Toxicity of Nanoparticles on The Spleen in Animal Studies: A Scoping Review

  • Dodi Faras Ilmiawan Sutomo Faculty of Medicine, Universitas Islam Indonesia, Sleman, D.I. Yogyakarta
  • Dwi Nur Ahsani Faculty of Medicine, Universitas Islam Indonesia, Sleman, D.I. Yogyakarta
  • Ika Fidianingsih Faculty of Medicine, Universitas Islam Indonesia, Sleman, D.I. Yogyakarta

Abstract

Nanotechnology has been developing in the medical field, but some nanoparticles have toxic effects on the body, including the spleen. This scoping review represents an attempt to take stock of existing research results related to the presence or absence of toxicity to the spleen caused by nanoparticles involving experimental animals. A scoping review was conducted to synthesize and map the toxicity of nanoparticles. It has been searched on PubMed databases for spleen or lien and toxic or toxicity, and nanoparticles or dendrimers or "metal nanoparticles" or “magnetite nanoparticles” or nanoshells or “multifunctional nanoparticles” or nanocapsules or nanoconjugates or nanodiamonds or nanogels or nanospheres. Seventeen studies met our inclusion criteria. In conclusion, it showed that 13 nanoparticles could cause toxicity in rodent spleen and as many as 4 nanoparticles did not cause toxicity in rodent spleen.

References

1. Nasimi P, Haidari M. Medical use of nanoparticles: Drug delivery and diagnosis diseases. Int J Green Nanotechnol. 2013 Jan 1;5(1):1–5.

2. Rizvi SAA, Saleh AM. Applications of nanoparticle systems in drug delivery technology. Saudi Pharm J. 2018 Jan;26(1):64–70.

3. Ibrahim R, Salem MY, Helal OK, Abd El-Monem SN. Effect of titanium dioxide nanoparticles on the spleen of adult male albino rats: Histological and immunohistochemical study. Egypt J Histol. 2018 Sept ;41(3):311–28.

4. Cataldi M, Vigliotti C, Mosca T, Cammarota MR, Capone D. Emerging role of the spleen in the pharmacokinetics of monoclonal antibodies, nanoparticles and exosomes. Int J Mol Sci. 2017 Jun 10;18(1249):1–24.

5. Zhou X, Zhao L, Luo J, Tang H, Xu M, Wang Y, et al. The toxic effects and mechanisms of Nano-Cu on the spleen of rats. Int J Mol Sci. 2019 Mar 22;20(6).

6. Dey A, Manna S, Adhikary J, Chattopadhyay S, De S, Chattopadhyay D, et al. Biodistribution and toxickinetic variances of chemical and green Copper oxide nanoparticles in vitro and in vivo. J Trace Elem Med Biol. 2019 June;55:154–69.
7. Bus JS, Popp JA. Perspectives on the mechanism of action of the splenic toxicity of aniline and structurally-related compounds. Food Chem Toxicol. 1987 Aug 1;25(8):619–26.

8. Petroianu A. Drug-induced splenic enlargement. Expert Opin Drug Saf. 2007 Mar;6(2):199–206.

9. Ratan N. Role of the Spleen in Drug Metabolism [Internet]. [cited 2021 Apr 5]. Available from: https://www.news-medical.net/health/Role-of-the-Spleen-in-Drug-Metabolism.aspx

10. Sukhanova A, Bozrova S, Sokolov P, Berestovoy M, Karaulov A, Nabiev I. Dependence of nanoparticle toxicity on their physical and chemical properties. Nanoscale Res Lett. 2018 Feb 7;13(1):44.

11. Graham UM, Jacobs G, Yokel RA, Davis BH, Dozier AK, Birch ME, et al. From dose to response: In vivo nanoparticle processing and potential toxicity. Adv Exp Med Biol. 2017;947:71-100

12. Hoshyar N, Gray S, Han H, Bao G. The effect of nanoparticle size on in vivo pharmacokinetics and cellular interaction. Nanomedicine (Lond). 2016 Mar;11(6):673-92.

13. Singh M, Harris-Birtill DCC, Markar SR, Hanna GB, Elson DS. Application of gold nanoparticles for gastrointestinal cancer theranostics: A systematic review Nanomedicine. 2015 Nov;11(8):2083-98.

14. Xia Q, Huang J, Feng Q, Chen X, Liu X, Li X, et al. Size- and cell type-dependent cellular
uptake, cytotoxicity and in vivo distribution of gold nanoparticles. Int J Nanomedicine. 2019 August 28;14:6957–70.

15. Lopez-Chaves C, Soto-Alvaredo J, Montes-Bayon M, Bettmer J, Llopis J, Sanchez-Gonzalez C. Gold nanoparticles: Distribution, bioaccumulation and toxicity. In vitro and in vivo studies. Nanomedicine Nanotechnology, Biol Med. 2018 Jan;14(1):1–12.

16. Bailly AL, Correard F, Popov A, Tselikov G, Chaspoul F, Appay R, et al. In vivo evaluation of safety, biodistribution and pharmacokinetics of lasersynthesized gold nanoparticles. Scientific Reports. 2019 Dec 9;9(1):1–12.

17. Khlebtsov N, Dykmana L. Biodistribution and toxicity of engineered gold nanoparticles: A review of in vitro and in vivo studies. Chem Soc Rev. 2011 Feb 22;40(3):1647–71.

18. Carnovale C, Bryant G, Shukla R, Bansal V. Identifying Trends in Gold Nanoparticle Toxicity and Uptake: Size, Shape, Capping Ligand, and Biological Corona. ACS Omega. 2019 Jan 4;4(1):242–56.

19. Lee IC, Ko JW, Park SH, Lim JO, Shin IS, Moon C, et al. Comparative toxicity and biodistribution of copper nanoparticles and cupric ions in rats. Int J Nanomedicine. 2016 Jun 16;11:2883–900.

20. Wang D, Lin Z, Wang T, Yao Z, Qin M, Zheng S, et al. Where does the toxicity of metal oxide nanoparticles come from: The nanoparticles, the ions, or a combination of both? J Hazard Mater. 2016 May 5;308:328–34.
21. Naz S, Gul A, Zia M. Toxicity of copper oxide nanoparticles: a review study. IET Nanobiotechnology. 2020 Feb 24;14(1):1–13.

22. Zhang CH, Wang Y, Sun QQ, Xia LL, Hu JJ, ChengK, et al. Copper nanoparticles show obvious in vitro and in vivo reproductive toxicity via ERK mediated signaling pathway in female mice. Int J Biol Sci. 2018;14(13):1834–44.

23. Feng Q, Liu Y, Huang J, Chen K, Huang J, Xiao K. Uptake, distribution, clearance, and toxicity of iron oxide nanoparticles with different sizes and coatings. Sci Rep. 2018 Jun;8(1):1–13.

24. Pham BTT, Colvin EK, Pham NTH, Kim BJ, Fuller ES, Moon EA, et al. Biodistribution and clearance of stable superparamagnetic maghemite iron oxide nanoparticles in mice following intraperitoneal administration. Int J Mol Sci. 2018 Jan 10;19(1):205.

25. Malhotra N, Ger T-R, Uapipatanakul B, Huang J-C, Chen KH-C, Hsiao C-D. Review of Copper and Copper Nanoparticle Toxicity in Fish. Nanomaterials. 2020 Jun 7;10(6):1126.

26. Rahimi Kalateh Shah Mohammad G, Seyedi SMR, Karimi E, Homayouni‐Tabrizi M. The cytotoxic properties of zinc oxide nanoparticles on the rat liver and spleen, and its anticancer impacts on human liver cancer cell lines. J Biochem Mol Toxicol. 2019 Jul 5;33(7):e22324.

27. Park EJ, Lee GH, Yoon C, Jeong U, Kim Y, Chang J, et al. Tissue distribution following 28 day repeated oral administration of aluminum-based nanoparticles with different properties and the in vitro toxicity. J Appl Toxicol. 2017 Dec;37(12):1408–19.

28. Pandurangan M, Kim DH. In vitro toxicity of zinc oxide nanoparticles: a review. J Nanoparticle Res. 2015 Mar 24;17(3).

29. Savery LC, Viñas R, Nagy AM, Pradeep P, Merrill SJ, Hood AM, et al. Deriving a provisional tolerable intake for intravenous exposure to silver nanoparticles
released from medical devices. Regul Toxicol Pharmacol. 2017 Apr ;85:108–18.
30. Wen H, Dan M, Yang Y, Lyu J, Shao A, Cheng X, et al. Acute toxicity and genotoxicity of silver nanoparticle in rats. Xu B, editor. PLoS One. 2017 Sep 27 ;12(9):e0185554.

31. Arya G, Sharma N, Mankamna R, Nimesh S. Antimicrobial silver nanoparticles: future of
nanomaterials. Nanotechnology in the Life Sciences. 2019. 89–119 p.

32. Ferdous Z, Nemmar A. Health impact of silver nanoparticles: A review of the biodistribution and toxicity following various routes of exposure. International Journal of Molecular Sciences. 2020 Mar 30;21(7):2375.

33. Patra CR, Bhattacharya R, Patra S, Vlahakis NE, Gabashvili A, Koltypin Y, et al.
Pro-angiogenic properties of europium(iii) hydroxide nanorods. Adv Mater. 2008 Feb 18;20(4):753–6.

34. Wei PF, Zhang L, Nethi SK, Barui AK, Lin J, Zhou W, et al. Accelerating the clearance of mutant huntingtin protein aggregates through autophagy induction by europium hydroxide nanorods. Biomaterials. 2014 Jan;35(3):899–907.

35. Patra CR, Abdel Moneim SS, Wang E, Dutta S, Patra S, Eshed M, et al. In vivo toxicity studies of europium hydroxide nanorods in mice. Toxicol Appl Pharmacol. 2009 Nov;240(1):88–98.

36. Bollu VS, Nethi SK, Dasari RK, Rao SSN, Misra S, Patra CR. Evaluation of in vivo cytogenetic toxicity of europium hydroxide nanorods (EHNs) in male and female Swiss albino mice. Nanotoxicology. 2016;10(4):413–25.

37. Labrador-Rached CJ, Browning RT, Braydich- Stolle LK, Comfort KK. Toxicological implications of platinum nanoparticle exposure: stimulation of intracellular stress, inflammatory response, and akt signaling in vitro. J Toxicol. 2018 Oct 1;2018:1367801.

38. Samadi A, Klingberg H, Jauffred L, Kjær A, Bendix PM, Oddershede LB. Platinum nanoparticles: A non-toxic, effective and thermally stable alternative plasmonic material for cancer therapy and bioengineering. Nanoscale. 2018 May 21 ;10(19):9097–107.

39. Almarzoug MHA, Ali D, Alarifi S, Alkahtani S, Alhadheq AM. Platinum nanoparticles induced genotoxicity and apoptotic activity in human normal and cancer hepatic cells via oxidative stress‐mediated Bax/Bcl‐2 and caspase‐3 expression. Environ Toxicol. 2020 Sep 20 ;35(9):930–41.

40. Ksiązyk M, Asztemborska M, Stęborowski R, Bystrzejewska-Piotrowska G. Toxic effect of silver and platinum nanoparticles toward the freshwater microalga Pseudokirchneriella subcapitata. Bull Environ Contam Toxicol. 2015 May 1 ;94(5):554–8.

41. Czubacka E, Czerczak S. Are platinum nanoparticles safe to human health?. Medycyna Pracy. 2019 Jul 16;70(4):487-495.

42. Lin C-X, Gu J-L, Cao J-M.

The acute toxic effects of platinum nanoparticles on ion channels, transmembrane potentials of cardiomyocytes in vitro and heart rhythm in vivo in mice. Int J Nanomedicine. 2019 Jul 22;14:5595–609.

43. Semete B, Booysen LIJ, Kalombo L, Venter JD, Katata L, Ramalapa B, et al. In vivo uptake and acute immune response to orally administered chitosan and PEG coated PLGA nanoparticles. Toxicol Appl Pharmacol. 2010 Dec 1;249(2):158–65.

44. Essa D, Kondiah PPD, Choonara YE, Pillay V. The Design of Poly(lactide-co-glycolide) Nanocarriers for Medical Applications. Frontiers in Bioengineering and Biotechnology. 2020 Feb 11;8:48.

45. Husni P. Potensi polimer poly-lactic-co-glicolyc acid untuk terapi kanker dan perkembangan uji kliniknya biodegradable polymer potential of poly-lactic-coglicolyc
acid for cancer therapy and its clinical trial. J Farm Klin Indones. 2018;7(1):59–68.

46. Singh SP, Kumari M, Kumari SI, Rahman MF, Mahboob M, Grover P. Toxicity assessment of manganese oxide micro and nanoparticles in Wistar rats after 28days of repeated oral exposure. J Appl Toxicol. 2013 Oct;33(10):1165–79.

47. Yousefalizadegan N, Mousavi Z, Rastegar T, Razavi Y, Najafizadeh P. Reproductive toxicity of manganese dioxide in forms of micro-and nanoparticles in male rats. Int J Reprod Biomed. 2019 May 1;17(5):361–70.

48. Samir D, Yousra I, Islam B. Characterization and acute toxicity evaluation of the MgO nanoparticles synthesized from aqueous leaf extract of Ocimum basilicum L. Alger J Biosci. 2020 Sep 21;01(1):1–6.

49. Dumková J, Smutná T, Vrlíková L, Le Coustumer P, Večeřa Z, Dočekal B, et al. Sub-chronic inhalation of lead oxide nanoparticles revealed their broad distribution and tissue-specific subcellular localization in target organs. Part Fibre Toxicol. 2017 Dec 21;14(1):55.

50. Moravec P, Smolik J, Ondráček J, Vodička P, Fajgar R. Lead and/or lead oxide nanoparticle generation for inhalation experiments. Aerosol Sci Technol. 2015 Jun 29;49(8):655–65.

51. Bratovcic A. Synthesis, characterization, applications, and toxicity of lead oxide nanoparticles. In: Lead Chemistry. IntechOpen; 2020 [cited 2021 Apr 3].

52. Poborilova Z, Opatrilova R, Babula P. Toxicity of aluminium oxide nanoparticles demonstrated using a BY-2 plant cell suspension culture model. Environ Exp Bot. 2013 Jul;91:1–11.

53. De A, Ghosh S, Chakrabarti M, Ghosh I, Banerjee R, Mukherjee A. Effect of low-dose exposure of aluminium oxide nanoparticles in Swiss albino mice: Histopathological changes and oxidative damage. Toxicol Ind Health. 2020 Aug 1;36(8):567–79.

54. Smulders S, Ketkar-Atre A, Luyts K, Vriens H, De Sousa Nobre S, Rivard C, et al. Body distribution of SiO2-Fe3O4 core-shell nanoparticles after intravenous injection and intratracheal instillation. Nanotoxicology. 2016;10(5):567–74.

55. Nishimori H, Kondoh M, Isoda K, Tsunoda S ichi, Tsutsumi Y, Yagi K. Histological analysis of 70-nm silica particles-induced chronic toxicity in mice. Eur J Pharm Biopharm. 2009 Aug;72(3):626–9.

56. Tarantini A, Huet S, Jarry G, Lanceleur R, Poul M, Tavares A, et al. Genotoxicity of synthetic amorphous silica nanoparticles in rats following short-term exposure. Part 1: Oral route. Environ Mol Mutagen. 2015 Mar 1;56(2):218–27.

57. Busra A, Eylem S. Toxicity of metal and metal oxide nanoparticles : a review. Environ Chem Lett. 2020;18(5):1659–83.

58. Shahbazi MA, Hamidi M, Mäkilä EM, Zhang H, Almeida P V., Kaasalainen M, et al. The mechanisms of surface chemistry effects of mesoporous silicon nanoparticles on immunotoxicity and biocompatibility. Biomaterials. 2013;34(31):7776–89.

59. Santos HA, Mäkilä E, Airaksinen AJ, Bimbo LM, Hirvonen J. Porous silicon nanoparticles for nanomedicine: Preparation and biomedical applications. Nanomedicine. 2014;9(4):535–54.

60. Mohammed MA, Syeda JTM, Wasan KM, Wasan EK. An overview of chitosan nanoparticles and its application in non-parenteral drug delivery. Pharmaceutics. 2017;9(4).

61. Liu Y, Kong M, Feng C, Yang KK, Li Y, Su J, et al. Biocompatibility, cellular uptake and biodistribution of the polymeric amphiphilic nanoparticles as oral drug carriers. Colloids Surfaces B Biointerfaces. 2013 Mar 1;103:345–53.

62. Quiñones JP, Peniche H, Peniche C. Chitosan Based Self-Assembled Nanoparticles in Drug Delivery. Polymers (Basel). 2018;10(235):1–32.

63. Rizeq BR, Younes NN, Rasool K, Nasrullah GK. Synthesis, bioapplications, and toxicity evaluation of chitosan-based nanoparticles enhanced reader. Int J Mol Sci. 2019;20(5776):1–24.

64. Janer G, Mas del Molino E, Fernández-Rosas E, Fernández A, Vázquez-Campos S. Cell uptake and oral absorption of titanium dioxide nanoparticles. Toxicol Lett. 2014 Jul 15;228(2):103–10.

65. Sang X, Zheng L, Sun Q, Li N, Cui Y, Hu R, et al. The chronic spleen injury of mice following long-term exposure to titanium dioxide nanoparticles. J Biomed Mater Res - Part A. 2012;100 A(4):894–902.

66. Shi H, Magaye R, Castranova V, Zhao J. Titanium dioxide nanoparticles: a review of current toxicological data. Part Fibre Toxicol. 2013 Apr 15;10(15):1–33.

67. International Agency for Research on Cancer (IARC). IARC Publications Website - Carbon Black, Titanium Dioxide, and Talc. [cited 2021 Apr 5].

68. Sagadevan S, Imteyaz S, Murugan B, Anita Lett J, Sridewi N, Weldegebrieal G, Fatimah I, Oh W. A comprehensive review on green synthesis of titanium dioxide nanoparticles and their diverse biomedical applications. Green Processing and Synthesis. 2022 Jan 7;11(1): 44-63.

Published
2022-10-30
How to Cite
SUTOMO, Dodi Faras Ilmiawan; AHSANI, Dwi Nur; FIDIANINGSIH, Ika. Toxicity of Nanoparticles on The Spleen in Animal Studies: A Scoping Review. JURNAL ILMU KEFARMASIAN INDONESIA, [S.l.], v. 20, n. 2, p. 158-168, oct. 2022. ISSN 2614-6495. Available at: <http://jifi.farmasi.univpancasila.ac.id/index.php/jifi/article/view/1082>. Date accessed: 05 nov. 2024. doi: https://doi.org/10.35814/jifi.v20i2.1082.
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