Generic placeholder image

Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

General Review Article

Toxicological Aspects of Carbon Nanotubes, Fullerenes and Graphenes

Author(s): Pranav Shah*, Manisha Lalan and Deepti Jani

Volume 27, Issue 4, 2021

Published on: 16 September, 2020

Page: [556 - 564] Pages: 9

DOI: 10.2174/1381612826666200916143741

Price: $65

Abstract

Nanomedicines exhibit unbelievable capability in overcoming the hurdles faced in biological applications. Carbon nanotubes (CNTs), graphene-family nanomaterials and fullerenes are a class of engineered nanoparticles that have emerged as a new option for possible use in drug/gene delivery for life-threatening diseases. Their adaptability to pharmaceutical applications has opened new vistas for biomedical applications. Successful applications of this family of engineered nanoparticles in various fields may not support their use in medicine due to inconsistent data on toxicity as well as the lack of a centralized toxicity database. Inconsistent toxicological studies and lack of mechanistic understanding have been the reasons for limited understanding of their toxicological aspects. These nanoparticles, when underivatized or pristine, are considered as safe, however less reactive. The derivatized forms or functionalization changes their chemistry significantly to modify their biological effects including toxicity. They can cause acute and long term injuries in tissues by penetration through the the blood-air barrier, blood-alveolus barrier, blood-brain barrier, and blood-placenta barrier. and by accumulating in the lung, liver, and spleen . The toxicological effects are manifested through inflammatory response, DNA damage, apoptosis, autophagy and necrosis. Other factors that largely influence the toxicity of carbon nanotubes, graphenes and fullerenes are the concentration, functionalization, dimensional and surface topographical factors. Thus, a better understanding of the toxicity profile of CNTs, graphene-family nanomaterials and fullerenes in humans, animals and the environment is of significant importance, to improve their biological safety, to facilitate their wide biological application and for the successful commercial application. The exploration of appropriate cell lines to investigate specific receptors and intracellular targets as well as chronic toxicity beyond the proof-of-concept is required.

Keywords: Carbon nanotubes, graphenes, fullerenes, toxicity, centralized toxicity database, apoptosis, autophagy.

[1]
Stout DA. Recent advancements in carbon nanofiber and carbon nanotube applications in drug delivery and tissue engineering. Curr Pharm Des 2015; 21(15): 2037-44.
[http://dx.doi.org/10.2174/1381612821666150302153406] [PMID: 25732658]
[2]
Tsukahara T, Haniu H. Cellular cytotoxic response induced by highly purified multi-wall carbon nanotube in human lung cells. Mol Cell Biochem 2011; 352(1-2): 57-63.
[http://dx.doi.org/10.1007/s11010-011-0739-z] [PMID: 21298324]
[3]
Mohanta D, Patnaik S, Sood S, Das N. Carbon nanotubes: Evaluation of toxicity at biointerfaces. J Pharm Anal 2019; 9(5): 293-300.
[http://dx.doi.org/10.1016/j.jpha.2019.04.003] [PMID: 31929938]
[4]
Pacurari M, Yin XJ, Zhao J, et al. Raw single-wall carbon nanotubes induce oxidative stress and activate MAPKs, AP-1, NF-kappaB, and Akt in normal and malignant human mesothelial cells. Environ Health Perspect 2008; 116(9): 1211-7.
[http://dx.doi.org/10.1289/ehp.10924] [PMID: 18795165]
[5]
Shvedova AA, Kisin ER, Porter D, et al. Mechanisms of pulmonary toxicity and medical applications of carbon nanotubes: Two faces of Janus? Pharmacol Ther 2009; 121(2): 192-204.
[http://dx.doi.org/10.1016/j.pharmthera.2008.10.009] [PMID: 19103221]
[6]
Wang L, Luanpitpong S, Castranova V, et al. Carbon nanotubes induce malignant transformation and tumorigenesis of human lung epithelial cells. Nano Lett 2011; 11(7): 2796-803.
[http://dx.doi.org/10.1021/nl2011214] [PMID: 21657258]
[7]
Watts PC, Fearon PK, Hsu WK, Billingham NC, Kroto HW, Walton DR. Carbon nanotubes as polymer antioxidants. J Mater Chem 2003; 13(3): 491-5.
[http://dx.doi.org/10.1039/b211328g]
[8]
Zhu L, Chang DW, Dai L, Hong Y. DNA damage induced by multiwalled carbon nanotubes in mouse embryonic stem cells. Nano Lett 2007; 7(12): 3592-7.
[http://dx.doi.org/10.1021/nl071303v] [PMID: 18044946]
[9]
Porter AE, Gass M, Bendall JS, et al. Uptake of noncytotoxic acid-treated single-walled carbon nanotubes into the cytoplasm of human macrophage cells. ACS Nano 2009; 3(6): 1485-92.
[http://dx.doi.org/10.1021/nn900416z] [PMID: 19459622]
[10]
Rodriguez-Yañez Y, Muñoz B, Albores A. Mechanisms of toxicity by carbon nanotubes. Toxicol Mech Methods 2013; 23(3): 178-95.
[http://dx.doi.org/10.3109/15376516.2012.754534] [PMID: 23193995]
[11]
Ge C, Lao F, Li W, et al. Quantitative analysis of metal impurities in carbon nanotubes: efficacy of different pretreatment protocols for ICPMS spectroscopy. Anal Chem 2008; 80(24): 9426-34.
[http://dx.doi.org/10.1021/ac801469b] [PMID: 18998708]
[12]
Ge C, Li W, Li Y, et al. Significance and systematic analysis of metallic impurities of carbon nanotubes produced by different manufacturers. J Nanosci Nanotechnol 2011; 11(3): 2389-97.
[http://dx.doi.org/10.1166/jnn.2011.3520] [PMID: 21449398]
[13]
Du J, Ge C, Liu Y, et al. The interaction of serum proteins with carbon nanotubes depend on the physicochemical properties of nanotubes. J Nanosci Nanotechnol 2011; 11(11): 10102-10.
[http://dx.doi.org/10.1166/jnn.2011.4976] [PMID: 22413351]
[14]
Entezar-Almahdi E, Morowvat MH. Pharmacokinetic Aspects of Carbon Nanotubes: Improving Outcomes of Functionalization. Curr Nanosci 2019; 15(5): 454-9.
[http://dx.doi.org/10.2174/1573413715666181204113525]
[15]
Wang H, Wang J, Deng X, et al. Biodistribution of carbon single-wall carbon nanotubes in mice. J Nanosci Nanotechnol 2004; 4(8): 1019-24.
[http://dx.doi.org/10.1166/jnn.2004.146] [PMID: 15656196]
[16]
Deng X, Jia G, Wang H, et al. Translocation and fate of multi-walled carbon nanotubes in vivo. Carbon 2007; 45(7): 1419-24.
[http://dx.doi.org/10.1016/j.carbon.2007.03.035]
[17]
Jaurand MC, Renier A, Daubriac J. Mesothelioma: Do asbestos and carbon nanotubes pose the same health risk? Part Fibre Toxicol 2009; 6: 16.
[http://dx.doi.org/10.1186/1743-8977-6-16] [PMID: 19523217]
[18]
Poland CA, Duffin R, Kinloch I, et al. Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat Nanotechnol 2008; 3(7): 423-8.
[http://dx.doi.org/10.1038/nnano.2008.111] [PMID: 18654567]
[19]
Palomäki J, Välimäki E, Sund J, et al. Long, needle-like carbon nanotubes and asbestos activate the NLRP3 inflammasome through a similar mechanism. ACS Nano 2011; 5(9): 6861-70.
[http://dx.doi.org/10.1021/nn200595c] [PMID: 21800904]
[20]
Sato Y, Yokoyama A, Shibata K, et al. Influence of length on cytotoxicity of multi-walled carbon nanotubes against human acute monocytic leukemia cell line THP-1 in vitro and subcutaneous tissue of rats in vivo. Mol Biosyst 2005; 1(2): 176-82.
[http://dx.doi.org/10.1039/b502429c] [PMID: 16880981]
[21]
Yamashita K, Yoshioka Y, Higashisaka K, et al. Carbon nanotubes elicit DNA damage and inflammatory response relative to their size and shape. Inflammation 2010; 33(4): 276-80.
[http://dx.doi.org/10.1007/s10753-010-9182-7] [PMID: 20174859]
[22]
Wick P, Manser P, Limbach LK, et al. The degree and kind of agglomeration affect carbon nanotube cytotoxicity. Toxicol Lett 2007; 168(2): 121-31.
[http://dx.doi.org/10.1016/j.toxlet.2006.08.019] [PMID: 17169512]
[23]
Jia G, Wang H, Yan L, et al. Cytotoxicity of carbon nanomaterials: single-wall nanotube, multi-wall nanotube, and fullerene. Environ Sci Technol 2005; 39(5): 1378-83.
[http://dx.doi.org/10.1021/es048729l] [PMID: 15787380]
[24]
Nagai H, Okazaki Y, Chew SH, et al. Diameter and rigidity of multiwalled carbon nanotubes are critical factors in mesothelial injury and carcinogenesis. Proc Natl Acad Sci USA 2011; 108(49): E1330-8.
[http://dx.doi.org/10.1073/pnas.1110013108] [PMID: 22084097]
[25]
Lam CW, James JT, McCluskey R, Hunter RL. Pulmonary toxicity of single-wall carbon nanotubes in mice 7 and 90 days after intratracheal instillation. Toxicol Sci 2004; 77(1): 126-34.
[http://dx.doi.org/10.1093/toxsci/kfg243] [PMID: 14514958]
[26]
Shvedova AA, Kisin ER, Mercer R, et al. Unusual inflammatory and fibrogenic pulmonary responses to single-walled carbon nanotubes in mice. Am J Physiol Lung Cell Mol Physiol 2005; 289(5): L698-708.
[http://dx.doi.org/10.1152/ajplung.00084.2005] [PMID: 15951334]
[27]
Pauluhn J. Subchronic 13-week inhalation exposure of rats to multiwalled carbon nanotubes: toxic effects are determined by density of agglomerate structures, not fibrillar structures. Toxicol Sci 2010; 113(1): 226-42.
[http://dx.doi.org/10.1093/toxsci/kfp247] [PMID: 19822600]
[28]
Nahle S, Safar R, Grandemange S, et al. Single wall and multiwall carbon nanotubes induce different toxicological responses in rat alveolar macrophages. J Appl Toxicol 2019; 39(5): 764-72.
[http://dx.doi.org/10.1002/jat.3765] [PMID: 30605223]
[29]
Manna SK, Sarkar S, Barr J, et al. Single-walled carbon nanotube induces oxidative stress and activates nuclear transcription factor-kappaB in human keratinocytes. Nano Lett 2005; 5(9): 1676-84.
[http://dx.doi.org/10.1021/nl0507966] [PMID: 16159204]
[30]
Demedts IK, Demoor T, Bracke KR, Joos GF, Brusselle GG. Role of apoptosis in the pathogenesis of COPD and pulmonary emphysema. Respir Res 2006; 7(1): 53.
[http://dx.doi.org/10.1186/1465-9921-7-53] [PMID: 16571143]
[31]
Ravichandran P, Periyakaruppan A, Sadanandan B, et al. Induction of apoptosis in rat lung epithelial cells by multiwalled carbon nanotubes. J Biochem Mol Toxicol 2009; 23(5): 333-44.
[http://dx.doi.org/10.1002/jbt.20296] [PMID: 19827037]
[32]
Toyokuni S. Genotoxicity and carcinogenicity risk of carbon nanotubes. Adv Drug Deliv Rev 2013; 65(15): 2098-110.
[http://dx.doi.org/10.1016/j.addr.2013.05.011] [PMID: 23751780]
[33]
Lindberg HK, Falck GC, Suhonen S, et al. Genotoxicity of nanomaterials: DNA damage and micronuclei induced by carbon nanotubes and graphite nanofibres in human bronchial epithelial cells in vitro. Toxicol Lett 2009; 186(3): 166-73.
[http://dx.doi.org/10.1016/j.toxlet.2008.11.019] [PMID: 19114091]
[34]
Patlolla A, Knighten B, Tchounwou P. Multi-walled carbon nanotubes induce cytotoxicity, genotoxicity and apoptosis in normal human dermal fibroblast cells Ethn Dis 2010; 20(1): 65-72.
[35]
Yang ST, Luo J, Zhou Q, Wang H. Pharmacokinetics, metabolism and toxicity of carbon nanotubes for biomedical purposes. Theranostics 2012; 2(3): 271-82.
[http://dx.doi.org/10.7150/thno.3618] [PMID: 22509195]
[36]
Principi E, Girardello R, Bruno A, et al. Systemic distribution of single-walled carbon nanotubes in a novel model: alteration of biochemical parameters, metabolic functions, liver accumulation, and inflammation in vivo. Int J Nanomedicine 2016; 11: 4299-316.
[http://dx.doi.org/10.2147/IJN.S109950] [PMID: 27621623]
[37]
Awasthi KK, John PJ, Awasthi A, Awasthi K. Multi walled carbon nano tubes induced hepatotoxicity in Swiss albino mice. Micron 2013; 44: 359-64.
[http://dx.doi.org/10.1016/j.micron.2012.08.008] [PMID: 23000350]
[38]
Kagan VE, Kapralov AA, St Croix CM, et al. Lung macrophages “digest” carbon nanotubes using a superoxide/peroxynitrite oxidative pathway. ACS Nano 2014; 8(6): 5610-21.
[http://dx.doi.org/10.1021/nn406484b] [PMID: 24871084]
[39]
Bardi G, Nunes A, Gherardini L, et al. Functionalized carbon nanotubes in the brain: cellular internalization and neuroinflammatory responses. PLoS One 2013; 8(11): e80964.
[http://dx.doi.org/10.1371/journal.pone.0080964] [PMID: 24260521]
[40]
Bussy C, Al-Jamal KT, Boczkowski J, et al. Microglia determine brain region-specific neurotoxic responses to chemically functionalized carbon nanotubes. ACS Nano 2015; 9(8): 7815-30.
[http://dx.doi.org/10.1021/acsnano.5b02358] [PMID: 26043308]
[41]
Kafa H, Wang JT, Rubio N, et al. The interaction of carbon nanotubes with an in vitro blood-brain barrier model and mouse brain in vivo. Biomaterials 2015; 53: 437-52.
[http://dx.doi.org/10.1016/j.biomaterials.2015.02.083] [PMID: 25890741]
[42]
Samiei F, Shirazi FH, Naserzadeh P, Dousti F, Seydi E, Pourahmad J. Correction to: Toxicity of multi-wall carbon nanotubes inhalation on the brain of rats. Environ Sci Pollut Res Int 2020; 27(23): 29699.
[http://dx.doi.org/10.1007/s11356-020-09667-3] [PMID: 32548744]
[43]
van Angelen AA, Glaudemans B, van der Kemp AW, Hoenderop JG, Bindels RJ. Cisplatin-induced injury of the renal distal convoluted tubule is associated with hypomagnesaemia in mice. Nephrol Dial Transplant 2013; 28(4): 879-89.
[http://dx.doi.org/10.1093/ndt/gfs499] [PMID: 23136218]
[44]
Cui D, Tian F, Ozkan CS, Wang M, Gao H. Effect of single wall carbon nanotubes on human HEK293 cells. Toxicol Lett 2005; 155(1): 73-85.
[http://dx.doi.org/10.1016/j.toxlet.2004.08.015] [PMID: 15585362]
[45]
Garibaldi S, Brunelli C, Bavastrello V, Ghigliotti G, Nicolini C. Carbon nanotube biocompatibility with cardiac muscle cells. Nanotechnology 2005; 17(2): 391.
[http://dx.doi.org/10.1088/0957-4484/17/2/008]
[46]
Joviano-Santos JV, Sá MA, Maria ML, et al. Evaluation of cardiovascular toxicity of carbon nanotubes functionalized with sodium hyaluronate in oral regenerative medicine. Braz J Med Biol Res 2014; 47(7): 560-6.
[http://dx.doi.org/10.1590/1414-431X20143894] [PMID: 24863649]
[47]
Hosseinpour M, Azimirad V, Alimohammadi M, Shahabi P, Sadighi M, Ghamkhari Nejad G. The cardiac effects of carbon nanotubes in rat. Bioimpacts 2016; 6(2): 79-84.
[http://dx.doi.org/10.15171/bi.2016.11] [PMID: 27525224]
[48]
Seaton A, Tran L, Aitken R, Donaldson K. Nanoparticles, human health hazard and regulation. J R Soc Interface 2010; 7(Suppl. 1): S119-29.
[http://dx.doi.org/10.1098/rsif.2009.0252.focus] [PMID: 19726441]
[49]
Ibrahim J, Berk BC, Hughes AD. Comparison of simultaneous measurements of blood pressure by tail-cuff and carotid arterial methods in conscious spontaneously hypertensive and Wistar-Kyoto rats. Clin Exp Hypertens 2006; 28(1): 57-72.
[http://dx.doi.org/10.1080/10641960500386817] [PMID: 16443565]
[50]
Deng X, Wu F, Liu Z, et al. The splenic toxicity of water soluble multi-walled carbon nanotubes in mice. Carbon 2009; 47(6): 1421-8.
[http://dx.doi.org/10.1016/j.carbon.2008.12.032]
[51]
Mehra NK, Cai D, Kuo L, Hein T, Palakurthi S. Safety and toxicity of nanomaterials for ocular drug delivery applications. Nanotoxicology 2016; 10(7): 836-60.
[http://dx.doi.org/10.3109/17435390.2016.1153165] [PMID: 27027670]
[52]
Ema M, Matsuda A, Kobayashi N, Naya M, Nakanishi J. Evaluation of dermal and eye irritation and skin sensitization due to carbon nanotubes. Regul Toxicol Pharmacol 2011; 61(3): 276-81.
[http://dx.doi.org/10.1016/j.yrtph.2011.08.007] [PMID: 21893152]
[53]
Koyama S, Endo M, Kim YA, et al. Role of systemic T-cells and histopathological aspects after subcutaneous implantation of various carbon nanotubes in mice. Carbon 2006; 44(6): 1079-92.
[http://dx.doi.org/10.1016/j.carbon.2005.08.006]
[54]
Murray AR, Kisin E, Leonard SS, et al. Oxidative stress and inflammatory response in dermal toxicity of single-walled carbon nanotubes. Toxicology 2009; 257(3): 161-71.
[http://dx.doi.org/10.1016/j.tox.2008.12.023] [PMID: 19150385]
[55]
Witzmann FA, Monteiro-Riviere NA. Multi-walled carbon nanotube exposure alters protein expression in human keratinocytes. Nanomedicine (Lond) 2006; 2(3): 158-68.
[http://dx.doi.org/10.1016/j.nano.2006.07.005] [PMID: 17292138]
[56]
Zhang LW, Zeng L, Barron AR, Monteiro-Riviere NA. Biological interactions of functionalized single-wall carbon nanotubes in human epidermal keratinocytes. Int J Toxicol 2007; 26(2): 103-13.
[http://dx.doi.org/10.1080/10915810701225133] [PMID: 17454250]
[57]
Zhang Y, Wang B, Meng X, Sun G, Gao C. Influences of acid-treated multiwalled carbon nanotubes on fibroblasts: proliferation, adhesion, migration, and wound healing. Ann Biomed Eng 2011; 39(1): 414-26.
[http://dx.doi.org/10.1007/s10439-010-0151-y] [PMID: 20824344]
[58]
Pietroiusti A, Campagnolo L, Fadeel B. Interactions of engineered nanoparticles with organs protected by internal biological barriers. Small 2013; 9(9-10): 1557-72.
[http://dx.doi.org/10.1002/smll.201201463] [PMID: 23097249]
[59]
Pietroiusti A, Massimiani M, Fenoglio I, et al. Low doses of pristine and oxidized single-wall carbon nanotubes affect mammalian embryonic development. ACS Nano 2011; 5(6): 4624-33.
[http://dx.doi.org/10.1021/nn200372g] [PMID: 21615177]
[60]
Zhang T, Tang M, Zhang S, et al. Systemic and immunotoxicity of pristine and PEGylated multi-walled carbon nanotubes in an intravenous 28 days repeated dose toxicity study. Int J Nanomedicine 2017; 12: 1539-54.
[http://dx.doi.org/10.2147/IJN.S123345] [PMID: 28280324]
[61]
Sargent LM, Porter DW, Staska LM, et al. Promotion of lung adenocarcinoma following inhalation exposure to multi-walled carbon nanotubes. Part Fibre Toxicol 2014; 11: 3.
[http://dx.doi.org/10.1186/1743-8977-11-3] [PMID: 24405760]
[62]
Kroto H, Heath J, O’Brien S, Curl R, Smalley R. C60: Buckminsterfullerene. Nature 1985; 318: 162-3.
[http://dx.doi.org/10.1038/318162a0]
[63]
Aschberger K, Johnston HJ, Stone V, et al. Review of fullerene toxicity and exposure--appraisal of a human health risk assessment, based on open literature. Regul Toxicol Pharmacol 2010; 58(3): 455-73.
[http://dx.doi.org/10.1016/j.yrtph.2010.08.017] [PMID: 20800639]
[64]
Johnston HJ, Hutchison GR, Christensen FM, Aschberger K, Stone V. The biological mechanisms and physicochemical characteristics responsible for driving fullerene toxicity. Toxicol Sci 2010; 114(2): 162-82.
[http://dx.doi.org/10.1093/toxsci/kfp265] [PMID: 19901017]
[65]
Nielsen GD, Roursgaard M, Jensen KA, Poulsen SS, Larsen ST. in vivo biology and toxicology of fullerenes and their derivatives. Basic Clin Pharmacol Toxicol 2008; 103(3): 197-208.
[http://dx.doi.org/10.1111/j.1742-7843.2008.00266.x] [PMID: 18684229]
[66]
Giełdoń A, Witt M, Gajewicz A, Puzyn T. Rapid insight into C60 influence on biological functions of proteins. Struct Chem 2017; 28(6): 1775-88.
[http://dx.doi.org/10.1007/s11224-017-0957-4]
[67]
Prylutska S, Grebinyk A, Lynchak V, et al. in vitro and in vivo toxicity of pristine C60 fullerene aqueous colloid solution. Fuller Nanotub Carbon Nanostruct 2019; 27(9): 715-28.
[http://dx.doi.org/10.1080/1536383X.2019.1634055]
[68]
Yamago S, Tokuyama H, Nakamura E, et al. in vivo biological behavior of a water-miscible fullerene: 14C labeling, absorption, distribution, excretion and acute toxicity. Chem Biol 1995; 2(6): 385-9.
[http://dx.doi.org/10.1016/1074-5521(95)90219-8] [PMID: 9383440]
[69]
Baker GL, Gupta A, Clark ML, et al. Inhalation toxicity and lung toxicokinetics of C60 fullerene nanoparticles and microparticles. Toxicol Sci 2008; 101(1): 122-31.
[http://dx.doi.org/10.1093/toxsci/kfm243] [PMID: 17878152]
[70]
Kuznietsova H, Dziubenko N, Hurmach V, et al. Water-Soluble Pristine C60 Fullerenes Inhibit Liver Fibrotic Alteration and Prevent Liver Cirrhosis in Rats. Oxid Med Cell Longev 2020; 2020: 8061246.
[http://dx.doi.org/10.1155/2020/8061246] [PMID: 32148657]
[71]
Gharbi N, Pressac M, Hadchouel M, Szwarc H, Wilson SR, Moussa F. [60]fullerene is a powerful antioxidant in vivo with no acute or subacute toxicity. Nano Lett 2005; 5(12): 2578-85.
[http://dx.doi.org/10.1021/nl051866b] [PMID: 16351219]
[72]
Chen HH, Yu C, Ueng TH, et al. Acute and subacute toxicity study of water-soluble polyalkylsulfonated C60 in rats. Toxicol Pathol 1998; 26(1): 143-51.
[http://dx.doi.org/10.1177/019262339802600117] [PMID: 9502397]
[73]
Scrivens WA, Tour JM, Creek KE, Pirisi L. Synthesis of 14C-labeled C60, its suspension in water, and its uptake by human keratinocytes. J Am Chem Soc 1994; 116(10): 4517-8.
[http://dx.doi.org/10.1021/ja00089a067]
[74]
Sayes CM, Fortner JD, Guo W, et al. The differential cytotoxicity of water-soluble fullerenes. Nano Lett 2004; 4(10): 1881-7.
[http://dx.doi.org/10.1021/nl0489586]
[75]
Dhawan A, Taurozzi JS, Pandey AK, et al. Stable colloidal dispersions of C60 fullerenes in water: evidence for genotoxicity. Environ Sci Technol 2006; 40(23): 7394-401.
[http://dx.doi.org/10.1021/es0609708] [PMID: 17180994]
[76]
Sera N, Tokiwa H, Miyata N. Mutagenicity of the fullerene C60-generated singlet oxygen dependent formation of lipid peroxides. Carcinogenesis 1996; 17(10): 2163-9.
[http://dx.doi.org/10.1093/carcin/17.10.2163] [PMID: 8895484]
[77]
Sanchez VC, Jachak A, Hurt RH, Kane AB. Biological interactions of graphene-family nanomaterials: an interdisciplinary review. Chem Res Toxicol 2012; 25(1): 15-34.
[http://dx.doi.org/10.1021/tx200339h] [PMID: 21954945]
[78]
Bitounis D, Ali-Boucetta H, Hong BH, Min DH, Kostarelos K. Prospects and challenges of graphene in biomedical applications. Adv Mater 2013; 25(16): 2258-68.
[http://dx.doi.org/10.1002/adma.201203700] [PMID: 23494834]
[79]
Xiaoli F, Qiyue C, Weihong G, et al. Toxicology data of graphene-family nanomaterials: an update. Arch Toxicol 2020; 94(6): 1915-39.
[http://dx.doi.org/10.1007/s00204-020-02717-2] [PMID: 32240330]
[80]
Lalwani G, D'Agati M, Khan AM, Sitharaman B. Toxicology of graphene-based nanomaterials Adv Drug Delivery Rev 2016; 105(Pt. B): 109-44.
[http://dx.doi.org/10.1016/j.addr.2016.04.028]
[81]
Ou L, Song B, Liang H, et al. Toxicity of graphene-family nanoparticles: a general review of the origins and mechanisms. Part Fibre Toxicol 2016; 13(1): 57.
[http://dx.doi.org/10.1186/s12989-016-0168-y] [PMID: 27799056]
[82]
Seabra AB, Paula AJ, de Lima R, Alves OL, Durán N. Nanotoxicity of graphene and graphene oxide. Chem Res Toxicol 2014; 27(2): 159-68.
[http://dx.doi.org/10.1021/tx400385x] [PMID: 24422439]
[83]
Volkov Y, McIntyre J, Prina-Mello A. Graphene toxicity as a double-edged sword of risks and exploitable opportunities: a critical analysis of the most recent trends and developments 2D Mater 2017; 4(2): 022001.
[84]
Gies V, Zou S. Systematic toxicity investigation of graphene oxide: evaluation of assay selection, cell type, exposure period and flake size. Toxicol Res (Camb) 2017; 7(1): 93-101.
[http://dx.doi.org/10.1039/C7TX00278E] [PMID: 30090566]
[85]
Mao L, Hu M, Pan B, Xie Y, Petersen EJ. Biodistribution and toxicity of radio-labeled few layer graphene in mice after intratracheal instillation. Part Fibre Toxicol 2016; 13: 7.
[http://dx.doi.org/10.1186/s12989-016-0120-1] [PMID: 26864058]
[86]
Yang K, Gong H, Shi X, Wan J, Zhang Y, Liu Z. in vivo biodistribution and toxicology of functionalized nano-graphene oxide in mice after oral and intraperitoneal administration. Biomaterials 2013; 34(11): 2787-95.
[http://dx.doi.org/10.1016/j.biomaterials.2013.01.001] [PMID: 23340196]
[87]
Sawosz E, Jaworski S, Kutwin M, et al. Toxicity of pristine graphene in experiments in a chicken embryo model. Int J Nanomedicine 2014; 9: 3913-22.
[PMID: 25152621]
[88]
Fadeel B, Bussy C, Merino S, et al. Safety assessment of graphene-based materials: focus on human health and the environment. ACS Nano 2018; 12(11): 10582-620.
[http://dx.doi.org/10.1021/acsnano.8b04758] [PMID: 30387986]
[89]
Bastús NG, Puntes V. Nanosafety: Towards Safer Nanoparticles by Design. Curr Med Chem 2018; 25(35): 4587-601.
[http://dx.doi.org/10.2174/0929867324666170413124915] [PMID: 28412902]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy