Differential Effects of Silver Nanoparticles and Silver Ions on Tissue Accumulation, Distribution, and Toxicity in the Sprague Dawley Rat Following Daily Oral Gavage Administration for 13 Weeks

Toxicological Sciences

Volumn 150, Issue 1, 2016, Pages 131-160

  Boudreau, Mary D ^a   Imam, Mohammed S ^a   Paredes, Angel M ^a   Bryant, Matthew S ^a   Cunningham, Candice K ^a   Felton, Robert P ^a   Jones, Margie Y ^a   Davis, Kelly J ^b   Olson, Greg R ^b  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^b Toxicologic Pathology Associates   (United States)

Author keywords

Accumulation; Distribution; Exposure assessment; In vivo; Nanoparticle; Oral administration rodent; Silver; Silver acetate; Transmission electron microscopy

Indexed keywords

CITRATE SODIUM; SILVER; SILVER ACETATE; SILVER NANOPARTICLE; UNCLASSIFIED DRUG; ION; METAL NANOPARTICLE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPSY; BIOACCUMULATION; BLOOD; BODY WEIGHT; CLINICAL CHEMISTRY; COLON; CONTROLLED STUDY; DRUG DISTRIBUTION; FEMALE; FLUID INTAKE; FOOD INTAKE; GENETIC SCREENING; GENITAL SYSTEM; HEMATOLOGY; HISTOPATHOLOGY; INDUCTIVELY COUPLED MASS SPECTROMETRY; JEJUNUM; KIDNEY; LIVER; MALE; MASS SPECTROMETRY; MICRONUCLEUS; MORPHOLOGY; NONHUMAN; ORGAN WEIGHT; PARTICLE SIZE; PHOTON CORRELATION SPECTROSCOPY; RAT; SEMEN ANALYSIS; SEX DIFFERENCE; SURVIVAL; TISSUE DISTRIBUTION; TRANSMISSION ELECTRON MICROSCOPY; VAGINA CYTOLOGY; ANIMAL; ATOMIC ABSORPTION SPECTROMETRY; DOSE RESPONSE; ORAL DRUG ADMINISTRATION; SEXUAL DEVELOPMENT; SPRAGUE DAWLEY RAT; SURFACE PROPERTY; TIME FACTOR;

ADMINISTRATION, ORAL; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; DYNAMIC LIGHT SCATTERING; FEMALE; IONS; MALE; METAL NANOPARTICLES; MICROSCOPY, ELECTRON, TRANSMISSION; PARTICLE SIZE; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS; SILVER; SPECTROPHOTOMETRY, ATOMIC; SURFACE PROPERTIES; TIME FACTORS; TISSUE DISTRIBUTION;

EID: 84963852505     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfv318     Document Type: Article

References (52)

1. Bailer, A. J., and Portier, C. J. (1988). Effects of treatment-induced mortality and tumor-induced mortality on tests for carcinogenicity in small samples. Biometrics 44, 417-431.
2. Bieler, G. S., and Williams, R. L. (1993). Ratio estimates, the delta method, and quantal response tests for increased carcinogenicity. Biometrics 49, 793-801.
3. Brunner, E., Domhof, S., and Langer, F. (2002). Nonparametric Analysis of Longitudinal Data in Factorial Experiments. Wiley Series in Probability and Statistics. John Wiley and Sons, New York.
4. CFR. (2010). Code of Federal Regulations (CFR) 21, Part 58. Good Laboratory Practice for Nonclinical Laboratory Studies.
5. Chen, X., and Schluesener, H. J. (2008). Nanosilver: a nanoproduct in medical application. Toxicol. Lett. 176, 1-12.
6. Clemente, G. F., Rossi, L. C., and Santaroni, G. P. (1977). Trace element intake and excretion in the Italian population. J. Radioanal. Chem. 37, 549-558.
7. Cooper, W. G., Reger, J. F., and Van Breemen, V. L. (1956). Observations on the basement membranes in rat kidney. J. Biophys. Biochem. Cytol. 2, 283-286.
8. Cumberland, S. A., and Lead, J. R. (2009). Particle size distributions of silver nanoparticles at environmentally relevant conditions. J. Chromatogr. A 1216, 9099-9105.
9. Doty, R. C., Tshikhudo, T. R., Brust, M., and Fernig, D. G. (2005). Extremely stable water-soluble Ag nanoparticles. Chem. Mater. 17, 4630-4635.
10. EPA. (2014). Integrated risk information system-silver. Journal [Online]. Available at: http://cfpub.epa.gov/ncea/iris/search/ index.cfm?keywordsilver. Accessed October 14, 2015.
11. Espinosa-Cristobal, L. F., Martinez-Castanon, G. A., Tellez-Dector, E. J., Nino-Martinez, N., Zavala-Alonso, N. V., and Loyola-Rodriguez, J. P. (2013). Adherence inhibition of Streptococcus mutans on dental enamel surface using silver nanoparticles. Mater. Sci. Eng. C Mater. Biol. Appl. 33, 2197- 2202.
12. Florence, A. T. (1997). The oral absorption of micro- and nanoparticulates: neither exceptional nor unusual. Pharm. Res. 14, 259-266.
13. Florence, A. T. (2005). Nanoparticle uptake by the oral route: fulfilling its potential? Drug Disc. Today: Technol. 2, 6.
14. Frawley, J. P., Wiebe, A. K., Klug, E. D., and Shelanski, M. V. (1964). Studies on the gastro-intestinal absorption of purified sodium carboxymethylcellulose. Food Cosmet. Toxicol. 2, 539-543.
15. Gibson, R. S., and Scythes, C. A. (1984). Chromium, selenium, and other trace element intakes of a selected sample of Canadian premenopausal women. Biol. Trace Elem. Res. 6, 105-116.
16. Hadrup, N., and Lam, H. R. (2014). Oral toxicity of silver ions, silver nanoparticles and colloidal silver-a review. Regul. Toxicol. Pharmacol. 68, 1-7.
17. Hadrup, N., Loeschner, K., Bergstrom, A., Wilcks, A., Gao, X., Vogel, U., Frandsen, H. L., Larsen, E. H., Lam, H. R., and Mortensen, A. (2012). Subacute oral toxicity investigation of nanoparticulate and ionic silver in rats. Arch. Toxicol. 86, 543-551.
18. Ham, K. N., and Tange, J. D. (1972). Silver deposition in rat glomerular basement membrane. Aust. J. Exp. Biol. Med. Sci. 50, 423-434.
19. Hamilton, E. J., and Minski, M. J. (1972/1973). Abundance of the chemical elements in man's diet and possible relations with environmental factors. Sci. Total Envron. 1, 375-394.
20. Horner, H. C., Roebuck, B. D., Smith, R. P., and English, J. P. (1983). Acute toxicity of some silver salts of sulfonamides in mice and the efficacy of penicillamine in silver. Drug Chem. Toxicol. 6, 267-277.
21. Hussain, N., Jaitley, V., and Florence, A. T. (2001). Recent advances in the understanding of uptake of microparticulates across the gastrointestinal lymphatics. Adv. Drug Deliv. Rev. 50, 35.
22. Ito, T., Sun, L., Bevan, M. A., and Crooks, R. M. (2004). Comparison of nanoparticle size and electrophoretic mobility measurements using a carbon-nanotube-based coulter counter, dynamic light scattering, transmission electron microscopy, and phase analysis light scattering. Langmuir 20, 6940-6945.
23. Jani, P., Halbert, G. W., Langridge, J., and Florence, A. T. (1990). Nanoparticle uptake by the rat gastrointestinal mucosa: quantitation and particle size dependency. J. Pharm. Pharmacol. 42, 821-826.
24. Khanal, R. C., and Nemere, I. (2008). Endocrine regulation of calcium transport in epithelia. Clin. Exp. Pharmacol. Physiol. 35, 1277-1287.
25. Kim, W. Y., Kim, J., Park, J. D., Ryu, H. Y., and Yu, I. J. (2009). Histological study of gender differences in accumulation of silver nanoparticles in kidneys of Fischer 344 rats. J. Toxicol. Environ. Health A 72, 1279-1284.
26. Kim, Y. S., Kim, J. S., Cho, H. S., Rha, D. S., Kim, J. M., Park, J. D., Choi, B. S., Lim, R., Chang, H. K., Chung, Y. H., et al. (2008). Twenty-eight-day oral toxicity, genotoxicity, and genderrelated tissue distribution of silver nanoparticles in Sprague- Dawley rats. Inhal. Toxicol. 20, 575-583.
27. Kim, Y. S., Song, M. Y., Park, J. D., Song, K. S., Ryu, H. R., Chung, Y. H., Chang, H. K., Lee, J. H., Oh, K. H., Kelman, B. J., et al. (2010). Subchronic oral toxicity of silver nanoparticles. Part. Fibre Toxicol. 7, 20.
28. Liu, J., and Hurt, R. H. (2010). Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ. Sci. Technol. 44, 2169-2175.
29. Loeschner, K., Hadrup, N., Qvortrup, K., Larsen, A., Gao, X., Vogel, U., Mortensen, A., Lam, H. R., and Larsen, E. H. (2011). Distribution of silver in rats following 28 days of repeated oral exposure to silver nanoparticles or silver acetate. Part. Fibre Toxicol. 8, 18.
30. Lok, C. N., Ho, C. M., Chen, R., He, Q. Y., Yu, W. Y., Sun, H., Tam, P. K., Chiu, J. F., and Che, C. M. (2007). Silver nanoparticles: partial oxidation and antibacterial activities. J. Biol. Inorg. Chem. 12, 527-534.
31. Matuk, Y., Ghosh, M., and McCulloch, C. (1981). Distribution of silver in the eyes and plasma proteins of the albino rat. Can. J. Ophthalmol. 16, 145-150.
32. Maunsbach, A. B., and Afzelius, B. A. (1999). Biomedical Electron Microscopy: Illustrated Methods and Presentations. Academic Press, San Diego, CA.
33. Mirsattari, S. M., Hammond, R. R., Sharpe, M. D., Leung, F. Y., and Young, G. B. (2004). Myoclonic status epilepticus following repeated oral ingestion of colloidal silver. Neurology 62, 1408-1410.
34. Moskovits, M., and Vlckova, B. (2005). Adsorbate-induced silver nanoparticle aggregation kinetics. J. Phys. Chem. B 109, 14755-14758.
35. Munger, M. A., Hadlock, G., Stoddard, G., Slawson, M. H., Wilkins, D. G., Cox, N., and Rollins, D. (2015). Assessing orally bioavailable commercial silver nanoparticle product on human cytochrome P450 enzyme activity. Nanotoxicology 9, 474-481.
36. Munger, M. A., Radwanski, P., Hadlock, G. C., Stoddard, G., Shaaban, A., Falconer, J., Grainger, D. W., and Deering-Rice, C. E. (2014). In vivo human time-exposure study of orally dosed commercial silver nanoparticles. Nanomedicine 10, 1-9.
37. NTP. (2002). Final study report. Developmental toxicity evaluation for silver acetate (CAS No. 563-63-3) administered by gavage to Sprague Dawley (CDR) rats on gestational days 6 through19. Teratology Report Series No. TER-20-001. National Institutes of Health, Public Health Service, U.S. Department of Human Health Services, National Technical Information Service, Research Triangle Park, NC.
38. NTP. (2011). Specifications for the conduct of studies to evaluate the toxic and carcinogenic potential of chemical, biological and physical agents in laboratory animals for the National Toxicology Program (NTP).
39. Oberdorster, G., Oberdorster, E., and Oberdorster, J. (2005). Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ. Health Perspect. 113, 823-839.
40. OECD. (1998). Guidelines for the Testing of Chemicals, Section 4.Health Effects.Test No. 408: Repeated dose 90-day oral toxicity study in rodents.
41. Peddada, S., and Kissling, G. (2006). A survival-adjusted quantalresponse test for analysis of tumor rates in animal carcinogenicity studies. Environ. Health Perspect. 114, 537-541.
42. Rai, M., Deshmukh, S. D., Ingle, A. P., Gupta, I. R., Galdiero, M., and Galdiero, S. (2014). Metal nanoparticles: the protective nanoshield against virus infection. Crit. Rev. Microbiol. doi: 10.3109/1040841X2013.879849, PMID:24754250.
43. Shahare, B., and Yashpal, M. (2013). Toxic effects of repeated oral exposure of silver nanoparticles on small intestine mucosa of mice. Toxicol. Mech. Methods 23, 161-167.
44. Shelanski, H. A., and Clark, A. M. (1948). Physiological action of sodium carboxymethylcellulose on laboratory animals and humans. Food Res. 13, 29-35.
45. Silver, S. (2003). Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol. Rev. 27, 341-353.
46. Tolaymat, T. M., El Badawy, A. M., Genaidy, A., Scheckel, K. G., Luxton, T. P., and Suidan, M. (2010). An evidence-based environmental perspective of manufactured silver nanoparticle in syntheses and applications: a systematic review and critical appraisal of peer-reviewed scientific papers. Sci. Total Environ. 408, 999-1006.
47. van der Zande, M., Vandebriel, R. J., Van Doren, E., Kramer, E., Herrera Rivera, Z., Serrano-Rojero, C. S., Gremmer, E. R., Mast, J., Peters, R. J., Hollman, P. C., 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.
48. Walker, F. (1971). Experimental argyria: a model for basement membrane studies. Br. J. Exp. Pathol. 52, 589-593.
49. Wijnhoven, S. W. P., Peijnenburg, W. J. G. M., Herberts, C. A., Hagens, W. I., Oomen, A. G., Heugens, E. H. W., Roszek, B., Bisschops, J., Gosens, I., Van De Meent, D., et al. (2009). Nano-silver-a review of available data and knowledge gaps in human and environmental risk assessment. Nanotoxicology 3, 109-138.
50. Williams, K., Milner, J., Boudreau, M. D., Gokulan, K., Cerniglia, C. E., and Khare, S. (2015). 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.
51. Witt, K. L., Livanos, E., Kissling, G. E., Torous, D. K., Caspary, W., Tice, R. R., and Recio, L. (2008). Comparison of flow cytometry- and microscopy-based methods for measuring micronucleated reticulocyte frequencies in rodents treated with nongenotoxic and genotoxic chemicals. Mutat. Res. 649, 101-113.
52. Zhang, S., Du, C., Wang, Z., Han, X., Zhang, K., and Liu, L. (2013). Reduced cytotoxicity of silver ions to mammalian cells at high concentration due to the formation of silver chloride. Toxicol. in vitro 27, 739-744.