journal article·2015-05Open access

Bioavailability and biodistribution of differently charged polystyrene nanoparticles upon oral exposure in rats

Agata P. Walczak, Peter J. M. Hendriksen, Ruud A. Woutersen, Meike van der Zande, Anna K. Undas, Richard Helsdingen, Hans H. J. van den Berg, Ivonne M. C. M. Rietjens, Hans Bouwmeester

Journal of Nanoparticle Research· Volume 17· Issue 5

Abstract

The likelihood of oral exposure to nanoparticles (NPs) is increasing, and it is necessary to evaluate the oral bioavailability of NPs. In vitro approaches could help reducing animal studies, but validation against in vivo studies is essential. Previously, we assessed the translocation of 50 nm polystyrene NPs of different charges (neutral, positive and negative) using a Caco-2/HT29-MTX in vitro intestinal translocation model. The NPs translocated in a surface charge-dependent manner. The present study aimed to validate this in vitro intestinal model by an in vivo study. For this, rats were orally exposed to a single dose of these polystyrene NPs and the uptake in organs was determined. A negatively charged NP was taken up more than other NPs, with the highest amounts in kidney (37.4 µg/g tissue), heart (52.8 µg/g tissue), stomach wall (98.3 µg/g tissue) and small intestinal wall (94.4 µg/g tissue). This partly confirms our in vitro findings, where the same NPs translocated to the highest extent. The estimated bioavailability of different types of NPs ranged from 0.2 to 1.7 % in vivo, which was much lower than in vitro (1.6-12.3 %). Therefore, the integrated in vitro model cannot be used for a direct prediction of the bioavailability of orally administered NPs. However, the model can be used for prioritizing NPs before further in vivo testing for risk assessment.
Source: openalex_inverted_index · Quality: baseline

Research context

OpenAlex topics: Child Nutrition and Water Access · Pharmaceutical studies and practices · Nanoparticles: synthesis and applications

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (43)

Show source-provided references
1. Araujo L, Lobenberg R, Kreuter J (1999) Influence of the surfactant concentration on the body distribution of nanoparticles. J Drug Target 6:373–38510.3109/10611869908996844 ↗
2. Baek M et al (2012) Pharmacokinetics, tissue distribution, and excretion of zinc oxide nanoparticles. Int J Nanomed 7:3081–3097. doi: 10.2147/Ijn.S32593
3. Bhattacharjee S, Marcelis ATM, Zuilhof H, Woutersen RA, Rietjens IMCM, Alink GM (2013) Role of surface charge in bioavailability and biodistribution of tri-block copolymer nanoparticles in rats after oral exposure. Toxicol Res 2:187–19210.1039/c3tx20072h ↗
4. Bouwmeester H, Brandhoff P, Marvin HJP, Weigel S, Peters RJB (2014) State of the safety assessment and current use of nanomaterials in food and food production. Trends Food Sci Technol 20:1–11. doi: 10.1016/j.tifs.2014.08.00910.3136/fstr.20.1 ↗
5. Chaudhry Q et al (2008) Applications and implications of nanotechnologies for the food sector. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 25:241–258. doi: 10.1080/0265203070174453810.1080/02652030701744538 ↗
6. Cho WS, Kang BC, Lee JK, Jeong J, Che JH, Seok SH (2013) Comparative absorption, distribution, and excretion of titanium dioxide and zinc oxide nanoparticles after repeated oral administration. Part Fibre Toxicol 10:9. doi: 10.1186/1743-8977-10-910.1186/1743-8977-10-9 ↗
7. des Rieux A, Ragnarsson EGE, Gullberg E, Preat V, Schneider YJ, Artursson P (2005) Transport of nanoparticles across an in vitro model of the human intestinal follicle associated epithelium. Eur J Pharm Sci 25:455–465. doi: 10.1016/j.ejps.2005.04.01510.1016/j.ejps.2005.04.015 ↗
8. Durmus-Altun G, Vatansever U, Arzu Vardar S, Altaner S, Dirlik B (2011) Scintigraphic evaluation of small intestinal transit in the streptozotocin induced diabetic rats. Hippokratia 5(3):262–264
9. El-Shabouri MH (2002) Positively charged nanoparticles for improving the oral bioavailability of cyclosporin-A. Int J Pharm 249:101–10810.1016/S0378-5173(02)00461-1 ↗
10. Fabian E, Landsiedel R, Ma-Hock L, Wiench K, Wohlleben W, van Ravenzwaay B (2008) Tissue distribution and toxicity of intravenously administered titanium dioxide nanoparticles in rats. Arch Toxicol 82(3):151–15710.1007/s00204-007-0253-y ↗
11. Fallingborg J, Christensen LA, Ingeman-Nielsen M, Jacobsen BA, Abildgaard K, Rasmussen HH (1989) pH-profile and regional transit times of the normal gut measured by a radiotelemetry device. Aliment Pharmacol Ther 3(6):605–61310.1111/j.1365-2036.1989.tb00254.x ↗
12. Fazlollahi F et al (2011) Polystyrene nanoparticle trafficking across MDCK-II. Nanomedicine 7:588–594. doi: 10.1016/j.nano.2011.01.00810.1016/j.nano.2011.01.008 ↗
13. Florence AT, Hillery AM, Hussain N, Jani PU (1995) Nanoparticles as carriers for oral peptide absorption—studies on particle uptake and fate. J Control Release 36:39–46. doi: 10.1016/0168-3659(95)00059-H10.1016/0168-3659(95)00059-H ↗
14. Genschow E et al (2002) The ECVAM international validation study on in vitro embryotoxicity tests: results of the definitive phase and evaluation of prediction models. European Centre for the Validation of Alternative Methods. Altern Lab Anim (ATLA) 30:151–17610.1177/026119290203000204 ↗
15. Geraets L, Oomen AG, Krystek P, Jacobsen NR, Wallin H, Laurentie M, Verharen HW, Brandon EFA, de Jong WH (2014) Tissue distribution and elimination after oral and intravenous administration of different titanium dioxide nanoparticles in rats. Part Fibre Toxicol 11:3010.1186/1743-8977-11-30 ↗
16. Hartung T, Luechtefeld T, Maertens A, Kleensang A (2013) Integrated testing strategies for safety assessments. Altex 30:3–1810.14573/altex.2013.1.003 ↗
17. Hillery AM, Florence AT (1996) The effect of adsorbed poloxamer 188 and 407 surfactants on the intestinal uptake of 60-nm polystyrene particles after oral administration in the rat. Int J Pharm 132:123–130. doi: 10.1016/0378-5173(95)04353-510.1016/0378-5173(95)04353-5 ↗
18. Hillery AM, Jani PU, Florence AT (1994) Comparative, quantitative study of lymphoid and non-lymphoid uptake of 60 nm polystyrene particles. J Drug Target 2:151–156. doi: 10.3109/1061186940901590410.3109/10611869409015904 ↗
19. Hillyer JF, Albrecht RM (2001) Gastrointestinal persorption and tissue distribution of differently sized colloidal gold nanoparticles. J Pharm Sci 90:1927–1936. doi: 10.1002/Jps.1143.Abs10.1002/jps.1143 ↗
20. Hussain N, Florence AT (1998) Utilizing bacterial mechanisms of epithelial cell entry: invasin-induced oral uptake of latex nanoparticles. Pharm Res 15:153–156. doi: 10.1023/A:101198161084010.1023/A:1011981610840 ↗
21. Hussain N, Jani PU, Florence AT (1997) Enhanced oral uptake of tomato lectin-conjugated nanoparticles in the rat. Pharm Res 14:613–618. doi: 10.1023/A:101215301188410.1023/A:1012153011884 ↗
22. Hussain N, Jaitley V, Florence AT (2001) Recent advances in the understanding of uptake of microparticulates across the gastrointestinal lymphatics. Adv Drug Deliv Rev 50:107–14210.1016/S0169-409X(01)00152-1 ↗
23. Jani P, Halbert GW, Langridge J, Florence AT (1989) The uptake and translocation of latex nanospheres and microspheres after oral administration to rats. J Pharm Pharmacol 41:809–81210.1111/j.2042-7158.1989.tb06377.x ↗
24. Jani P, Halbert GW, Langridge J, Florence AT (1990) Nanoparticle uptake by the rat gastrointestinal mucosa: quantitation and particle size dependency. J Pharm Pharmacol 42:821–82610.1111/j.2042-7158.1990.tb07033.x ↗
25. Jani P, McCarthy DE, Florence AT (1992) Nanosphere and microsphere uptake via Peyer’s patches: observation of the rate of uptake in the rat after a single oral dose. Int J Pharm 86:239–24610.1016/0378-5173(92)90202-D ↗
26. Kandarova H, Letasiova S (2011) Alternative methods in toxicology: pre-validated and validated methods. Interdiscip Toxicol 4:107–113. doi: 10.2478/v10102-011-0018-610.2478/v10102-011-0018-6 ↗
27. Kulkarni SA, Feng SS (2013) Effects of particle size and surface modification on cellular uptake and biodistribution of polymeric nanoparticles for drug delivery. Pharm Res 30:2512–2522. doi: 10.1007/s11095-012-0958-310.1007/s11095-012-0958-3 ↗
28. Lakowicz JR (2007) Principles of fluorescence spectroscopy. Springer, New York. e-ISBN-13 978-0-387-46312-4
29. Lankveld DP, Oomen AG, Krystek P, Neigh A, Troost-de Jong A, Noorlander CW, Van Eijkeren JC, Geertsma RE, De Jong WH (2010) The kinetics of the tissue distribution of silver nanoparticles of different sizes. Biomaterials 31(32):8350–8361. doi: 10.1016/j.biomaterials.2010.07.04510.1016/j.biomaterials.2010.07.045 ↗
30. Lee CM, Jeong HJ, Yun KN, Kim DW, Sohn MH, Lee JK, Jeong J, Lim ST (2012) Optical imaging to trace near infrared fluorescent zinc oxide nanoparticles following oral exposure. Int J Nanomed 7:3203–3209
31. Liu D, Mori A, Huang L (1992) Role of liposome size and RES blockade in controlling biodistribution and tumor uptake of GM1-containing liposomes. Biochim Biophys Acta 1104(1):95–10110.1016/0005-2736(92)90136-A ↗
32. Loeschner K, Navratilova J, Kobler C, Molhave K, Wagner S, von der Kammer F, Larsen EH (2013) Detection and characterization of silver nanoparticles in chicken meat by asymmetric flow field flow fractionation with detection by conventional or single particle ICP-MS. Anal Bioanal Chem 405:8185–819510.1007/s00216-013-7228-z ↗
33. Mahler GJ, Esch MB, Tako E, Southard TL, Archer SD, Glahn RP, Shuler ML (2012) Oral exposure to polystyrene nanoparticles affects iron absorption. Nat Nanotechnol 7:264–271. doi: 10.1038/nnano.2012.310.1038/nnano.2012.3 ↗
34. Martinez-Argudo I, Sands C, Jepson MA (2007) Translocation of enteropathogenic Escherichia coli across an in vitro M cell model is regulated by its type III secretion system. Cell Microbiol 9:1538–1546. doi: 10.1111/j.1462-5822.2007.00891.x10.1111/j.1462-5822.2007.00891.x ↗
35. PEN (2013) The project on emerging nanotechnologies (28 October 2013 edn). http://www.nanotechproject.org/news/archive/9242/
36. Seifert J, Haraszti B, Sass W (1996) The influence of age and particle number on absorption of polystyrene particles from the rat gut. J Anat 189(Pt 3):483–486
37. Szentkuti L (1997) Light microscopical observations on luminally administered dyes, dextrans, nanospheres and microspheres in the pre-epithelial mucus gel layer of the rat distal colon. J Control Release 46:233–242. doi: 10.1016/S0168-3659(96)01600-810.1016/S0168-3659(96)01600-8 ↗
38. van der Zande M 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. doi: 10.1021/nn302649p10.1021/nn302649p ↗
39. Walczak AP et al (2012) Behaviour of silver nanoparticles and silver ions in an in vitro human gastrointestinal digestion model. Nanotoxicology. doi: 10.3109/17435390.2012.726382
40. Walczak AP, Kramer E, Hendriksen PJ, Tromp P, Helsper JP, van der Zande M, Rietjens IM, Bouwmeester H (2014) Translocation of differently sized and charged polystyrene nanoparticles in in vitro intestinal cell models of increasing complexity. Nanotoxicology: 1–9
41. Walczak AP, Kramer E, Hendriksen PJ, Helsdingen R, van der Zande M, Rietjens IMCM, Bouwmeester H (2015) In vitro gastrointestinal digestion increases the translocation of polystyrene nanoparticles in an in vitro intestinal co-culture model. Nanotoxicology (Early Online): 1–9. doi: 10.3109/17435390.2014.98866410.3109/17435390.2014.988664 ↗
42. Worth AP, Balls M (2004) The principles of validation and the ECVAM validation process. Altern Lab Anim (ATLA) 32(Suppl 1B):623–62910.1177/026119290403201s105 ↗
43. Xiao K et al (2011) The effect of surface charge on in vivo biodistribution of PEG-oligocholic acid based micellar nanoparticles. Biomaterials 32:3435–3446. doi: 10.1016/j.biomaterials.2011.01.02110.1016/j.biomaterials.2011.01.021 ↗