapehebur 5
1 Associate Professor, Department of Physiology, School of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran
2 Professor, Department of Histology, School of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran
3 Department of Physiology, School of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran
4 PhD Student, Department of Histology, School of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran
5 PhD Student, Department of Anatomical Sciences, School of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran
Abstract
Background: Silver nanoparticles (AgNPs) are widely consumed in different fields of biology and exposure to them have increased. This study was designed to evaluate the effects of subcutaneous administration of silver nanoparticles during pregnancy on development of some internal organs and liver histomorphometry of mouse offspring.Methods: Fifteen pregnant NMRI female mice in three groups were subcutaneously administered every three days until delivery with 0 (control), 0.2, and 2 mg/kg of body weight (BW) of silver nanoparticles. Internal organs of five male and five female offspring from each groups were weighed following anesthesia on 28th day offspring. Histological liver sections were also prepared to assess histomorphometry of liver. Finally, results were analyzed according to the treatment and sex.Findings: There were no significant differences in offspring body weights (P > 0.05). Partial weight of spleen were lower in the group received 2 mg/kg nanoparticles compared to the control group (P < 0.01). Although liver partial weight were not significantly different between the groups (P > 0.05), the effect of silver nanoparticles on liver weight was influenced by the sex (P < 0.05), in a way that only the liver weight of male mice were increased (P < 0.05). Number of hepatocytes decreased and their size increased sex-independently in silver-nanoparticles-treated groups compared to control group (P < 0.01).Conclusion: Although exposure of pregnant mice to silver nanoparticles has no effect on the growth of their offspring, it leads to increased liver weight and liver structural changes.
Keywords
Silver nanoparticles
Liver histomorphometry
Offspring
  1. Sladkova M, Vlckova B, Pavel I, Siskova K, Slouf M. Surface-enhanced Raman scattering from a single molecularly bridged silver nanoparticle aggregate. J Mol Struct 2009; 924-926: 567-70.
  2. Ananth AN, Daniel SCG, Sironmani TA, Umapathi S. PVA and BSA stabilized silver nanoparticles based surface-enhanced plasmon resonance probes for protein detection. Colloids Surf B: Biointerfaces 2011; 85(2): 138-44.
  3. kiruba Daniel SCG, Sironmani A, Tharmaraj V, Pitchumani K. Synthesis and characterization of fluorophore attached silver nanoparticles. Bull Mater Sci 2011; 34(4): 639-43.
  4. Gurunathan S, Lee KJ, Kalishwaralal K, Sheikpranbabu S, Vaidyanathan R, Eom SH. Antiangiogenic properties of silver nanoparticles. Biomaterials 2009; 30(31): 6341-50.
  5. Asharani PV, Hande MP, Valiyaveettil S. Anti-proliferative activity of silver nanoparticles. BMC Cell Biol 2009; 10: 65.
  6. Hussain SM, Hess KL, Gearhart JM, Geiss KT, Schlager JJ. In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol In Vitro 2005; 19(7): 975-83.
  7. Arora S, Jain J, Rajwade JM, Paknikar KM. Interactions of silver nanoparticles with primary mouse fibroblasts and liver cells. Toxicol Appl Pharmacol 2009; 236(3): 310-8.
  8. Piao MJ, Kang KA, Lee IK, Kim HS, Kim S, Choi JY, et al. Silver nanoparticles induce oxidative cell damage in human liver cells through inhibition of reduced glutathione and induction of mitochondria-involved apoptosis. Toxicol Lett 2011; 201(1): 92-100.
  9. Sahu SC, Zheng J, Graham L, Chen L, Ihrie J, Yourick JJ, et al. Comparative cytotoxicity of nanosilver in human liver HepG2 and colon Caco2 cells in culture. J Appl Toxicol 2014; 34(11): 1155-66.
  10. Kim YS, Kim JS, Cho HS, Rha DS, Kim JM, Park JD, et al. Twenty-eight-day oral toxicity, genotoxicity, and gender-related tissue distribution of silver nanoparticles in Sprague-Dawley rats. Inhal Toxicol 2008; 20(6): 575-83.
  11. Kim YS, Song MY, Park JD, Song KS, Ryu HR, Chung YH, et al. Subchronic oral toxicity of silver nanoparticles. Part Fibre Toxicol 2010; 7: 20.
  12. Xue Y, Zhang S, Huang Y, Zhang T, Liu X, Hu Y, et al. Acute toxic effects and gender-related biokinetics of silver nanoparticles following an intravenous injection in mice. J Appl Toxicol 2012; 32(11): 890-9.
  13. Hsin YH, Chen CF, Huang S, Shih TS, Lai PS, Chueh PJ. The apoptotic effect of nanosilver is mediated by a ROS- and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cells. Toxicol Lett 2008; 179(3): 130-9.
  14. Cha K, Hong HW, Choi YG, Lee MJ, Park JH, Chae HK, et al. Comparison of acute responses of mice livers to short-term exposure to nano-sized or micro-sized silver particles. Biotechnol Lett 2008; 30(11): 1893-9.
  15. Heydarnejad MS, Yarmohammadi-Samani P, Mobini-Dehkordi M, Shadkhast M, Rahnama S. Histopathological effects of nanosilver (Ag-NPs) in liver after dermal exposure during wound healing. Nano Medical 2014; 1(3): 191-7.
  16. Korani M, Rezayat SM, Gilani K, Arbabi BS, Adeli S. Acute and subchronic dermal toxicity of nanosilver in guinea pig. Int J Nanomedicine 2011; 6: 855-62.
  17. Lee Y, Kim P, Yoon J, Lee B, Choi K, Kil KH, et al. Serum kinetics, distribution and excretion of silver in rabbits following 28 days after a single intravenous injection of silver nanoparticles. Nanotoxicology 2013; 7(6): 1120-30.
  18. Choi JE, Kim S, Ahn JH, Youn P, Kang JS, Park K, et al. Induction of oxidative stress and apoptosis by silver nanoparticles in the liver of adult zebrafish. Aquat Toxicol 2010; 100(2): 151-9.
  19. Massarsky A, Abraham R, Nguyen KC, Rippstein P, Tayabali AF, Trudeau VL, et al. Nanosilver cytotoxicity in rainbow trout (Oncorhynchus mykiss) erythrocytes and hepatocytes. Comp Biochem Physiol C Toxicol Pharmacol 2014; 159: 10-21.
  20. Akradi L, Sohrabi Haghdoost I, Djeddi AN, Mortazavi P. Histopathologic and apoptotic effect of nanosilver in liver of broiler chickens. Afr J Biotechnol 2012; 11(22): 6207-11.
  21. Lee Y, Choi J, Kim P, Choi K, Kim S, Shon W, et al. A transfer of silver nanoparticles from pregnant rat to offspring. Toxicol Res 2012; 28(3): 139-41.
  22. Wang Z, Qu G, Su L, Wang L, Yang Z, Jiang J, et al. Evaluation of the biological fate and the transport through biological barriers of nanosilver in mice. Curr Pharm Des 2013; 19(37): 6691-7.
  23. Yu WJ, Son JM, Lee J, Kim SH, Lee IC, Baek HS, et al. Effects of silver nanoparticles on pregnant dams and embryo-fetal development in rats. Nanotoxicology 2014; 8(Suppl 1): 85-91.
  24. Lankveld DP, Oomen AG, Krystek P, Neigh A, Troost-de JA, Noorlander CW, et al. The kinetics of the tissue distribution of silver nanoparticles of different sizes. Biomaterials 2010; 31(32): 8350-61.
  25. Dziendzikowska K, Gromadzka-Ostrowska J, Lankoff A, Oczkowski M, Krawczynska A, Chwastowska J, et al. Time-dependent biodistribution and excretion of silver nanoparticles in male Wistar rats. J Appl Toxicol 2012; 32(11): 920-8.
  26. Khaksary Mahabady M. The evaluation of teratogenicity of nanosilver on skeletal system and placenta of rat fetuses in prenatal period. Afr J Pharm Pharmacol 2012; 6(6): 419-24.
  27. Hong JS, Kim S, Lee SH, Jo E, Lee B, Yoon J, et al. Combined repeated-dose toxicity study of silver nanoparticles with the reproduction/developmental toxicity screening test. Nanotoxicology 2014; 8(4): 349-62.
  28. Tang J, Xiong L, Wang S, Wang J, Liu L, Li J, et al. Distribution, translocation and accumulation of silver nanoparticles in rats. J Nanosci Nanotechnol 2009; 9(8): 4924-32.
  29. Austin CA, Umbreit TH, Brown KM, Barber DS, Dair BJ, Francke-Carroll S, et al. Distribution of silver nanoparticles in pregnant mice and developing embryos. Nanotoxicology 2012; 6: 912-22.
  30. Braydich-Stolle L, Hussain S, Schlager JJ, Hofmann MC. In vitro cytotoxicity of nanoparticles in mammalian germline stem cells. Toxicol Sci 2005; 88(2): 412-9.
  31. Oberdorster G. Safety assessment for nanotechnology and nanomedicine: concepts of nanotoxicology. J Intern Med 2010; 267(1): 89-105.
  32. Puvanakrishnan P, Park J, Chatterjee D, Krishnan S, Tunnell JW. In vivo tumor targeting of gold nanoparticles: effect of particle type and dosing strategy. Int J Nanomedicine 2012; 7: 1251-8.
  33. Ghaderi S, Tabatabaei SR, Varzi HN, Rashno M. Induced adverse effects of prenatal exposure to silver nanoparticles on neurobehavioral development of offspring of mice. J Toxicol Sci 2015; 40(2): 263-75.
  34. Li Y, Zhang Y, Yan B. Nanotoxicity overview: nano-threat to susceptible populations. Int J Mol Sci 2014; 15(3): 3671-97.
  35. Fatemi M, Roodbari NH, Ghaedi K, Naderi G. The effects of prenatal exposure to silver nanoparticles on the developing brain in neonatal rats. J Biol Res-Thessalon 2013; 20(1): 233-42.
  36. Gaiser BK, Hirn S, Kermanizadeh A, Kanase N, Fytianos K, Wenk A, et al. Effects of silver nanoparticles on the liver and hepatocytes in vitro. Toxicol Sci 2013; 131(2): 537-47.
  37. Rappaport AM. Hepatic blood flow: morphologic aspects and physiologic regulation. Int Rev Physiol 1980; 21: 1-63.
  38. Hume DA. The mononuclear phagocyte system. Curr Opin Immunol 2006; 18(1): 49-53.
  39. Guillouzo A. Liver cell models in in vitro toxicology. Environ Health Perspect 1998; 106(Suppl 2): 511-32.
  40. Wijnhoven SWP, Peijnenburg WJGM, Herberts CA, Hagens WI, Oomen AG, Heugens EHW, et al. Nano-silver _ a review of available data and knowledge gaps in human and environmental risk assessment. Nanotoxicology 2009; 3(2): 109-38.
  41. Kabir SML, Rahman MM, Rahman MB, Ahmed SU. The dynamics of probiotics on growth performance and immune response in broilers. Int J Poult Sci 2004; 3(5): 361-4.
  42. Siegmund B, Rieder F, Albrich S, Wolf K, Bidlingmaier C, Firestein GS, et al. Adenosine kinase inhibitor GP515 improves experimental colitis in mice. J Pharmacol Exp Ther 2001; 296(1): 99-105.
  43. Chernousova S, Epple M. Silver as antibacterial agent: ion, nanoparticle, and metal. Angew Chem Int Ed Engl 2013; 52(6): 1636-53.
  44. Lim JH, Kim SH, Lee IC, Moon C, Kim SH, Shin DH, et al. Evaluation of maternal toxicity in rats exposed to multi-wall carbon nanotubes during pregnancy. Environ Health Toxicol 2011; 26: e2011006.
  45. Jackson P, Hougaard KS, Boisen AM, Jacobsen NR, Jensen KA, Moller P, et al. Pulmonary exposure to carbon black by inhalation or instillation in pregnant mice: effects on liver DNA strand breaks in dams and offspring. Nanotoxicology 2012; 6(5): 486-500.
  46. Crawley JN, Paylor R. A proposed test battery and constellations of specific behavioral paradigms to investigate the behavioral phenotypes of transgenic and knockout mice. Horm Behav 1997; 31(3): 197-211.
Journal of Isfahan Medical School
Volume 33, Issue 364 - Serial Number 364
November and December 2016
Pages 2247-2255

  • Receive Date 09 September 2015
  • Accept Date 06 April 2022