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Individual and combined toxicity of carboxylic acid functionalized multi-walled carbon nanotubes and benzo a pyrene in lung adenocarcinoma cells

  • Mansour Rezazadeh Azari
  • Yousef MohammadianEmail author
  • Jalal Pourahmad
  • Fariba Khodagholi
  • Habibollah Peirovi
  • Yadollah Mehrabi
  • Meisam Omidi
  • Athena Rafieepour
Research Article
  • 35 Downloads

Abstract

Co-exposure to carboxylic acid functionalized multi-walled carbon nanotubes (F-MWCNTs) and polycyclic aromatic hydrocarbons (PAHs) such as benzo a pyrene (BaP) in ambient air have been reported. Adsorption of BaP to F-MWCNTs can influence combined toxicity. Studying individual toxicity of F-MWCNTs and BaP might give unrealistic data. Limited information is available on the combined toxicity of F-MWCNTs and BaP in human cells. The objective of the present work is to evaluate the toxicity of F-MWCNTs and BaP individually and combined in human lung adenocarcinoma (A549 cells). The in vitro toxicity is evaluated through cell viability, the production of reactive oxygen species (ROS), apoptosis, and the production of 8-OHdG assays. Adsorption of BaP to F-MWCNTs was confirmed using a spectrophotometer. The results indicated that the F-MWCNTs and BaP reduce cell viability individually and produce ROS, apoptosis, and 8-OHdG in exposed cells. Stress oxidative is found to be a mechanism of cytotoxicity for both F-MWCNTs and BaP. Combined exposure to F-MWCNTs and BaP decreases cytotoxicity compared to individual exposure, but the difference is not statistically significant in all toxicity assays; hence, the two-factorial analysis indicated an additive toxic interaction. Adsorption of BaP to F-MWCNTs could mitigate the bioavailability and toxicity of BaP in biological systems. Considering the mixture toxicity of MWCNTs and BaP is required for risk assessment of ambient air contaminants.

Keywords

Functionalized multi-walled carbon nanotubes Benzo a pyrene Combined toxicity A549 cells 

Notes

Acknowledgments

The present study was carried out as partial fulfillment of a Ph.D. thesis at the Shahid Beheshti University of Medical Sciences, and authors thank the School of Public Health and safety of the Shahid Beheshti University of Medical Sciences for their moral support. We would also like to express our gratitude to Professor Motamedi and Professor Ahmadiani from the Neuroscience Research Center of Shahid Beheshti University of Medical Sciences for their cooperation with this project.

Funding information

The present study was financially supported by the School of Public Health of the Shahid Beheshti University of Medical Sciences.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abdalla S, Al-Marzouki F, Al-Ghamdi AA, Abdel-Daiem A (2015) Different technical applications of carbon nanotubes. Nanoscale Res Lett 10:358CrossRefGoogle Scholar
  2. Allegri M, Perivoliotis DK, Bianchi MG, Chiu M, Pagliaro A, Koklioti MA, Trompeta A-FA, Bergamaschi E, Bussolati O, Charitidis CA (2016) Toxicity determinants of multi-walled carbon nanotubes: the relationship between functionalization and agglomeration. Toxicol Rep 3:230–243CrossRefGoogle Scholar
  3. Armstrong B, Hutchinson E, Unwin J, Fletcher T (2004) Lung cancer risk after exposure to polycyclic aromatic hydrocarbons: a review and meta-analysis. Environ Health Perspect 112:970–978CrossRefGoogle Scholar
  4. Asweto CO, Wu J, Hu H, Feng L, Yang X, Duan J, Sun Z (2017) Combined effect of silica nanoparticles and benzo [a] pyrene on cell cycle arrest induction and apoptosis in human umbilical vein endothelial cells. Int J Environ Res Public Health 14:289CrossRefGoogle Scholar
  5. Azizi M, Ghourchian H, Yazdian F, Dashtestani F, AlizadehZeinabad H (2017) Cytotoxic effect of albumin coated copper nanoparticle on human breast cancer cells of MDA-MB 231. PLoS One 12:e0188639CrossRefGoogle Scholar
  6. Balasubramanian K, Burghard M (2005) Chemically functionalized carbon nanotubes. Small 1:180–192CrossRefGoogle Scholar
  7. Bianco A, Kostarelos K, Partidos CD, Prato M (2005) Biomedical applications of functionalised carbon nanotubes. Chem Commun 571-577Google Scholar
  8. Birch ME, Ku B-K, Evans DE, Ruda-Eberenz TA (2011) Exposure and emissions monitoring during carbon nanofiber production—part I: elemental carbon and iron–soot aerosols. Ann Occup Hyg 55:1016–1036Google Scholar
  9. Birch ME, Ruda-Eberenz TA, Chai M, Andrews R, Hatfield RL (2013) Properties that influence the specific surface areas of carbon nanotubes and nanofibers. Ann Occup Hyg 57:1148–1166Google Scholar
  10. Bo C, Ying L, Song WM, Hayashi Y, Ding XC, Li WH (2011) In vitro evaluation of cytotoxicity and oxidative stress induced by multiwalled carbon nanotubes in murine RAW 264.7 macrophages and human A549 lung cells. Biomed Environ Sci 24:593–601Google Scholar
  11. Bosetti C, Boffetta P, La Vecchia C (2006) Occupational exposures to polycyclic aromatic hydrocarbons, and respiratory and urinary tract cancers: a quantitative review to 2005. Ann Oncol 18:431–446CrossRefGoogle Scholar
  12. Campos-Garcia J, Martinez DST, Alves OL, Leonardo AFG, Barbieri E (2015) Ecotoxicological effects of carbofuran and oxidised multiwalled carbon nanotubes on the freshwater fish Nile tilapia: nanotubes enhance pesticide ecotoxicity. Ecotoxicol Environ Saf 111:131–137CrossRefGoogle Scholar
  13. Chatterjee N, Yang J, Kim H-M, Jo E, Kim P-J, Choi K, Choi J (2014) Potential toxicity of differential functionalized multiwalled carbon nanotubes (MWCNT) in human cell line (BEAS2B) and Caenorhabditis elegans. J Toxic Environ Health A 77:1399–1408CrossRefGoogle Scholar
  14. Chin BY, Choi ME, Burdick MD, Strieter RM, Risby TH, Choi AM (1998) Induction of apoptosis by particulate matter: role of TNF-α and MAPK. Am J Phys Lung Cell Mol Phys 275:L942–L949Google Scholar
  15. de la Gala Morales M, Holgado FR, Marín MRP, Blázquez LC, Gil EP (2015) Ambient air levels and health risk assessment of benzo (a) pyrene in atmospheric particulate matter samples from low-polluted areas: application of an optimized microwave extraction and HPLC-FL methodology. Environ Sci Pollut Res 22:5340–5349CrossRefGoogle Scholar
  16. De Volder MF, Tawfick SH, Baughman RH, Hart AJ (2013) Carbon nanotubes: present and future commercial applications. Science 339:535–539CrossRefGoogle Scholar
  17. Deng R, Lin D, Zhu L, Majumdar S, White JC, Gardea-Torresdey JL, Xing B (2017) Nanoparticle interactions with co-existing contaminants: joint toxicity, bioaccumulation and risk. Nanotoxicology 11:591–612CrossRefGoogle Scholar
  18. Dhasmana A, Jamal QMS, Mir SS, Bhatt MLB, Rahman Q, Gupta R, Siddiqui MH, Lohani M (2014) Titanium dioxide nanoparticles as guardian against environmental carcinogen benzo[alpha]pyrene. PLoS One 9(9):e107068.  https://doi.org/10.1371/journal.pone.0107068
  19. Dong X, Liu L, Zhu D, Zhang H, Li Y, Leng X (2015) Effects of carboxylated multiwalled carbon nanotubes on the function of macrophages. J Nanomater 2015:4Google Scholar
  20. Ercegovac M, Jovic N, Simic T, Beslac-Bumbasirevic L, Sokic D, Djukic T, Savic-Radojevic A, Matic M, Mimic-Oka J, Pljesa-Ercegovac M (2010) Byproducts of protein, lipid and DNA oxidative damage and antioxidant enzyme activities in seizure. Seizure-European Journal of Epilepsy 19:205–210CrossRefGoogle Scholar
  21. Francis AP, Devasena T (2018) Toxicity of carbon nanotubes: a review. Toxicol Ind Health 34:200–210CrossRefGoogle Scholar
  22. Girardello R, Baranzini N, Tettamanti G, de Eguileor M, Grimaldi A (2017) Cellular responses induced by multi-walled carbon nanotubes: in vivo and in vitro studies on the medicinal leech macrophages. Sci Rep 7:8871CrossRefGoogle Scholar
  23. Glomstad B, Altin D, Sørensen L, Liu J, Jenssen BM, Booth AM (2016) Carbon nanotube properties influence adsorption of phenanthrene and subsequent bioavailability and toxicity to Pseudokirchneriella subcapitata. Environ Sci Technol 50:2660–2668CrossRefGoogle Scholar
  24. Gorrochategui E, Li J, Fullwood NJ, Ying G-G, Tian M, Cui L, Shen H, Lacorte S, Tauler R, Martin FL (2016) Diet-sourced carbon-based nanoparticles induce lipid alterations in tissues of zebrafish (Danio rerio) with genomic hypermethylation changes in brain. Mutagenesis 32:91–103CrossRefGoogle Scholar
  25. Guerreiro C, Horálek J, De Leeuw F, Couvidat F (2016) Benzo (a) pyrene in Europe: ambient air concentrations, population exposure and health effects. Environ Pollut 214:657–667CrossRefGoogle Scholar
  26. Han JH, Lee EJ, Lee JH, So KP, Lee YH, Bae GN, Lee S-B, Ji JH, Cho MH, Yu IJ (2008) Monitoring multiwalled carbon nanotube exposure in carbon nanotube research facility. Inhal Toxicol 20:741–749CrossRefGoogle Scholar
  27. Happo MS, Sippula O, Jalava PI, Rintala H, Leskinen A, Komppula M, Kuuspalo K, Mikkonen S, Lehtinen K, Jokiniemi J (2014) Role of microbial and chemical composition in toxicological properties of indoor and outdoor air particulate matter. Part Fibre Toxicol 11:60CrossRefGoogle Scholar
  28. Harper S, Wohlleben W, Doa M, Nowack B, Clancy S, Canady R, Maynard A (2015) Measuring nanomaterial release from carbon nanotube composites: review of the state of the science, Journal of Physics: Conference Series. IOP Publishing, pp 012026Google Scholar
  29. Hassan A, Alam S, Abdel-Aziem S, Ahmed K (2011) Benzo-a-pyrene induced genotoxicity and cytotoxicity in germ cells of mice: intervention of radish and cress. J Genet Eng Biotechnol 9:65–72CrossRefGoogle Scholar
  30. Jang M-H, Hwang YS (2018) Effects of functionalized multi-walled carbon nanotubes on toxicity and bioaccumulation of lead in Daphnia magna. PLoS One 13:e0194935CrossRefGoogle Scholar
  31. Jensen K, Kembouche Y, Christiansen E, Jacobsen N, Wallin H, Guiot C, Spalla O, Witschger O (2011) Final protocol for producing suitable manufactured nanomaterial exposure media. NANOGENOTOX deliverable report n 3Google Scholar
  32. Ji K, Xing C, Jiang F, Wang X, Guo H, Nan J, Qian L, Yang P, Lin J, Li M (2013) Benzo [a] pyrene induces oxidative stress and endothelial progenitor cell dysfunction via the activation of the NF-κB pathway. Int J Mol Med 31:922–930CrossRefGoogle Scholar
  33. Jung HS, Miller A, Park K, Kittelson DB (2013) Carbon nanotubes among diesel exhaust particles: real samples or contaminants? J Air Waste Manage Assoc 63:1199–1204CrossRefGoogle Scholar
  34. Kah M, Zhang X, Jonker MT, Hofmann T (2011) Measuring and modeling adsorption of PAHs to carbon nanotubes over a six order of magnitude wide concentration range. Environ Sci Technol 45:6011–6017CrossRefGoogle Scholar
  35. Kim S-M, Lee H-M, Hwang K-A, Choi K-C (2017) Benzo (a) pyrene induced cell cycle arrest and apoptosis in human choriocarcinoma cancer cells through reactive oxygen species-induced endoplasmic reticulum-stress pathway. Food Chem Toxicol 107:339–348CrossRefGoogle Scholar
  36. Kolosnjaj-Tabi J, Just J, Hartman KB, Laoudi Y, Boudjemaa S, Alloyeau D, Szwarc H, Wilson LJ, Moussa F (2015) Anthropogenic carbon nanotubes found in the airways of Parisian children. EBioMedicine 2:1697–1704CrossRefGoogle Scholar
  37. Kuang T, Chang L, Chen F, Sheng Y, Fu D, Peng X (2016) Facile preparation of lightweight high-strength biodegradable polymer/multi-walled carbon nanotubes nanocomposite foams for electromagnetic interference shielding. Carbon 105:305–313CrossRefGoogle Scholar
  38. Kuijpers E, Bekker C, Fransman W, Brouwer D, Tromp P, Vlaanderen J, Godderis L, Hoet P, Lan Q, Silverman D (2015) Occupational exposure to multi-walled carbon nanotubes during commercial production synthesis and handling. Ann Occup Hyg 60:305–317CrossRefGoogle Scholar
  39. Lee J, Kim M, Hong CK, Shim SE (2007) Measurement of the dispersion stability of pristine and surface-modified multiwalled carbon nanotubes in various nonpolar and polar solvents. Meas Sci Technol 18:3707–3712CrossRefGoogle Scholar
  40. Lee JH, Lee S-B, Bae GN, Jeon KS, Yoon JU, Ji JH, Sung JH, Lee BG, Lee JH, Yang JS (2010) Exposure assessment of carbon nanotube manufacturing workplaces. Inhal Toxicol 22:369–381CrossRefGoogle Scholar
  41. Li J, Ying G-G, Jones KC, Martin FL (2015) Real-world carbon nanoparticle exposures induce brain and gonadal alterations in zebrafish (Danio rerio) as determined by biospectroscopy techniques. Analyst 140:2687–2695CrossRefGoogle Scholar
  42. Li J, Tian M, Cui L, Dwyer J, Fullwood NJ, Shen H, Martin FL (2016) Low-dose carbon-based nanoparticle-induced effects in A549 lung cells determined by biospectroscopy are associated with increases in genomic methylation. Sci Rep 6:20207CrossRefGoogle Scholar
  43. Li J, Hu L-X, Ying G-G, Martin FL (2017) Co-exposure of C 60 fullerene with benzo [a] pyrene results in enhanced biological effects in cells as determined by Fourier-transform infrared spectroscopy. Environ Sci Nano 4:1404–1418CrossRefGoogle Scholar
  44. Lin S, Wang L, Huang Y, Wang Y, Wang C, Greene ND, Ren A (2018) Oxidative stress and apoptosis in benzo [a] pyrene-induced neural tube defects. Free Radic Biol Med 116:149–158CrossRefGoogle Scholar
  45. Liu J, Wang W (2015) Reduced cadmium accumulation and toxicity in Daphnia magna under carbon nanotube exposure. Environ Tox Chem 34:2824–2832Google Scholar
  46. Liu Z, Lu Y, Rosenstein B, Lebwohl M, Wei H (1998) Benzo [a] pyrene enhances the formation of 8-hydroxy-2 ‘-deoxyguanosine by ultraviolet a radiation in calf thymus DNA and human epidermoid carcinoma cells. Biochemistry 37:10307–10312CrossRefGoogle Scholar
  47. Liu Z, Dong X, Song L, Zhang H, Liu L, Zhu D, Song C, Leng X (2014) Carboxylation of multiwalled carbon nanotube enhanced its biocompatibility with L02 cells through decreased activation of mitochondrial apoptotic pathway. J Biomed Mater Res A 102:665–673CrossRefGoogle Scholar
  48. Liu Y, Liggio J, Li S-M, Breznan D, Vincent R, Thomson EM, Kumarathasan P, Das D, Abbatt J, Antiñolo M (2015) Chemical and toxicological evolution of carbon nanotubes during atmospherically relevant aging processes. Environ Sci Technol 49:2806–2814CrossRefGoogle Scholar
  49. Long J, Xiao Y, Liu L, Cao Y (2017) The adverse vascular effects of multi-walled carbon nanotubes (MWCNTs) to human vein endothelial cells (HUVECs) in vitro: role of length of MWCNTs. J Nanobiotechnol 15:80CrossRefGoogle Scholar
  50. Long J, Li X, Kang Y, Ding Y, Gu Z, Cao Y (2018) Internalization, cytotoxicity, oxidative stress and inflammation of multi-walled carbon nanotubes in human endothelial cells: influence of pre-incubation with bovine serum albumin. RSC Adv 8:9253–9260CrossRefGoogle Scholar
  51. Mohammadian Y, Shahtaheri SJ, Kakooei H, Hajaghazadeh M (2013a) Determination of toxicological indexes of carbon nanotubes and chrysotile according to in vitro cytotoxicity on human lung epithelium cells. J School Public Health Insti Public Health Res 10:33–44Google Scholar
  52. Mohammadian Y, Shahtaheri SJ, Yaraghi AAS, Kakooei H, Hajaghazadeh M (2013b) Cytotoxicity of single-walled carbon nanotubes, multi-walled carbon nanotubes, and chrysotile to human lung epithelial cells. Toxicol Environ Chem 95:1037–1047CrossRefGoogle Scholar
  53. Mohammadian Y, Rezazadeh Azari M, Peirovi H, Khodagholi F, Pourahmad J, Omidi M, Mehrabi Y, Rafieepour A (2018) Combined toxicity of multi-walled carbon nanotubes and benzo [a] pyrene in human epithelial lung cells. Toxin Rev 1-11Google Scholar
  54. MohseniBandpi A, Eslami A, Shahsavani A, Khodagholi F, Alinejad A (2017) Physicochemical characterization of ambient PM2. 5 in Tehran air and its potential cytotoxicity in human lung epithelial cells (A549). Sci Total Environ 593:182–190CrossRefGoogle Scholar
  55. Muthusamy S, Peng C, Ng JC (2016) The binary, ternary and quaternary mixture toxicity of benzo [a] pyrene, arsenic, cadmium and lead in HepG2 cells. Toxicol Res 5:703–713Google Scholar
  56. Myer MH, Henderson WM, Black MC (2017) Effects of multiwalled carbon nanotubes on the bioavailability and toxicity of diphenhydramine to Pimephales promelas in sediment exposures. Environ Toxicol Chem 36:320–328CrossRefGoogle Scholar
  57. Nasirzadeh N, Azari MR, Rasoulzadeh Y, Mohammadian Y (2019) An assessment of the cytotoxic effects of graphene nanoparticles on the epithelial cells of the human lung. Toxicol Ind Health 35:79–87CrossRefGoogle Scholar
  58. Ogasawara Y, Umezu N, Ishii K (2012) DNA damage in human pleural mesothelial cells induced by exposure to carbon nanotubes. Nihon eiseigaku zasshi Japanese Journal of Hygiene 67:76–83CrossRefGoogle Scholar
  59. Phuyal S, Kasem M, Rubio L, Karlsson HL, Marcos R, Skaug V, Zienolddiny S (2017) Effects on human bronchial epithelial cells following low-dose chronic exposure to nanomaterials: a 6-month transformation study. Toxicol in Vitro 44:230–240CrossRefGoogle Scholar
  60. Rhiem S, Riding MJ, Baumgartner W, Martin FL, Semple KT, Jones KC, Schäffer A, Maes HM (2015) Interactions of multiwalled carbon nanotubes with algal cells: quantification of association, visualization of uptake, and measurement of alterations in the composition of cells. Environ Pollut 196:431–439CrossRefGoogle Scholar
  61. Rivera-Figueroa A, Ramazan K, Finlayson-Pitts B (2004) Fluorescence, absorption, and excitation spectra of polycyclic aromatic hydrocarbons as a tool for quantitative analysis. J Chem Educ 81:242CrossRefGoogle Scholar
  62. Schwab F, Bucheli TD, Camenzuli L, Magrez A, Knauer K, Sigg L, Nowack B (2013) Diuron sorbed to carbon nanotubes exhibits enhanced toxicity to Chlorella vulgaris. Environ Sci Technol 47:7012–7019CrossRefGoogle Scholar
  63. Shrestha B, Anderson TA, Acosta-Martinez V, Payton P, Cañas-Carrell JE (2015) The influence of multiwalled carbon nanotubes on polycyclic aromatic hydrocarbon (PAH) bioavailability and toxicity to soil microbial communities in alfalfa rhizosphere. Ecotoxicol Environ Saf 116:143–149CrossRefGoogle Scholar
  64. Siegrist KJ, Reynolds SH, Kashon ML, Lowry DT, Dong C, Hubbs AF, Young S-H, Salisbury JL, Porter DW, Benkovic SA (2014) Genotoxicity of multi-walled carbon nanotubes at occupationally relevant doses. Particle Fib Toxicol 11:6.  https://doi.org/10.1186/1743-8977-11-6
  65. Simon A, Maletz SX, Hollert H, Schäffer A, Maes HM (2014) Effects of multiwalled carbon nanotubes and triclocarban on several eukaryotic cell lines: elucidating cytotoxicity, endocrine disruption, and reactive oxygen species generation. Nanoscale Res Lett 9:396CrossRefGoogle Scholar
  66. Simon A, Preuss TG, Schäffer A, Hollert H, Maes HM (2015) Population level effects of multiwalled carbon nanotubes in Daphnia magna exposed to pulses of triclocarban. Ecotoxicology 24:1199–1212CrossRefGoogle Scholar
  67. Song M, Wang F, Zeng L, Yin J, Wang H, Jiang G (2014) Co-exposure of carboxyl-functionalized single-walled carbon nanotubes and 17α-ethinylestradiol in cultured cells: effects on bioactivity and cytotoxicity. Environ Sci Technol 48:13978–13984CrossRefGoogle Scholar
  68. Sosnowski TR, Koliński M, Gradoń L (2011) Interactions of benzo [a] pyrene and diesel exhaust particulate matter with the lung surfactant system. Ann Occup Hyg 55:329–338Google Scholar
  69. Speit G, Bonzheim I (2003) Genotoxic and protective effects of hyperbaric oxygen in A549 lung cells. Mutagenesis 18:545–548CrossRefGoogle Scholar
  70. Takaya M, Ono-Ogasawara M, Shinohara Y, Kubota H, Tsuruoka S, Koda S (2012) Evaluation of exposure risk in the weaving process of MWCNT-coated yarn with real-time particle concentration measurements and characterization of dust particles. Ind Health 50:147–155CrossRefGoogle Scholar
  71. Therond P (2006) Oxidative stress and damages to biomolecules (lipids, proteins, DNA), Annales pharmaceutiques francaises, pp 383–389Google Scholar
  72. Tofighy MA, Mohammadi T (2011) Adsorption of divalent heavy metal ions from water using carbon nanotube sheets. J Hazard Mater 185:140–147CrossRefGoogle Scholar
  73. Ursini CL, Cavallo D, Fresegna AM, Ciervo A, Maiello R, Casciardi S, Tombolini F, Buresti G, Iavicoli S (2012) Study of cytotoxic and genotoxic effects of hydroxyl-functionalized multiwalled carbon nanotubes on human pulmonary cells. J Nanomater 2012:7CrossRefGoogle Scholar
  74. Valavanidis A, Vlachogianni T, Fiotakis C (2009) 8-Hydroxy-2′-deoxyguanosine (8-OHdG): a critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health C 27:120–139CrossRefGoogle Scholar
  75. Yan Z, Liu Y, Sun H, Lu G (2018) Influence of multiwall carbon nanotubes on the toxicity of 17β-estradiol in the early life stages of zebrafish. Environ Sci Pollut Res 25:7566–7574CrossRefGoogle Scholar
  76. Yang K, Zhu L, Xing B (2006) Adsorption of polycyclic aromatic hydrocarbons by carbon nanomaterials. Environ Sci Technol 40:1855–1861CrossRefGoogle Scholar
  77. Yu Y, Duan J, Li Y, Yu Y, Jin M, Li C, Wang Y, Sun Z (2015) Combined toxicity of amorphous silica nanoparticles and methylmercury to human lung epithelial cells. Ecotoxicol Environ Saf 112:144–152CrossRefGoogle Scholar
  78. Zakeri M, Mahmoodian Sany H (2012) Carbon nano tubes play a role in the adsorption some of carcinogenic compounds, 4th International Conference on Nanostructures (ICNS4)Google Scholar
  79. Zhou L, Forman HJ, Ge Y, Lunec J (2017) Multi-walled carbon nanotubes: a cytotoxicity study in relation to functionalization, dose and dispersion. Toxicol in Vitro 42:292–298CrossRefGoogle Scholar
  80. Zindler F, Glomstad B, Altin D, Liu J, Jenssen BM, Booth AM (2016) Phenanthrene bioavailability and toxicity to Daphnia magna in the presence of carbon nanotubes with different physicochemical properties. Environ Sci Technol 50:12446–12454CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Mansour Rezazadeh Azari
    • 1
  • Yousef Mohammadian
    • 1
    • 2
    Email author
  • Jalal Pourahmad
    • 3
  • Fariba Khodagholi
    • 4
  • Habibollah Peirovi
    • 5
  • Yadollah Mehrabi
    • 1
  • Meisam Omidi
    • 6
  • Athena Rafieepour
    • 1
  1. 1.School of Public Health and SafetyShahid Beheshti University of Medical SciencesTehranIran
  2. 2.Department of Occupational Health Engineering, Faculty of HealthTabriz University of Medical SciencesTabrizIran
  3. 3.Department of Toxicology, Faculty of PharmacyShahid Beheshti University of Medical SciencesTehranIran
  4. 4.Neuroscience Research CenterShahid Beheshti University of Medical SciencesTehranIran
  5. 5.Medical Nanotechnology and Tissue Engineering Research CenterShahid Beheshti University of Medical SciencesTehranIran
  6. 6.Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in MedicineShahid Beheshti University of Medical SciencesTehranIran

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