Toxicity of Zero- and One-Dimensional Carbon Nanomaterials
Abstract
:1. Introduction
2. In Vitro Cellular Toxicity of Zero- and One-Dimensional Carbon Nanomaterials
3. In Vivo Toxicity of Zero-and One-Dimensional Carbon Nanomaterials
4. Conclusions and Perspectives
Author Contributions
Funding
Conflicts of Interest
References
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Carbon Nanomaterial; Nanoparticle Dimension | Cell Line; Concentrations; Exposure | Toxicity Effects | Reference |
---|---|---|---|
PEI-CQDs; PS = 6.5 ± 2 nm, HD = 56.54 nm | Kidney epithelial cells (African green monkey); 200, 400, 600 and 800 μg/mL; 48 h | PEI-CQDs exhibited toxic effects above concentration 600 μg/mL. | [46] |
CQDs; PS = ~7 nm, HD = 60.3 ± 7 nm | Human bronchial epithelial cells (16HBE); 1, 10, 50, 100 and 200 μg/mL; 24 h | CQDs reduced cell viability inducing oxidative stress. | [47] |
OH-GQDs; PS = 5.6 ± 1.1 nm, HD = 10.3 ± 1.9 nm | Human lung carcinoma cell lines (H1299 and A549); 12.5, 25, 50 and 100 μg/mL; 24 and 48 h | The hydroxylated GQDs induced cell senescence and inhibited Rb phosphorylation in both types of cells at concentration 50 μg/mL. | [50] |
GQDs; PS = ~20 nm | Human breast cancer cells (MCF-7) and human gastric cancer cells (MGC-803); 20, 100, 200 and 400 μg/mL; 24 h | GQDs were found less cytotoxic on both type of cells though the nanoparticles permeated into cytoplasm and nucleus. | [51] |
NDs; PS = 4 –5 nm | Mouse embryonic stem cells; 5 or 100 μg/mL; 24 h | NDs exhibited genotoxicity, expressing an increased level of DNA repair proteins. | [52] |
NDs; HD = 41–103 nm | Human keratinocyte (HaCaT) and human alveolar basal epithelial cells (A549); 0.01, 0.1 and 1.0 mg/mL; 6 and 24 h | NDs were not involved in decreasing cell viability and generating intracellular ROS. However, the nanoparticles inhibited colony formation in cells even at concentration 1.0 mg/mL. | [53] |
NDs; PS = 6–500 nm | Mouse macrophages (RAW 264.7); 0, 10, 50, 100 and 200 μg/mL; 24 h | The results revealed that NDs reduced cell proliferation and metabolic activity in a dose dependent manner. | [54] |
CBNPs; PS = 260 ± 13.7 nm | A549 cells; 0.39 and 0.78 μg/mL; 24 and 48 h | Size dependent cytotoxicity was observed in CBNPs treated cells. Ultrafine CBNPs affected more oxidative stress in cells than fine CBNPs. | [59] |
CBNPs; PS = 14 nm | FE1-Muta mouse lung epithelial cell line; 75 μg/mL; 8 × 72 h | CBNPs caused genetic mutation increasing the quantity of oxidized purines. | [61] |
CBNPs; PS = 14 nm, SSA = 300 m2/g | RAW 264.7 cells; 0.25, 10, 25, 50 and 100 μg/mL; 24, 48 and 72 h | Cytotoxic and genotoxic effects were observed, along with the formation of acentric chromosome fragments at all concentrations. | [63] |
CBNPs; PS = 14 nm | A549 cells; 100 μg/mL; 0.5–24 h | CBNPs induced DNA single-strand breaks at 100 μg/mL at 3 h of post exposure. | [64] |
C60; PS = 0.7 nm | FE1-Muta mouse lung epithelial cells; 100 μg/mL; 576 h | C60 increased the level of oxidized purines significantly without affecting DNA strands. | [66] |
C60; PS = 0.7 nm | A549 cells; 0.02–200 μg/mL; 48 h | C60 treated cells witnessed increased micronuclei frequency depending on dosage. | [67] |
C60(OH)n | Chinese hamster ovary cells (CHO K1); 11–221 μM; 24 h | The nanoparticles treated cells showed decreased micronuclei frequency and chromosome aberration in a dose dependent manner. | [27] |
C60(OH)n; PS = 7.1 ± 2.4 nm | Human umbilical vascular endothelial cells; 1–100 μg/mL; 24 h | The hydroxylated C60 decreased cell viability in a concentration dependent manner. | [69] |
SWCNTs; n/a | Human embryonic kidney cells (HEK293T); 0.78, 1.56, 3.12, 6.25, 12.5, 25, 50, 100, 150 and 200 μg/mL; 0–5 days | SWCNTs decreased cell adhesion and inhibited cell proliferation depending on dose and time. | [70] |
SWCNTs; L = 300–1000 nm, W = 1 nm | Murine 3T3 and human 3T6 fibroblast cells; 1, 5 and 10 μM; 1 h | The nanoparticles had the potential to permeate the cell and exhibited toxicity above 10 µM. | [73] |
SWCNTs; PS = 0.8–2.0 nm | Normal and malignant human mesothelial cells; 12.5, 25 and 125 μg/cm2; 24 h | DNA damage, cell death, and ROS generation were observed in nanoparticles treated cells. | [77] |
SWCNTs; PS = 0.4–1.2 nm, SSA = 1040 m2/g | Chinese hamster lung V79 fibroblasts; 0, 24, 48 and 96 μg/cm2; 3 and 24 h | SWCNTs caused DNA damage in cells at 24 h of post-exposure. | [78] |
MWCNTs; PS = 67 nm, SSA = 26 m2/g | Mouse macrophages (J774.1 and CHO-K1); 10–1000 μg/mL; 16–32 h | MWCNTs treated cells exhibited larger cytotoxicity than crocidolite treated cells. | [79] |
MWCNTs; PS = 100 nm | Human epidermal keratinocytes (HEK) cells; 0.1, 0.2 and 0.4 mg/mL; 1, 2, 4, 8, 12, 24 and 48 h | MWCNTs penetrated the cell membrane and altered the gene expression level of various proteins. | [80] |
MWCNTs; PS = 30 nm | Human skin fibroblasts (HSF42); 0.06, 0.6 and 6 μg/mL; 48 h | MWCNTs caused an increase in apoptosis and necrosis disrupting intracellular signaling pathways, cell metabolism and cellular transport. | [81] |
MWCNTs; L = 1–5 µm, W = 20–40 nm | Human blood T lymphocytes; 10 ng/cell; 0, 24, 48, 72, 96 and 120 h | The oxidized form of MWCNTs exhibited more cytotoxicity than pristine MWCNTs. Both types of nanoparticles induced apoptosis in cells in a time and dose dependent manner. | [82] |
Carbon Nanomaterial; Nanoparticle Dimension | Animal Model; Concentrations; Exposure | Toxicity Effects | Reference |
---|---|---|---|
CQDs; PS ≤ 10 nm, HD = 40 nm, IS = 0.32 nm | Zebrafish; 0, 10, 30, 50, 70, 100 and 200 mg/L; 0, 24, 48, 72, and 96 h Zooplankton; 0, 10, 30, 50, 70, 100 and 200 mg/L; 48 h Phytoplankton; 0, 5, 10, 50, 100, 200 and 500 mg/L; 0, 24, 48, 72, and 96 h | CQDs, at higher dose of 200 mg/L, did not affect swimming and feeding behaviors. CQDs exhibited moderate toxicity to zooplankton, inducing mortality and immobility with EC50 value 97.5 mg/L. CQDs induced oxidative stress and water acidification, inhibited photosynthesis and depleted nutrition absorption in a dose and time dependent manner. It retarded the growth of phytoplankton with EC50 value 74.8 mg/L at 96 h of the study. | [83] |
CQDs; PS = 1–5 nm | Male and female ICR mice; 250, 320, 400 and 500 mg/kg, single dose, intravenous injections; 14 day sMale ICR mice; 100 mg/kg, repeated dose, intravenous injections; 1, 7, 30 and 90 days, once/day | Male mice (LD50 391.62 mg/kg) were found to be more sensitive to the higher doses of the nanoparticles than female mice (LD50 357.77 mg/kg). An acute inflammatory response was observed after seven doses, however the data on the body weight, organ coefficients, blood biochemistry, and organ histopathology suggested that the nanoparticles had low toxicity during the entire experimental period. | [84] |
CQDs; PS = 2–6 nm | Male and female embryos/larvae of rare minnows; 0, 1, 5, 10, 20, 40, and 80 mg/L; 12–96 hpf | In lower dose treated groups (1, 5, 10, and 20 mg/L), no significant developmental defects were observed at the stage of 12 hpf, whereas higher dose treated groups (40 mg/L and 80 mg/L) caused embryos yolk agglutination in a concentration-dependent manner. The noticeable time-dependent deleterious effects were decreased spontaneous movements, higher heart rate, and increased hatching rate. Most of the unhatched embryos died when the exposure time reached 96 hpf. | [9] |
CQDs; PS = 8 ± 2 nm | Male ICR mice; 0, 6, 12 and 24 mg/kg, intraperitoneal injection; 30 days | The histopathological examination showed that no obvious toxic effects were triggered by CQDs on mice. However, NMR metabolomic profiles revealed that CQDs could affect cell membrane, immune system, and normal liver clearance. | [8] |
GQDs; PS = 2.3–6.4 nm, IS = 0.36 nm, height = 0.6–3.5 nm, 1–3 layers | AB strains of wild-type zebrafish embryo/larva; 0, 12.5, 25, 50, 100 and 200 μg/mL; 4–120 hpf | The heart rate of treated animals was found to be decreased with a dose-dependent effect. The exposure of GQDs suggested that they might have little effect during the heart development stage of zebrafish embryos and larvae. | [85] |
GQDs, PS = 3.315 ± 1.74 nm | AB strains of wild-type zebrafish embryo/larva; 0, 12.5, 25, 50, 100, and 200 μg/mL; 4–96 hpf | At low concentrations of GQDs, no significant toxicity was observed. When the concentration was above 50 μg/mL, GQDs disturbed the embryonic development. The hatching rate and heart rate were decrease, accompanied with an increase in mortality. At high concentration of GQDs (200 μg/mL), various embryonic malformations including pericardial edema, vitelline cyst, bent tail, and bent spine occurred. | [86] |
PEG-GQDs; PS = 3–5 nm, height = 0.5–1 nm, 1–2 layers | Female BALB/c mice; 20 mg/kg, intraperitoneal injection, multiple doses; 2 weeks | PEG-GQDs exhibited no-toxicity effects because of nanoparticle encapsulation. | [87] |
COOH-GQDs; PS = 3–6 nm | SD rats; 5 and 10 mg/kg, intravenous injection; 7 doses in 22 days with an interval of 2 days | The studies revealed that the GQDs were distributed in liver, spleen, lung, kidney, and tumor sites after injection, however there was no obvious organ damage at 21 days of post-administration. The serum biochemistry and complete blood count studies revealed that the GQDs did not cause any significant toxicity to the treated animals. | [88] |
NDs; HD = ~120 nm | Wild type young Caenorhabditis elegans; 0.5 mg/mL, microinjection | The NDs were found in the distal gonad and oocytes at 30 min after injection. No detectable toxicity effects were found in brood size and longevity of the treated animal groups. | [89] |
NDs; PS = 4 and 50 nm, IS = 0.202 nm | Male ICR mice; 1.0 mg/kg, intratracheal instillation; 1, 7, 14 and 28 days of post-exposure | At 1 day of post-exposure, both kinds of nanoparticles produced a temporary increase in lung index but there was no trace of lipid peroxidation in lung tissue. During the whole exposure period, the burden of nanoparticle in macrophages was observed and the number of nanoparticles decreased by time in alveolar. | [90] |
NDs; PS = 2–10 nm and 40–100 nm | Male Kun Ming mice; intratracheal instillation; 0.8, 4 and 20 mg/kg; 3 days | A dose-dependent toxicity effect was observed in the lung tissue of mice at 3 days of post-exposure of both kinds of nanoparticles and the higher concentration treated mice (4 and 20 mg/kg) exhibited significant toxicity. | [13] |
NDs-BSA; PS = ~100 nm | Zebrafish (AB strain) embryos/larvae; 1, 2, 5 mg/mL; 4–96 hpf | The different stages of zebrafish embryos exhibited similar development when compared to the control groups at a lower concentration of NDs (1 mg/mL). However, a higher concentration of NDs affected the zebrafish embryos at the Pharyngula stage. The medium concentrated NDs (2 and 5 mg/mL) caused fin curving of zebrafish larvae at the hatching stage. | [14] |
CBNPs; PS = 14 nm | Female C57BL/6J mice, 10 mg/mouse, intratracheal instillation; 21 days | CBNPs did not exert any significant adverse clinical effects. However, the histopathological studies revealed that they decreased lung compliance inducing inflammation when administered along with bleomycin. They augmented the levels of CCL2, TGF-b1, KC, IL-6, and nitrotyrosine in mice on different days of exposure. | [91] |
CBNPs; PS = 14 and 56 nm | Male ICR mice; 50 μg/body, intratracheal instillation; 1, 7 or 14 days | CBNPs of 14 nm aggravated porcine pancreatic elastase mediated pulmonary exposure on emphysematous lung injury at an early stage (day 1) and expressed more interleukin-b and keratinocyte-derived chemoattractant. CBNPs of 56 nm caused inflammation but did not induce porcine pancreatic elastase triggered pathophysiology in the lung. | [92] |
CBNPs; PS = 14 nm, SSA = 295–338 m2/g | Time mated C57BL/6BomTac mice, 42 mg/m3, whole-body inhalation; 1 h/day on gestation days (GD) 8–18 days 11, 54 and 268 μg/animal, intratracheal instillation; 1 h/day, GD 7, 10, 15 and 18 days | The whole-body inhalation induced significant DNA strand breaks in the liver of mothers and their offspring, whereas the intratracheal instillation did not have that effect. However, gestation and lactation were not affected in both ways of administrations. The pulmonary inflammation in time mated mice was similar in both administrations for the medium dose of nanoparticles. | [17] |
CBNPs; PS = 14 nm, SSA = 295–338 m2/g | Female C57BL/6 mice; 162 μg/mouse, intratracheal instillation; 3 h, 1, 2, 3, 4, 5, 14 and 42 days | In the initial days of post-exposure, the worsening of pulmonary homeostasis occurred by the induction of oxidative stress, DNA strand breaks, cell cycle arrest, and cell death. Multiple chronic pulmonary inflammatory processes were the possible effects at the later points of post-exposure days. | [18] |
CBNPs; GMD = 53 ± 1.57 nm | Male C57BL/6 mice; 12.5 μg/m3, nasal inhalation; 4 h/day, 7 days | The histopathology analyses revealed that the inhalation of nanoparticles exacerbated lung inflammation expressing a significant level of interleukin-6, interferon-γ, and fibronectin in lung tissues. | [93] |
PAH-CBNPs; PS = 14.2 ± 0.1 nm, SSA = 115 ± 3 m2/g | Male Wistar rats (strain Crl: WI (Han)); 6 mg/m3, nasal inhalation; 6 h/day, 2 weeks | A significant increase in polymorphonuclear granulocyte numbers was observed for the animals treated with CBNPs and PAH-CBNPs when compared to clean air control on day 1 post-exposure. PAH-CBNPs induced bronchioalveolar hyperplasia, whereas CBNPs caused very slight histological alterations on day 14 post-exposure. When compared to control, only PAH-CBNPs exhibited significant IL-6 mRNA expression and keratinocyte chemoattractant. | [94] |
C60; PS = 33 nm, SSA = 104.6 m2/g | Male Wistar rats; 0.33, 0.66 and 3.3 mg/kg, intratracheal instillation; 3 days, 1 week, 1, 3 and 6 months | No significant increase was observed in total cell count and in the expression of the cytokine-induced neutrophil chemoattractants CINC-1, -2αβ and -3 at a low dose of fullerene treated groups. The higher dose of fullerene treated rat group showed a significant increase in gene expression and total cell counts. | [95] |
Male Wistar rats; 0.12 ± 0.03 mg/m3, whole-body inhalation; 4 weeks, 6 h/day, 5 days/week | There were no significant changes in total cell count in BALF and gene expression of CINC-1, -2αβ and -3 in lung tissue. | ||
C60; GMD = 96 nm, SSA = 0.92 m2/g | Male Wistar rats; 0.12 mg/m3, whole-body inhalation; 4 weeks 6h/day, 5 days/week | Gene expression profiles revealed that the major histocompatibility complex (MHC) mediated immunity and metalloendopeptidase activity were upregulated at 3 days and 1 month of post-exposure. Some upregulated genes were involved in oxidative stress, inflammation, and apoptosis. The nanoparticles were found in alveolar epithelial cells and engulfed by macrophages. | [96] |
C60; HD = 234.1 ± 48.9 nm and 856.5 ± 119.2 nm | gpt delta transgenic mice; 0.2 mg/animal, single dose, intratracheal instillation; 3 hMultiple doses (4 times) | Mutant frequencies were significantly increased (2–3 fold) in the lungs of the nanoparticle treated group when compared to control.There was a slight number of A:T to T:A transversion in C60 treated animals, while no genetic transversion was observed in control groups. | [67] |
C60; PS = 46.7 ± 18.6 nm | ICR male mice; 0.5, 1, 2 mg/kg, intratracheal instillation; 1, 7, 14 and 28 days | Increase in pro-inflammatory cytokines including TNF-α, IL-1 and IL-6 and increase in T-cell distribution were observed in C60 treated mice. The gene expression of MHC class 2 was greater than that of MHC class 1 (H2-T23). | [97] |
C60; HD = 407–5117 nm | Female Fisher 344 rats; single oral intragastric administration; 0.064 and 64 mg/kg; 24 h | Only high dose of fullerene generated oxidative damage by expressing a high level of mRNA 8-oxoguanine DNA glycosylase (8-oxodG) in the lung. | [98] |
C60; n/a | Sprague-Dawley male and female rats; 2000 mg/kg, oral exposure, single dose; 14 days | No acute oral toxicity and no deaths were reported. | [26] |
C60(OH)n | BALB/c female mice; 0.02, 0.2, 2.0, 20 and 200 μg/animal, intratracheal instillation; 24 h | The BAL data indicated that only 200 μg treated mice showed increased neutrophil influx in the lungs causing inflammation, whereas other low concentration treated groups did not present any significant changes. | [99] |
SWCNTs; L ≤ 1 µm, W = 0.9–1.7 nm | Female Fisher 344 rats; 0.064 and 64 mg/Kg, single dose, oral intragastric administration; 24 h | SWCNTs were reported to cause oxidatively damaged DNA in lung and liver by increasing the level of 8-oxodG. | [98] |
SWCNTs; n/a | Male Sprague-Dawley rats; 0.4, 2 and 4 mg/kg, intrapulmonary instillation; 1, 7, 30 and 90 days | Increase in lung granulomatous and inflammatory responses along with fibrosis and collagen deposition was observed in a time and dose-dependent manner for SWCNTs treated groups. | [41] |
SWCNTs; L = 10 nm to several µm, W = 1–2 nm | Male ICR mice; 0.5 mg/kg, intratracheal instillation, single dose; 3 and 14 days | The histological data of SWCNTs treated groups revealed that an increase in macrophage infiltration, foamy-like macrophages formation in the alveolar space, and no significant granuloma formation were observed at 3 days of investigation. Meanwhile, a profound multifocal granuloma was found after 14 days. | [40] |
SWCNTs; n/a | Female C57BL/6 mice; 40 µg/mouse, single dose, intraperitoneal injection; 1 and 7 days | Non-degraded nanotubes treated mice induced inflammation and tissue granulomas, while biodegraded nanotubes treated mice were not induced. | [100] |
SWCNTs; L ≤ 5 µm, W = ~8 nm | SPF male and female Wistar rats; 2 and 10 mg/kg, intratracheal instillation; 5 weeks | High dose exposure of SWCNTs registered increased level of inflammatory markers such as IL-1, IL-6 and TNF-α in BALF than low dose exposure in rat lungs. Transgelin 2 gene expression was also found to be higher in high dose treated rats. | [101] |
SWCNTs; HD = 48.4 nm | Male ICR mice; 25, 50 and 100 μg/kg, intratracheal instillation; after 24 h | The administration of SWCNTs increased the secretion of IL-6 and MCP-1, and the number of total cells including neutrophils, lymphocytes, and eosinophils in the lungs of higher dose-treated mice. | [39] |
SWCNTs; L = ≤1 µm, W = 0.8–1.7 nm | Female C57BL/6J mice; 0.9, 2.8, 8.4 mg/kg, intratracheal instillation, single dose; 1, 3 and 28 days | A dose-dependent increase in Saa3 mRNA expression was observed in the lung. | [102] |
SWCNTs; PS = 1–2 nm, SSA = 1040 m2/g | Female C57BL/6J mice; 40 μg/mouse, pharyngeal aspiration, single dose; 1, 7 and 28 days | The SWCNTs treated vitamin E-deficient mice had shown a greater decrease in pulmonary antioxidants when compared to controls. Acute inflammation and enhanced profibrotic responses were also observed. | [42] |
SWCNTs; L = ≤1 µm, W = 0.8–1.2 nm, SSA = 400–1000 m2/g | Male C57BL/6J mice; 10 μg/mouse, pharyngeal aspiration, single dose; 2 weeks | Both Survanta (natural lung surfactant) dispersed and acetone/sonication dispersed SWCNTs induced lung fibrosis in mice by increasing collagen deposition. | [43] |
MWCNTs; PS = 15–50 nm | Male Wistar rats; 5mg/m3, nasal inhalation; single dose; 4 h, 1, 7, and 14 days | A significant increase in cell count, lactate dehydrogenase, alkaline phosphatase, and cytokines and a decrease in cell viability and alveolar macrophage count were observed in MWCNTs-treated rats in all the investigated days, when compared to control rats. Inflammation, granuloma, and fibrosis were also reported in the lungs of MWCNTs-treated rats on 7 and 14 days of post-exposure. | [32] |
MWCNTs; short (L = 1–5 µm, W = 15 ± 5 nm), intermediate (L = 5–20 µm, W = 15 ± 5 nm), long (L = ~13 µm, W = 40–50 nm) | Female C57Bl/6 mice; 50 mg/mouse, intraperitoneal injection; 1 and 7 days | Size-dependent studies revealed that long sized MWCNTs (mean 13 µm) affected significant inflammation and granuloma in mice at 1 and 7 days of post-operation while short (1–5 µm) and intermediate (5–20 µm) MWCNTs did not cause any significant changes. Furthermore, short MWCNTs were readily involved in phagocytosis while long sized MWCNTs had frustrated phagocytosis. | [103] |
MWCNTs; L = 1.1 ± 2.7 µm, W = 63 ± 1.5 nm | Male Wistar rats; 0.66 and 3.3 mg/kg, intratracheal instillation; 3, 7, 30, 90, and 180 days Male Wistar rats; whole-body inhalation; 6 h/day, 4 weeks | Lung inflammations and CINC-1 expressions were found significantly in high dose treated rats and temporary inflammation was observed in the low dose treated groups. Minimal pulmonary inflammation and a temporary increase in CINC-1 to CINC-3 expressions were found. | [104] |
MWCNTs; L = 5.9 ± 0.05 µm, W = 9.7 ± 2.1 nm, SSA = 378 ± 20 m2/g | Female Sprague–Dawley rats; 0.5 and 2 mg/rat, intratracheal instillation; 0, 28 and 60 days | At 60 days, pulmonary lesions were observed for MWCNTs treated rats owing to collagen-rich granulomas formation protruding in the bronchial lumen. TNF-α was excessively produced in the lungs of treated animals. | [105] |
MWCNTs; n/a | Male guinea pigs; 12.5 mg/pig, intratracheal instillation; 90 days | At 90 days, the MWCNTs exposure caused pneumonitis with mild peribronchiolar fibrosis in pigs, which was not observed in the controls. | [106] |
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Raja, I.S.; Song, S.-J.; Kang, M.S.; Lee, Y.B.; Kim, B.; Hong, S.W.; Jeong, S.J.; Lee, J.-C.; Han, D.-W. Toxicity of Zero- and One-Dimensional Carbon Nanomaterials. Nanomaterials 2019, 9, 1214. https://doi.org/10.3390/nano9091214
Raja IS, Song S-J, Kang MS, Lee YB, Kim B, Hong SW, Jeong SJ, Lee J-C, Han D-W. Toxicity of Zero- and One-Dimensional Carbon Nanomaterials. Nanomaterials. 2019; 9(9):1214. https://doi.org/10.3390/nano9091214
Chicago/Turabian StyleRaja, Iruthayapandi Selestin, Su-Jin Song, Moon Sung Kang, Yu Bin Lee, Bongju Kim, Suck Won Hong, Seung Jo Jeong, Jae-Chang Lee, and Dong-Wook Han. 2019. "Toxicity of Zero- and One-Dimensional Carbon Nanomaterials" Nanomaterials 9, no. 9: 1214. https://doi.org/10.3390/nano9091214