Particle size dependent deposition and pulmonary inflammation after short-term inhalation of silver nanoparticles

Particle and Fibre Toxicology

Volumn 11, Issue 1, 2014, Pages

  Braakhuis, Hedwig M ^a,b   Gosens, Ilse ^b   Krystek, Petra ^c   Boere, John A F ^b   Cassee, Flemming R ^b,d   Fokkens, Paul H B ^b   Post, Jan A ^e   van Loveren, Henk ^a,b   Park, Margriet V D Z ^b  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^c PHILIPS RESEARCH LABORATORIES   (Germany)

^d UTRECHT UNIVERSITY   (Netherlands)

^e UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Cellular uptake; Dissolution; Inhalation exposure; Nanoparticles; Pulmonary toxicity

Indexed keywords

CYTOKINE; GAMMA INTERFERON; GLUTATHIONE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 6; LACTATE DEHYDROGENASE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; SILVER NANOPARTICLE; TUMOR NECROSIS FACTOR ALPHA; AIR POLLUTANT; BIOLOGICAL MARKER; METAL NANOPARTICLE; SILVER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DAMAGE; CELL DIFFERENTIATION; CELL MIGRATION; CELL NUCLEUS; CELL VACUOLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DISSOLUTION; HISTOPATHOLOGY; INHALATION; LEUKOCYTE COUNT; LUNG ALVEOLUS CELL; LUNG LAVAGE; LUNG TOXICITY; LYMPHOCYTE COUNT; MALE; NEUTROPHIL COUNT; NONHUMAN; OXIDATIVE STRESS; PARTICLE SIZE; PNEUMONIA; RAT; TISSUE DISTRIBUTION; TRANSMISSION ELECTRON MICROSCOPY; ADVERSE EFFECTS; AGONISTS; AIR POLLUTANT; ANALYSIS; ANIMAL; CHEMICALLY INDUCED; CHEMISTRY; COMPARATIVE STUDY; CYTOPLASM VESICLE; DRUG EFFECTS; EXPOSURE; FISCHER 344 RAT; GERMFREE ANIMAL; IMMUNOLOGY; LUNG; METABOLISM; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; RANDOMIZATION; RESPIRATORY FUNCTION; RESPIRATORY TRACT MUCOSA; TOXICITY; TOXICITY TESTING; TOXICOKINETICS; ULTRASTRUCTURE;

AIR POLLUTANTS; ANIMALS; BIOMARKERS; CELL NUCLEUS; CYTOKINES; CYTOPLASMIC VESICLES; GLUTATHIONE; INHALATION EXPOSURE; LUNG; MALE; METAL NANOPARTICLES; NEUTROPHIL INFILTRATION; PARTICLE SIZE; PNEUMONIA; RANDOM ALLOCATION; RATS, INBRED F344; RESPIRATORY MUCOSA; RESPIRATORY TRACT ABSORPTION; SILVER; SPECIFIC PATHOGEN-FREE ORGANISMS; TISSUE DISTRIBUTION; TOXICITY TESTS, ACUTE; TOXICOKINETICS;

EID: 84907258515     PISSN: 17438977     EISSN: 17438977     Source Type: Journal    
DOI: 10.1186/s12989-014-0049-1     Document Type: Article

References (54)

1. Nanotechnologies PoE: Consumer Products Inventory. Retrieved [June, 2014], from .., http://www.nanotechproject.org/cpi
2. Maynard AD, Kuempel ED. Airborne nanostructured particles and occupational health. J Nanoparticle Res 2005, 7:587-614. 10.1007/s11051-005-6770-9.
3. Christensen FM, Johnston HJ, Stone V, Aitken RJ, Hankin S, Peters S, Aschberger K. Nano-silver - feasibility and challenges for human health risk assessment based on open literature. Nanotoxicology 2010, 4:284-295. 10.3109/17435391003690549, 20795910.
4. Wijnhoven SWP, Peijnenburg WJGM, Herberts CA, Hagens WI, Oomen AG, Heugens EHW, Roszek B, Bisschops J, Gosens I, Meent D, Dekkers S, Jong WH, Zijverden M, Sips AJAM, Geertsma RE. Nano-silver - a review of available data and knowledge gaps in human and environmental risk assessment. Nanotoxicology 2009, 3:109-138. 10.1080/17435390902725914.
5. Sotiriou GA, Pratsinis SE. Engineering nanosilver as an antibacterial, biosensor and bioimaging material. Curr Opin Chem Eng 2011, 1:3-10. 10.1016/j.coche.2011.07.001, 23730551.
6. Sotiriou GA, Pratsinis SE. Antibacterial activity of nanosilver ions and particles. Environ Sci Technol 2010, 44:5649-5654. 10.1021/es101072s, 20583805.
7. Lok CN, Ho CM, Chen R, He QY, Yu WY, Sun H, Tam PK, Chiu JF, Che CM. Silver nanoparticles: partial oxidation and antibacterial activities. J Biol Inorg Chem 2007, 12:527-534. 10.1007/s00775-007-0208-z, 17353996.
8. Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramirez JT, Yacaman MJ. The bactericidal effect of silver nanoparticles. Nanotechnology 2005, 16:2346-2353. 10.1088/0957-4484/16/10/059, 20818017.
9. Xiu ZM, Zhang QB, Puppala HL, Colvin VL, Alvarez PJ. Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett 2012, 12:4271-4275. 10.1021/nl301934w, 22765771.
10. Sung JH, Ji JH, Song KS, Lee JH, Choi KH, Lee SH, Yu IJ. Acute inhalation toxicity of silver nanoparticles. Toxicol Ind Health 2011, 27:149-154. 10.1177/0748233710382540, 20870693.
11. Ji JH, Jung JH, Kim SS, Yoon JU, Park JD, Choi BS, Chung YH, Kwon IH, Jeong J, Han BS, Shin JH, Sung JH, Song KS, Yu IJ. Twenty-eight-day inhalation toxicity study of silver nanoparticles in Sprague-Dawley rats. Inhal Toxicol 2007, 19:857-871. 10.1080/08958370701432108, 17687717.
12. Stebounova LV, Adamcakova-Dodd A, Kim JS, Park H, O'Shaughnessy PT, Grassian VH, Thorne PS. Nanosilver induces minimal lung toxicity or inflammation in a subacute murine inhalation model. Part Fibre Toxicol 2011, 8:5. 10.1186/1743-8977-8-5, 21266073.
13. Song KS, Sung JH, Ji JH, Lee JH, Lee JS, Ryu HR, Lee JK, Chung YH, Park HM, Shin BS, Chang HK, Kelman B, Yu IJ. Recovery from silver-nanoparticle-exposure-induced lung inflammation and lung function changes in Sprague Dawley rats. Nanotoxicology 2012, 7:169-180. 10.3109/17435390.2011.648223, 22264098.
14. Sung JH, Ji JH, Yoon JU, Kim DS, Song MY, Jeong J, Han BS, Han JH, Chung YH, Kim J, Kim TS, Chang HK, Lee EJ, Lee JH, Yu IJ. Lung function changes in Sprague-Dawley rats after prolonged inhalation exposure to silver nanoparticles. Inhal Toxicol 2008, 20:567-574. 10.1080/08958370701874671, 18444009.
15. 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. Subchronic inhalation toxicity of silver nanoparticles. Toxicol Sci 2009, 108:452-461. 10.1093/toxsci/kfn246, 19033393.
16. Asgharian B, Price O, Miller F, Subramaniam R, Cassee FR, Freijer J, van Bree L, Winter-Sorkina R. Multiple-Path Particle Dosimetry Model (MPPD v 2.11): A Model for Human and Rat Airway Particle Dosimetry. Hamner Institutes for Health Sciences Applied Research Associates (ARA), National Institute for Public Health and the Environment (RIVM), and Ministry of Housing, Spatial Planning and the Environment, Editor 2009, Applied Research Associates (ARA), Raleigh, North Carolina, USA.
17. Human respiratory tract model for radiological protection. International Commission on Radiological Protection. ICRP Publication 66 1994, 24:1-3.
18. Carvalho TC, Peters JI, Williams RO. Influence of particle size on regional lung deposition-what evidence is there?. Int J Pharm 2011, 406:1-10. 10.1016/j.ijpharm.2010.12.040, 21232585.
19. Cassee FR, Muijser H, Duistermaat E, Freijer JJ, Geerse KB, Marijnissen JC, Arts JH. Particle size-dependent total mass deposition in lungs determines inhalation toxicity of cadmium chloride aerosols in rats. Application of a multiple path dosimetry model. Arch Toxicol 2002, 76:277-286. 10.1007/s00204-002-0344-8, 12107645.
20. Braakhuis HM, Park MV, Gosens I, De Jong WH, Cassee FR. Physicochemical characteristics of nanomaterials that affect pulmonary inflammation. Part Fibre Toxicol 2014, 11:18. 10.1186/1743-8977-11-18, 24725891.
21. Geiser M, Kreyling WG. Deposition and biokinetics of inhaled nanoparticles. Part Fibre Toxicol 2010, 7:2. 10.1186/1743-8977-7-2, 20205860.
22. Oberdorster G. Dosimetric principles for extrapolating results of rat inhalation studies to humans, using an inhaled Ni compound as an example. Health Phys 1989, 57(Suppl 1):213-220. 10.1097/00004032-198907001-00027, 2606684.
23. Oberdorster G, Ferin J, Lehnert BE: Correlation between particle size,in vivoparticle persistence, and lung injury.Environ Health Perspect 1994, 102(Suppl 5):173-179..
24. Geraets L, Oomen AG, Schroeter JD, Coleman VA, Cassee FR. Tissue distribution of inhaled micro- and nano-sized cerium oxide particles in rats: results from a 28-day exposure study. Toxicol Sci 2012, 127:463-473. 10.1093/toxsci/kfs113, 22430073.
25. Phalen RF, Mendez LB, Oldham MJ. New developments in aerosol dosimetry. Inhal Toxicol 2010, 22(Suppl 2):6-14. 10.3109/08958378.2010.516031, 20939685.
26. Oberdorster G, Pott F. Extrapolation from rat studies with environmental tobacco smoke (ETS) to humans: comparison of particle mass deposition and of clearance behavior of ETS compounds. Toxicol Lett 1987, 35:107-112. 10.1016/0378-4274(87)90093-2, 3810670.
27. Oberdorster G, Finkelstein JN, Johnston C, Gelein R, Cox C, Baggs R, Elder AC. Acute pulmonary effects of ultrafine particles in rats and mice. Res Rep Health Eff Inst 2000, 96:5-74. disc 75-86, 11205815.
28. Bakand S, Hayes A, Dechsakulthorn F. Nanoparticles: a review of particle toxicology following inhalation exposure. Inhal Toxicol 2012, 24:125-135. 10.3109/08958378.2010.642021, 22260506.
29. Muhlfeld C, Gehr P, Rothen-Rutishauser B. Translocation and cellular entering mechanisms of nanoparticles in the respiratory tract. Swiss Med Wkly 2008, 138:387-391. 18642134.
30. Geiser M, Casaulta M, Kupferschmid B, Schulz H, Semmler-Behnke M, Kreyling W. The role of macrophages in the clearance of inhaled ultrafine titanium dioxide particles. Am J Respir Cell Mol Biol 2008, 38:371-376. 10.1165/rcmb.2007-0138OC, 17947511.
31. Ma R, Levard C, Marinakos SM, Cheng Y, Liu J, Michel FM, Brown GE, Lowry GV. Size-controlled dissolution of organic-coated silver nanoparticles. Environ Sci Technol 2012, 46:752-759. 10.1021/es201686j, 22142034.
32. Leo BF, Chen S, Kyo Y, Herpoldt KL, Terrill NJ, Dunlop IE, McPhail DS, Shaffer MS, Schwander S, Gow A, Zhang J, Chung KF, Tetley TD, Porter AE, Ryan MP. The stability of silver nanoparticles in a model of pulmonary surfactant. Environ Sci Technol 2013, 47:11232-11240. 10.1021/es403377p, 23988335.
33. Stebounova LV, Guio E, Grassian VH. Silver nanoparticles in simulated biological media: a study of aggregation, sedimentation, and dissolution. J Nanopar Res 2011, 13:12.
34. Kent RD, Vikesland PJ. Controlled evaluation of silver nanoparticle dissolution using atomic force microscopy. Environ Sci Technol 2012, 46:6977-6984. 10.1021/es203475a, 22191460.
35. Zook JM, Long SE, Cleveland D, Geronimo CL, MacCuspie RI. Measuring silver nanoparticle dissolution in complex biological and environmental matrices using UV-visible absorbance. Anal Bioanal Chem 2011, 401:1993-2002. 10.1007/s00216-011-5266-y, 21808990.
36. Pratsinis A, Hervella P, Leroux JC, Pratsinis SE, Sotiriou GA. Toxicity of silver nanoparticles in macrophages. Small 2013, 9:2576-2584. 10.1002/smll.201202120, 23418027.
37. Beer C, Foldbjerg R, Hayashi Y, Sutherland DS, Autrup H. Toxicity of silver nanoparticles - nanoparticle or silver ion?. Toxicol Lett 2012, 208:286-292. 10.1016/j.toxlet.2011.11.002, 22101214.
38. Wang X, Ji Z, Chang CH, Zhang H, Wang M, Liao YP, Lin S, Meng H, Li R, Sun B, Winkle LV, Pinkerton KE, Zink JI, Xia T, Nel AE. Use of coated silver nanoparticles to understand the relationship of particle dissolution and bioavailability to cell and lung toxicological potential. Small 2014, 10:385-398. 10.1002/smll.201301597, 24039004.
39. Singh S, Kumar A, Karakoti A, Seal S, Self WT. Unveiling the mechanism of uptake and sub-cellular distribution of cerium oxide nanoparticles. Mol Biosyst 2010, 6:1813-1820. 10.1039/c0mb00014k, 20697616.
40. Herzog F, Clift MJ, Piccapietra F, Behra R, Schmid O, Petri-Fink A, Rothen-Rutishauser B: Exposure of silver-nanoparticles and silver-ions to lung cellsin vitroat the air-liquid interface.Part Fibre Toxicol 2013, 10:11..
41. Lubick N. Nanosilver toxicity: ions, nanoparticles-or both?. Environ Sci Technol 2008, 42:8617. 10.1021/es8026314, 19192768.
42. Park EJ, Yi J, Kim Y, Choi K, Park K. Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism. Toxicol In Vitro 2010, 24:872-878. 10.1016/j.tiv.2009.12.001, 19969064.
43. Limbach LK, Wick P, Manser P, Grass RN, Bruinink A, Stark WJ. Exposure of engineered nanoparticles to human lung epithelial cells: influence of chemical composition and catalytic activity on oxidative stress. Environ Sci Technol 2007, 41:4158-4163. 10.1021/es062629t, 17612205.
44. Stoeger T, Reinhard C, Takenaka S, Schroeppel A, Karg E, Ritter B, Heyder J, Schulz H. Instillation of six different ultrafine carbon particles indicates a surface area threshold dose for acute lung inflammation in mice. Environ Health Perspect 2006, 114:328-333. 10.1289/ehp.8266, 16507453.
45. Horie M, Fukui H, Endoh S, Maru J, Miyauchi A, Shichiri M, Fujita K, Niki E, Hagihara Y, Yoshida Y, Morimoto Y, Iwahashi H. Comparison of acute oxidative stress on rat lung induced by nano and fine-scale, soluble and insoluble metal oxide particles: NiO and TiO2. Inhal Toxicol 2012, 24:391-400. 10.3109/08958378.2012.682321, 22642288.
46. Duffin R, Tran L, Brown D, Stone V, Donaldson K: Proinflammogenic effects of low-toxicity and metal nanoparticlesin vivoandin vitro: highlighting the role of particle surface area and surface reactivity.Inhal Toxicol 2007, 19:849-856.
47. Kobayashi N, Naya M, Endoh S, Maru J, Yamamoto K, Nakanishi J. Comparative pulmonary toxicity study of nano-TiO(2) particles of different sizes and agglomerations in rats: different short- and long-term post-instillation results. Toxicology 2009, 264:110-118. 10.1016/j.tox.2009.08.002, 19666077.
48. Ho M, Wu KY, Chein HM, Chen LC, Cheng TJ. Pulmonary toxicity of inhaled nanoscale and fine zinc oxide particles: mass and surface area as an exposure metric. Inhal Toxicol 2011, 23:947-956. 10.3109/08958378.2011.629235, 22122307.
49. Zhu MT, Feng WY, Wang B, Wang TC, Gu YQ, Wang M, Wang Y, Ouyang H, Zhao YL, Chai ZF. Comparative study of pulmonary responses to nano- and submicron-sized ferric oxide in rats. Toxicology 2008, 247:102-111. 10.1016/j.tox.2008.02.011, 18394769.
50. Pauluhn J. Pulmonary toxicity and fate of agglomerated 10 and 40 nm aluminum oxyhydroxides following 4-week inhalation exposure of rats: toxic effects are determined by agglomerated, not primary particle size. Toxicol Sci 2009, 109:152-167. 10.1093/toxsci/kfp046, 19251949.
51. Roursgaard M, Poulsen SS, Poulsen LK, Hammer M, Jensen KA, Utsunomiya S, Ewing RC, Balic-Zunic T, Nielsen GD, Larsen ST. Time-response relationship of nano and micro particle induced lung inflammation. Quartz as reference compound. Hum Exp Toxicol 2010, 29:915-933. 10.1177/0960327110363329, 20237177.
52. Gosens I, Mathijssen LE, Bokkers BG, Muijser H, Cassee FR. Comparative hazard identification of nano- and micro-sized cerium oxide particles based on 28-day inhalation studies in rats. Nanotoxicology 2013, 8:643-653. 10.3109/17435390.2013.815814, 23768316.
53. Krystek P, Braakhuis HM, Park MVDZ, Jong WH. Inductively Coupled Plasma-Mass Spectrometry in Biodistribution Studies of (Engineered) Nanoparticles. Encyclopedia of Analytical Chemistry 2013, John Wiley & Sons, Ltd, .
54. Krystek P. A review on approaches to biodistribution studies about gold and silver engineered nanoparticles by inductively couples plasma mass spectrometry. Microchem J 2012, 105:39-43. 10.1016/j.microc.2012.02.008.