Developmental toxicity of carbon nanoparticles during embryogenesis in chicken

  • Dalia H. Samak
  • Yasser S. El-Sayed
  • Hazem M. Shaheen
  • Ali H. El-Far
  • Mohamed E. Abd El-Hack
  • Ahmed E. Noreldin
  • Karima El-Naggar
  • Sameh A. Abdelnour
  • Essa M. Saied
  • Hesham R. El-Seedi
  • Lotfi Aleya
  • Mohamed M. Abdel-Daim
Nanotechnology, Nanopollution, Nanotoxicology and Nanomedicine (NNNN)


Nanoparticles (NPs) are very small particles present in a wide range of materials. There is a dearth of knowledge regarding their potential secondary effects on the health of living organisms and the environment. Increasing research attention, however, has been directed toward determining the effects on humans exposed to NPs in the environment. Although the majority of studies focus on adult animals or populations, embryos of various species are considered more susceptible to environmental effects and pollutants. Hence, research studies dealing mainly with the impacts of NPs on embryogenesis have emerged recently, as this has become a major concern. Chicken embryos occupy a special place among animal models used in toxicity and developmental investigations and have also contributed significantly to the fields of genetics, virology, immunology, cell biology, and cancer. Their rapid development and easy accessibility for experimental observance and manipulation are just a few of the advantages that have made them the vertebrate model of choice for more than two millennia. The early stages of chicken embryogenesis, which are characterized by rapid embryonic growth, provide a sensitive model for studying the possible toxic effects on organ development, body weight, and oxidative stress. The objective of this review was to evaluate the toxicity of various types of carbon black nanomaterials administered at the beginning of embryogenesis in a chicken embryo model. In addition, the effects of diamond and graphene NPs and carbon nanotubes are reviewed.


Nanotoxicity Carbon black nanoparticles Embryogenesis Chicken 



The authors extend thanks to their respective institutes and universities.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests with regard to the manuscript.


  1. Aam BB, Fonnum F (2007) Carbon black particles increase reactive oxygen species formation in rat alveolar macrophages in vitro. Arch Toxicol 81:441–446CrossRefGoogle Scholar
  2. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ (2010) Structure and function of the blood–brain barrier. Neurobiol Dis 37:13–25CrossRefGoogle Scholar
  3. Ali H, Bhunia SK, Dalal C, Jana NR (2016) Red fluorescent carbon nanoparticle-based cell imaging probe. ACS Appl Mater Interfaces 8:9305–9313CrossRefGoogle Scholar
  4. Allen R, Tresini M (2000) Oxidative stress and gene regulation. Free Radic Biol Med 28:463–499CrossRefGoogle Scholar
  5. Azad N, Iyer AKV, Wang L, Liu Y, Lu Y, Rojanasakul Y (2013) Reactive oxygen species-mediated p38 MAPK regulates carbon nanotube-induced fibrogenic and angiogenic responses. Nanotoxicology 7:157–168CrossRefGoogle Scholar
  6. Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, Cogliano V, Group WIAfRoCMW (2006) Carcinogenicity of carbon black, titanium dioxide, and talc. Lancet Oncol 7:295–296CrossRefGoogle Scholar
  7. Baulig A, Garlatti M, Bonvallot V, Marchand A, Barouki R, Marano F, Baeza-Squiban A (2003) Involvement of reactive oxygen species in the metabolic pathways triggered by diesel exhaust particles in human airway epithelial cells. Am J Phys Lung Cell Mol Phys 285:L671–L679Google Scholar
  8. Belyanskaya L, Weigel S, Hirsch C, Tobler U, Krug HF, Wick P (2009) Effects of carbon nanotubes on primary neurons and glial cells. Neurotoxicology 30:702–711CrossRefGoogle Scholar
  9. Bhunia SK, Saha A, Maity AR, Ray SC, Jana NR (2013) Carbon nanoparticle-based fluorescent bioimaging probes. Sci Rep 3:1473CrossRefGoogle Scholar
  10. Bonner JC (2002) The epidermal growth factor receptor at the crossroads of airway remodeling. Am J Phys Lung Cell Mol Phys 283:L528–L530Google Scholar
  11. Bonner JC (2007) Lung fibrotic responses to particle exposure. Toxicol Pathol 35:148–153CrossRefGoogle Scholar
  12. Boonstra J, Post JA (2004) Molecular events associated with reactive oxygen species and cell cycle progression in mammalian cells. Gene 337:1–13CrossRefGoogle Scholar
  13. Bresgen N, Karlhuber G, Krizbai I, Bauer H, Bauer HC, Eckl PM (2003) Oxidative stress in cultured cerebral endothelial cells induces chromosomal aberrations, micronuclei, and apoptosis. J Neurosci Res 72:327–333CrossRefGoogle Scholar
  14. Butterfield DA, Castegna A, Lauderback CM, Drake J (2002) Evidence that amyloid beta-peptide-induced lipid peroxidation and its sequelae in Alzheimer’s disease brain contribute to neuronal death. Neurobiol Aging 23:655–664CrossRefGoogle Scholar
  15. Buzea C, Pacheco II, Robbie K (2007) Nanomaterials and nanoparticles: sources and toxicity. Biointerphases 2:MR17–MR71CrossRefGoogle Scholar
  16. Chan JK, Kodani SD, Charrier JG, Morin D, Edwards PC, Anderson DS, Anastasio C, Van Winkle LS (2013) Age-specific effects on rat lung glutathione and antioxidant enzymes after inhaling ultrafine soot. Am J Respir Cell Mol Biol 48:114–124CrossRefGoogle Scholar
  17. Chen R, Zhang L, Ge C, Tseng MT, Bai R, Qu Y, Beer C, Autrup H, Chen C (2015) Subchronic toxicity and cardiovascular responses in spontaneously hypertensive rats after exposure to multiwalled carbon nanotubes by intratracheal instillation. Chem Res Toxicol 28:440–450CrossRefGoogle Scholar
  18. Chen S, Hu S, Smith EF, Ruenraroengsak P, Thorley AJ, Menzel R, Goode AE, Ryan MP, Tetley TD, Porter AE (2014) Aqueous cationic, anionic and non-ionic multi-walled carbon nanotubes, functionalised with minimal framework damage, for biomedical application. Biomaterials 35:4729–4738CrossRefGoogle Scholar
  19. Choi J, Krushel LA, Crossin KL (2001) NF-κB activation by N-CAM and cytokines in astrocytes is regulated by multiple protein kinases and redox modulation. Glia 33:45–56CrossRefGoogle Scholar
  20. Clichici S, Biris AR, Tabaran F, Filip A (2012) Transient oxidative stress and inflammation after intraperitoneal administration of multiwalled carbon nanotubes functionalized with single strand DNA in rats. Toxicol Appl Pharmacol 259:281–292CrossRefGoogle Scholar
  21. Donaldson K, Stone V (2003) Current hypotheses on the mechanisms of toxicity of ultrafine particles. Ann Ist Super Sanita 39:405–410Google Scholar
  22. Donaldson K, Tran L, Jimenez LA, Duffin R, Newby DE, Mills N, MacNee W, Stone V (2005) Combustion-derived nanoparticles: a review of their toxicology following inhalation exposure. Part Fibre Toxicol 2:10CrossRefGoogle Scholar
  23. Donaldson K, Murphy FA, Duffin R, Poland CA (2010) Asbestos, carbon nanotubes and the pleural mesothelium: a review of the hypothesis regarding the role of long fibre retention in the parietal pleura, inflammation and mesothelioma. Part Fibre Toxicol 7:5CrossRefGoogle Scholar
  24. Dörger M, Krombach F (2002) Response of alveolar macrophages to inhaled particulates. Eur Surg Res 34:47–52CrossRefGoogle Scholar
  25. Du P, Zhao J, Mashayekhi H, Xing B (2014) Adsorption of bovine serum albumin and lysozyme on functionalized carbon nanotubes. J Phys Chem C 118:22249–22257CrossRefGoogle Scholar
  26. El-Sayed YS, Shimizu R, Onoda A, Takeda K, Umezawa M (2015) Carbon black nanoparticle exposure during middle and late fetal development induces immune activation in male offspring mice. Toxicology 327:53–61CrossRefGoogle Scholar
  27. Engelhardt B, Sorokin L (2009) The blood–brain and the blood–cerebrospinal fluid barriers: function and dysfunction, Semin Immunopathol. Springer, pp. 497–511Google Scholar
  28. Eom H-J, Choi J (2010) p38 MAPK activation, DNA damage, cell cycle arrest and apoptosis as mechanisms of toxicity of silver nanoparticles in Jurkat T cells. Environ Sci Technol 44:8337–8342CrossRefGoogle Scholar
  29. 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 82:151–157CrossRefGoogle Scholar
  30. Fenoglio I, Greco G, Tomatis M, Muller J, Raymundo-Pinero E, Béguin F, Fonseca A, Nagy JB, Lison D, Fubini B (2008) Structural defects play a major role in the acute lung toxicity of multiwall carbon nanotubes: physicochemical aspects. Chem Res Toxicol 21:1690–1697CrossRefGoogle Scholar
  31. Firme CP, Bandaru PR (2010) Toxicity issues in the application of carbon nanotubes to biological systems. Nanomedicine 6:245–256CrossRefGoogle Scholar
  32. Floyd RA, Carney JM (1992) Free radical damage to protein and DNA: mechanisms involved and relevant observations on brain undergoing oxidative stress. Ann Neurol 32:S22–S27CrossRefGoogle Scholar
  33. Frikke-Schmidt H, Roursgaard M, Lykkesfeldt J, Loft S, Nøjgaard JK, Møller P (2011) Effect of vitamin C and iron chelation on diesel exhaust particle and carbon black induced oxidative damage and cell adhesion molecule expression in human endothelial cells. Toxicol Lett 203:181–189CrossRefGoogle Scholar
  34. Fukai T, Folz RJ, Landmesser U, Harrison DG (2002) Extracellular superoxide dismutase and cardiovascular disease. Cardiovasc Res 55:239–249CrossRefGoogle Scholar
  35. García-Arellano H, Buenrostro-Gonzalez E, Vazquez-Duhalt R (2004) Biocatalytic transformation of petroporphyrins by chemical modified cytochrome c. Biotechnol Bioeng 85:790–798CrossRefGoogle Scholar
  36. Genestra M (2007) Oxyl radicals, redox-sensitive signalling cascades and antioxidants. Cell Signal 19:1807–1819CrossRefGoogle Scholar
  37. Grodzik M, Sawosz E, Wierzbicki M, Orlowski P, Hotowy A, Niemiec T, Szmidt M, Mitura K, Chwalibog A (2011) Nanoparticles of carbon allotropes inhibit glioblastoma multiforme angiogenesis in ovo. Int J Nanomedicine 6:3041Google Scholar
  38. Grodzik M (2013) Changes in glioblastoma multiforme ultrastructure after diamond nanoparticles treatment. Experimental model in ovo. Ann Warsaw Univ Life Sci Anim Sci 52:29–35Google Scholar
  39. Grodzik M, Sawosz F, Sawosz E, Hotowy A, Wierzbicki M, Kutwin M, Jaworski S, Chwalibog A (2013) Nano-nutrition of chicken embryos. The effect of in ovo administration of diamond nanoparticles and L-glutamine on molecular responses in chicken embryo pectoral muscles. Int J Mol Sci 14:23033–23044CrossRefGoogle Scholar
  40. Gürer H, Özgünes H, Neal R, Spitz DR, Erçal N (1998) Antioxidant effects of N-acetylcysteine and succimer in red blood cells from lead-exposed rats. Toxicology 128:181–189CrossRefGoogle Scholar
  41. Habib GM, Shi Z-Z, Lieberman MW (2007) Glutathione protects cells against arsenite-induced toxicity. Free Radic Biol Med 42:191–201CrossRefGoogle Scholar
  42. Halliwell B (1994) Free radicals, antioxidants, and human disease: curiosity, cause, or consequence? Lancet 344:721–724CrossRefGoogle Scholar
  43. Halliwell B (1996) Antioxidants: the basics-what they are and how to evaluate them. Adv Pharmacol. Elsevier, pp. 3–20Google Scholar
  44. Hawkins BT, Davis TP (2005) The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 57:173–185CrossRefGoogle Scholar
  45. He X, Young S-H, Schwegler-Berry D, Chisholm WP, Fernback JE, Ma Q (2011) Multiwalled carbon nanotubes induce a fibrogenic response by stimulating reactive oxygen species production, activating NF-κB signaling, and promoting fibroblast-to-myofibroblast transformation. Chem Res Toxicol 24:2237–2248CrossRefGoogle Scholar
  46. Hsin Y-H, Chen C-F, Huang S, Shih T-S, Lai P-S, Chueh PJ (2008) The apoptotic effect of nanosilver is mediated by a ROS-and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cells. Toxicol Lett 179:130–139CrossRefGoogle Scholar
  47. Huang C-C, Aronstam RS, Chen D-R, Huang Y-W (2010) Oxidative stress, calcium homeostasis, and altered gene expression in human lung epithelial cells exposed to ZnO nanoparticles. Toxicol in Vitro 24:45–55CrossRefGoogle Scholar
  48. Hussain S, Thomassen LC, Ferecatu I, Borot M-C, Andreau K, Martens JA, Fleury J, Baeza-Squiban A, Marano F, Boland S (2010) Carbon black and titanium dioxide nanoparticles elicit distinct apoptotic pathways in bronchial epithelial cells. Part Fibre Toxicol 7:10CrossRefGoogle Scholar
  49. IARC (2010) Carbon black, titanium dioxide, and talc., Monographs on the Evaluation of Carcinogenic Risks to Humans/World Health Organization. IARC Press, International Agency for Research on Cancer, pp. 1–413Google Scholar
  50. IFA (2018) Criteria for assessment of the effectiveness of protective measuresGoogle Scholar
  51. Jackson P, Hougaard KS, Boisen AMZ, Jacobsen NR, Jensen KA, Møller P, Brunborg G, Gutzkow KB, Andersen O, Loft S (2012) Pulmonary exposure to carbon black by inhalation or instillation in pregnant mice: effects on liver DNA strand breaks in dams and offspring. Nanotoxicology 6:486–500CrossRefGoogle Scholar
  52. Jackson P, Jacobsen NR, Baun A, Birkedal R, Kühnel D, Jensen KA, Vogel U, Wallin H (2013) Bioaccumulation and ecotoxicity of carbon nanotubes. Chem Cent J 7:154CrossRefGoogle Scholar
  53. Jacobsen NR, White PA, Gingerich J, Møller P, Saber AT, Douglas GR, Vogel U, Wallin H (2011) Mutation spectrum in FE1-MUTATMMouse lung epithelial cells exposed to nanoparticulate carbon black. Environ Mol Mutagen 52:331–337CrossRefGoogle Scholar
  54. Karagkiozaki V, Karagiannidis P, Gioti M, Kavatzikidou P, Georgiou D, Georgaraki E, Logothetidis S (2013) Bioelectronics meets nanomedicine for cardiovascular implants: PEDOT-based nanocoatings for tissue regeneration. Biochim Biophys Acta, Gen Subj 1830:4294–4304CrossRefGoogle Scholar
  55. Karpeta-Kaczmarek J, Dziewięcka M, Augustyniak M, Rost-Roszkowska M, Pawlyta M (2016) Oxidative stress and genotoxic effects of diamond nanoparticles. Environ Res 148:264–272CrossRefGoogle Scholar
  56. Koromilas ND, Lainioti GC, Gialeli C, Barbouri D, Kouravelou KB, Karamanos NK, Voyiatzis GA, Kallitsis JK (2014) Preparation and toxicological assessment of functionalized carbon nanotube-polymer hybrids. PLoS One 9:e107029CrossRefGoogle Scholar
  57. Kreyling W, Semmler M, Erbe F, Mayer P, Takenaka S, Schulz H, Oberdörster G, Ziesenis A (2002) Translocation of ultrafine insoluble iridium particles from lung epithelium to extrapulmonary organs is size dependent but very low. J Toxicol Environ Health A 65:1513–1530CrossRefGoogle Scholar
  58. Krueger M, Bechmann I (2010) CNS pericytes: concepts, misconceptions, and a way out. Glia 58:1–10CrossRefGoogle Scholar
  59. Kurantowicz N, Sawosz E, Halik G, Strojny B, Hotowy A, Grodzik M, Piast R, Pasanphan W, Chwalibog A (2017) Toxicity studies of six types of carbon nanoparticles in a chicken-embryo model. Int J Nanomedicine 12:2887CrossRefGoogle Scholar
  60. Lara-Martínez LA, Massó F, González EP, García-Peláez I, Contreras-Ramos A, Valverde M, Rojas E, Cervantes-Sodi F, Hernández-Gutiérrez S (2017) Evaluating the biological risk of functionalized multiwalled carbon nanotubes and functionalized oxygen-doped multiwalled carbon nanotubes as possible toxic, carcinogenic, and embryotoxic agents. Int J Nanomedicine 12:7695CrossRefGoogle Scholar
  61. Lavrinenko V, Tchaikovskyi Y, Degtiariova L (2016a) Biological effect of nanodiamonds and soot on structural and functional conditions of chiken embryo kidneys. Bulletin of Taras Shevchenko National University of Kyiv. Series. Biology 70:61–64Google Scholar
  62. Lavrinenko V, Zinabadinova S, Chaikovsky Y, Sokurenko L, Shobat L (2016b) Influence of nanodiamonds and carbon nanowires on survival and cells structure in chicken embryo. Georgian Med News 255:93–99Google Scholar
  63. Le Goff A, Holzinger M, Cosnier S (2011) Enzymatic biosensors based on SWCNT-conducting polymer electrodes. Analyst 136:1279–1287CrossRefGoogle Scholar
  64. Lee WJ, Maiti UN, Lee JM, Lim J, Han TH, Kim SO (2014) Nitrogen-doped carbon nanotubes and graphene composite structures for energy and catalytic applications. Chem Commun 50:6818–6830CrossRefGoogle Scholar
  65. Lenaz G (2001) The mitochondrial production of reactive oxygen species: mechanisms and implications in human pathology. IUBMB Life 52:159–164CrossRefGoogle Scholar
  66. Li JJ, Muralikrishnan S, Ng C-T, Yung L-YL, Bay B-H (2010) Nanoparticle-induced pulmonary toxicity. Exp Biol Med 235:1025–1033CrossRefGoogle Scholar
  67. Li N, Xia T, Nel AE (2008) The role of oxidative stress in ambient particulate matter-induced lung diseases and its implications in the toxicity of engineered nanoparticles. Free Radic Biol Med 44:1689–1699CrossRefGoogle Scholar
  68. Lim JH, Kim SH, Shin IS, Park NH, Moon C, Kang SS, Kim SH, Park SC, Kim JC (2011): Maternal exposure to multi-wall carbon nanotubes does not induce embryo-fetal developmental toxicity in rats. Birth defects research. Part B, Developmental and reproductive toxicology 92, 69–76. CrossRefGoogle Scholar
  69. Lochhead JJ, McCaffrey G, Quigley CE, Finch J, DeMarco KM, Nametz N, Davis TP (2010) Oxidative stress increases blood–brain barrier permeability and induces alterations in occludin during hypoxia–reoxygenation. J Cereb Blood Flow Metab 30:1625–1636CrossRefGoogle Scholar
  70. Lu T, Chai Q, Yu L, d’Uscio LV, Katusic ZS, He T, Lee H-C (2012) Reactive oxygen species signaling facilitates FOXO-3a/FBXO-dependent vascular BK channel β1 subunit degradation in diabetic mice. Diabetes, DB_111658CrossRefGoogle Scholar
  71. Magrez A, Kasas S, Salicio V, Pasquier N, Seo JW, Celio M, Catsicas S, Schwaller B, Forró L (2006) Cellular toxicity of carbon-based nanomaterials. Nano Lett 6:1121–1125CrossRefGoogle Scholar
  72. Manke A, Wang L, Rojanasakul Y (2013) Mechanisms of nanoparticle-induced oxidative stress and toxicity. Biomed Res Int 2013:1–15CrossRefGoogle Scholar
  73. Manna SK, Sarkar S, Barr J, Wise K, Barrera EV, Jejelowo O, Rice-Ficht AC, Ramesh GT (2005) Single-walled carbon nanotube induces oxidative stress and activates nuclear transcription factor-κB in human keratinocytes. Nano Lett 5:1676–1684CrossRefGoogle Scholar
  74. Maynard AD, Baron PA, Foley M, Shvedova AA, Kisin ER, Castranova V (2004) Exposure to carbon nanotube material: aerosol release during the handling of unrefined single-walled carbon nanotube material. J Toxicol Environ Health A 67:87–107CrossRefGoogle Scholar
  75. Maynard AD, Ku BK, Emery M, Stolzenburg M, McMurry PH (2007) Measuring particle size-dependent physicochemical structure in airborne single walled carbon nanotube agglomerates. J Nanopart Res 9:85–92CrossRefGoogle Scholar
  76. Mc Carthy DJ, Malhotra M, O’Mahony AM, Cryan JF, O’Driscoll CM (2015) Nanoparticles and the blood-brain barrier: advancing from in-vitro models towards therapeutic significance. Pharm Res 32:1161–1185CrossRefGoogle Scholar
  77. Methner M (2008) Engineering case reports. Effectiveness of local exhaust ventilation (LEV) in controlling engineered nanomaterial emissions during reactor cleanout operations. J Occup Environ Hyg 5:D63CrossRefGoogle Scholar
  78. Mitchell LA, Gao J, Wal RV, Gigliotti A, Burchiel SW, McDonald JD (2007) Pulmonary and systemic immune response to inhaled multiwalled carbon nanotubes. Toxicol Sci 100:203–214CrossRefGoogle Scholar
  79. Mohr U, Ernst H, Roller M, Pott F (2006) Pulmonary tumor types induced in Wistar rats of the so-called “19-dust study”. Exp Toxicol Pathol 58:13–20CrossRefGoogle Scholar
  80. Möller W, Brown DM, Kreyling WG, Stone V (2005) Ultrafine particles cause cytoskeletal dysfunctions in macrophages: role of intracellular calcium. Part Fibre Toxicol 2:7CrossRefGoogle Scholar
  81. Ong L-C, Chung FF-L, Tan Y-F, Leong C-O (2016) Toxicity of single-walled carbon nanotubes. Arch Toxicol 90:103–118CrossRefGoogle Scholar
  82. Pacurari M, Yin XJ, Zhao J, Ding M, Leonard SS, Schwegler-Berry D, Ducatman BS, Sbarra D, Hoover MD, Castranova V (2008) Raw single-wall carbon nanotubes induce oxidative stress and activate MAPKs, AP-1, NF-κB, and Akt in normal and malignant human mesothelial cells. Environ Health Perspect 116:1211CrossRefGoogle Scholar
  83. Park E-J, Choi J, Park Y-K, Park K (2008) Oxidative stress induced by cerium oxide nanoparticles in cultured BEAS-2B cells. Toxicology 245:90–100CrossRefGoogle Scholar
  84. Petersen EJ, Zhang L, Mattison NT, O’Carroll DM, Whelton AJ, Uddin N, Nguyen T, Huang Q, Henry TB, Holbrook RD (2011) Potential release pathways, environmental fate, and ecological risks of carbon nanotubes. Environ Sci Technol 45:9837–9856CrossRefGoogle Scholar
  85. Piccinno F, Gottschalk F, Seeger S, Nowack B (2012) Industrial production quantities and uses of ten engineered nanomaterials in Europe and the world. J Nanopart Res 14:1109CrossRefGoogle Scholar
  86. Poljak-Blaži M, Jaganjac M, Žarković N (2010) Cell oxidative stress: risk of metal nanoparticles, handbook of nanophysics nanomedicine and nanorobotics. CRC Press Taaylor, NewYork, pp 1–17Google Scholar
  87. Pumera M (2010) Carbon nanotube biosensors based on electrochemical detection, Carbon Nanotubes. Springer, pp. 205–212Google Scholar
  88. Rahman SH, Nanny C, Ibrahim K, O’Reilly D, Larvin M, Kingsnorth AJ, McMahon MJ (2005) Genetic polymorphisms of GSTT1, GSTM1, GSTP1, MnSOD, and catalase in nonhereditary chronic pancreatitis: evidence of xenobiotic stress and impaired antioxidant capacity. Dig Dis Sci 50:1376–1383CrossRefGoogle Scholar
  89. Ramnani P, Saucedo NM, Mulchandani A (2016) Carbon nanomaterial-based electrochemical biosensors for label-free sensing of environmental pollutants. Chemosphere 143:85–98CrossRefGoogle Scholar
  90. Rashidi H, Sottile V (2009) The chick embryo: hatching a model for contemporary biomedical research. Bioessays 31:459–465CrossRefGoogle Scholar
  91. Reddy AR, Krishna DR, Reddy YN, Himabindu V (2010) Translocation and extra pulmonary toxicities of multi wall carbon nanotubes in rats. Toxicol Mech Methods 20:267–272CrossRefGoogle Scholar
  92. Reisetter AC, Stebounova LV, Baltrusaitis J, Powers L, Gupta A, Grassian VH, Monick MM (2011) Induction of inflammasome-dependent pyroptosis by carbon black nanoparticles. J Biol Chem 286:21844–21852CrossRefGoogle Scholar
  93. Ren X, Chen C, Nagatsu M, Wang X (2011) Carbon nanotubes as adsorbents in environmental pollution management: a review. Chem Eng J 170:395–410CrossRefGoogle Scholar
  94. Ribatti D (2012) Chicken chorioallantoic membrane angiogenesis model, Cardiovascular Development. Springer, pp. 47–57Google Scholar
  95. Richard V, Kenneth J, Ramaprabha P, Kirupakaran H, Chandy G (2001) Impact of introduction of sharps containers and of education programmes on the pattern of needle stick injuries in a tertiary care Centre in India. J Hosp Infect 47:163–165CrossRefGoogle Scholar
  96. Risom L, Møller P, Loft S (2005) Oxidative stress-induced DNA damage by particulate air pollution. Mutat Res 592:119–137CrossRefGoogle Scholar
  97. Rivera Gil P, Oberdörster GN, Elder A, Puntes VC, Parak WJ (2010) Correlating physico-chemical with toxicological properties of nanoparticles: the present and the future. ACS Nano 4:5527–5531CrossRefGoogle Scholar
  98. Roman D, Yasmeen A, Mireuta M, Stiharu I, Al Moustafa A-E (2013) Significant toxic role for single-walled carbon nanotubes during normal embryogenesis. Nanomedicine 9:945–950CrossRefGoogle Scholar
  99. Saber AT, Jensen KA, Jacobsen NR, Birkedal R, Mikkelsen L, Møller P, Loft S, Wallin H, Vogel U (2012) Inflammatory and genotoxic effects of nanoparticles designed for inclusion in paints and lacquers. Nanotoxicology 6:453–471CrossRefGoogle Scholar
  100. Sadauskas E, Wallin H, Stoltenberg M, Vogel U, Doering P, Larsen A, Danscher G (2007) Kupffer cells are central in the removal of nanoparticles from the organism. Part Fibre Toxicol 4:10CrossRefGoogle Scholar
  101. Sadauskas E, Jacobsen NR, Danscher G, Stoltenberg M, Vogel U, Larsen A, Kreyling W, Wallin H (2009) Biodistribution of gold nanoparticles in mouse lung following intratracheal instillation. Chem Cent J 3:16CrossRefGoogle Scholar
  102. Samak DH, El-Sayed YS, Shaheen HM, El-Far AH, Onoda A, Abdel-Daim MM, Umezawa M (2018) In-ovo exposed carbon black nanoparticles altered mRNA gene transcripts of antioxidants, proinflammatory and apoptotic pathways in the brain of chicken embryos. Chem Biol Interact 295:133–139. CrossRefGoogle Scholar
  103. Sandoval KE, Witt KA (2008) Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis 32:200–219CrossRefGoogle Scholar
  104. Sarnat SE, Raysoni AU, Li W-W, Holguin F, Johnson BA, Luevano SF, Garcia JH, Sarnat JA (2011) Air pollution and acute respiratory response in a panel of asthmatic children along the US–Mexico border. Environ Health Perspect 120:437–444CrossRefGoogle Scholar
  105. Saunders NR, Ek CJ, Habgood MD, Dziegielewska KM (2008) Barriers in the brain: a renaissance? Trends Neurosci 31:279–286CrossRefGoogle Scholar
  106. Sawosz E, Jaworski S, Kutwin M, Hotowy A, Wierzbicki M, Grodzik M, Kurantowicz N, Strojny B, Lipińska L, Chwalibog A (2014) Toxicity of pristine graphene in experiments in a chicken embryo model. Int J Nanomedicine 9:3913Google Scholar
  107. Schulte P, Geraci C, Zumwalde R, Hoover M, Kuempel E (2008) Occupational risk management of engineered nanoparticles. J Occup Environ Hyg 5:239–249CrossRefGoogle Scholar
  108. Scida K, Stege PW, Haby G, Messina GA, García CD (2011) Recent applications of carbon-based nanomaterials in analytical chemistry: critical review. Anal Chim Acta 691:6–17CrossRefGoogle Scholar
  109. Shah M, Choi MH, Ullah N, Kim MO, Yoon SC (2011) Synthesis and characterization of PHV-block-mPEG diblock copolymer and its formation of amphiphilic nanoparticles for drug delivery. J Nanosci Nanotechnol 11:5702–5710CrossRefGoogle Scholar
  110. Sharma HS, Ali SF, Hussain SM, Schlager JJ, Sharma A (2009) Influence of engineered nanoparticles from metals on the blood-brain barrier permeability, cerebral blood flow, brain edema and neurotoxicity. An experimental study in the rat and mice using biochemical and morphological approaches. J Nanosci Nanotechnol 9:5055–5072CrossRefGoogle Scholar
  111. Sharma HS, Sharma A (2013) New perspectives of nanoneuroprotection, nanoneuropharmacology and nanoneurotoxicity: modulatory role of amino acid neurotransmitters, stress, trauma, and co-morbidity factors in nanomedicine. Amino Acids 45:1055–1071CrossRefGoogle Scholar
  112. Shvedova AA, Kisin E, Murray AR, Johnson VJ, Gorelik O, Arepalli S, Hubbs AF, Mercer RR, Keohavong P, Sussman N (2008) Inhalation vs. aspiration of single-walled carbon nanotubes in C57BL/6 mice: inflammation, fibrosis, oxidative stress, and mutagenesis. Am J Phys Lung Cell Mol Phys 295:L552–L565Google Scholar
  113. Shvedova AA, Kapralov AA, Feng WH, Kisin ER, Murray AR, Mercer RR, Croix CMS, Lang MA, Watkins SC, Konduru NV (2012a) Impaired clearance and enhanced pulmonary inflammatory/fibrotic response to carbon nanotubes in myeloperoxidase-deficient mice. PLoS One 7:e30923CrossRefGoogle Scholar
  114. Shvedova AA, Pietroiusti A, Fadeel B, Kagan VE (2012b) Mechanisms of carbon nanotube-induced toxicity: focus on oxidative stress. Toxicol Appl Pharmacol 261:121–133CrossRefGoogle Scholar
  115. Stambe C, Atkins RC, Tesch GH, Masaki T, Schreiner GF, Nikolic-Paterson DJ (2004) The role of p38α mitogen-activated protein kinase activation in renal fibrosis. J Am Soc Nephrol 15:370–379CrossRefGoogle Scholar
  116. Stern ST, McNeil SE (2007) Nanotechnology safety concerns revisited. Toxicol Sci 101:4–21CrossRefGoogle Scholar
  117. Stone V, Tuinman M, Vamvakopoulos J, Shaw J, Brown D, Petterson S, Faux S, Borm P, MacNee W, Michaelangeli F (2000) Increased calcium influx in a monocytic cell line on exposure to ultrafine carbon black. Eur Respir J 15:297–303CrossRefGoogle Scholar
  118. Stone V, Johnston H, Clift MJ (2007) Air pollution, ultrafine and nanoparticle toxicology: cellular and molecular interactions. IEEE Trans Nanotechnol 6:331–340Google Scholar
  119. Su Y, Yan X, Pu Y, Xiao F, Wang D, Yang M (2013) Risks of single-walled carbon nanotubes acting as contaminants-carriers: potential release of phenanthrene in Japanese medaka (Oryzias latipes). Environ Sci Technol 47:4704–4710CrossRefGoogle Scholar
  120. Szmidt M, Sawosz E, Urbańska K, Jaworski S, Kutwin M, Hotowy A, Wierzbicki M, Grodzik M, Lipińska L, Chwalibog A (2016) Toxicity of different forms of graphene in a chicken embryo model. Environ Sci Pollut Res Int 23:19940–19948CrossRefGoogle Scholar
  121. Tiwari JN, Vij V, Kemp KC, Kim KS (2015) Engineered carbon-nanomaterial-based electrochemical sensors for biomolecules. ACS Nano 10:46–80CrossRefGoogle Scholar
  122. Utsunomiya S, Jensen KA, Keeler GJ, Ewing RC (2004) Direct identification of trace metals in fine and ultrafine particles in the Detroit urban atmosphere. Environ Sci Technol 38:2289–2297CrossRefGoogle Scholar
  123. Van Broekhuizen P, van Broekhuizen F, Cornelissen R, Reijnders L (2011) Use of nanomaterials in the European construction industry and some occupational health aspects thereof. J Nanopart Res 13:447–462CrossRefGoogle Scholar
  124. Warheit DB, Laurence BR, Reed KL, Roach DH, Reynolds GA, Webb TR (2004) Comparative pulmonary toxicity assessment of single-wall carbon nanotubes in rats. Toxicol Sci 77:117–125CrossRefGoogle Scholar
  125. Watts LT, Rathinam ML, Schenker S, Henderson GI (2005) Astrocytes protect neurons from ethanol-induced oxidative stress and apoptotic death. J Neurosci Res 80:655–666CrossRefGoogle Scholar
  126. Wierzbicki M, Sawosz E, Grodzik M, Hotowy A, Prasek M, Jaworski S, Sawosz F, Chwalibog A (2013) Carbon nanoparticles downregulate expression of basic fibroblast growth factor in the heart during embryogenesis. Int J Nanomedicine 8:3427Google Scholar
  127. Wilson MR, Lightbody JH, Donaldson K, Sales J, Stone V (2002) Interactions between ultrafine particles and transition metals in vivo and in vitro. Toxicol Appl Pharmacol 184:172–179CrossRefGoogle Scholar
  128. Xia T, Kovochich M, Brant J, Hotze M, Sempf J, Oberley T, Sioutas C, Yeh JI, Wiesner MR, Nel AE (2006) Comparison of the abilities of ambient and manufactured nanoparticles to induce cellular toxicity according to an oxidative stress paradigm. Nano Lett 6:1794–1807CrossRefGoogle Scholar
  129. Xia T, Kovochich M, Liong M, Zink JI, Nel AE (2007) Cationic polystyrene nanosphere toxicity depends on cell-specific endocytic and mitochondrial injury pathways. ACS Nano 2:85–96CrossRefGoogle Scholar
  130. Xiao-feng P, Qiang Z, Bao-qing Z, Zhi-Hong L (2006) Biological Effects of the Carbon Nanotubes, Engineering in Medicine and Biology Society, 2005. IEEE-EMBS 2005. 27th Annual International Conference of the. IEEE, pp. 1240–1243Google Scholar
  131. Yemisci M, Gursoy-Ozdemir Y, Vural A, Can A, Topalkara K, Dalkara T (2009) Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery. Nat Med 15:1031CrossRefGoogle Scholar
  132. Yuan Y, Wang X, Jia G, Liu J-H, Wang T, Gu Y, Yang S-T, Zhen S, Wang H, Liu Y (2010) Pulmonary toxicity and translocation of nanodiamonds in mice. Diam Relat Mater 19:291–299CrossRefGoogle Scholar
  133. Zelko IN, Mariani TJ, Folz RJ (2002) Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med 33:337–349CrossRefGoogle Scholar
  134. Zhen X, Ng WC, Tong YW, Dai Y, Neoh KG, Wang C-H (2017) Toxicity assessment of carbon black waste: a by-product from oil refineries. J Hazard Mater 321:600–610CrossRefGoogle Scholar
  135. Zinabadinova S, Lavrinenko V, Kaminsky R, Korsak A, Sokurenko L, Chaikovsky Y (2018) Effects of technogenic pollutants on chicken embryos. Current Issues in Pharmacy and Medical Sciences 31:34–38CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Dalia H. Samak
    • 1
  • Yasser S. El-Sayed
    • 1
  • Hazem M. Shaheen
    • 2
  • Ali H. El-Far
    • 3
  • Mohamed E. Abd El-Hack
    • 4
  • Ahmed E. Noreldin
    • 5
  • Karima El-Naggar
    • 6
  • Sameh A. Abdelnour
    • 7
  • Essa M. Saied
    • 8
  • Hesham R. El-Seedi
    • 9
    • 10
  • Lotfi Aleya
    • 11
  • Mohamed M. Abdel-Daim
    • 12
  1. 1.Department of Veterinary Forensic Medicine and Toxicology, Faculty of Veterinary MedicineDamanhour UniversityDamanhourEgypt
  2. 2.Department of Pharmacology, Faculty of Veterinary MedicineDamanhour UniversityDamanhourEgypt
  3. 3.Department of Biochemistry, Faculty of Veterinary MedicineDamanhour UniversityDamanhourEgypt
  4. 4.Department of Poultry, Faculty of AgricultureZagazig UniversityZagazigEgypt
  5. 5.Department of Histology and Cytology, Faculty of Veterinary MedicineDamanhour UniversityDamanhourEgypt
  6. 6.Department of Nutrition and Veterinary Clinical Nutrition, Faculty of Veterinary MedicineAlexandria UniversityEdfinaEgypt
  7. 7.Department of Animal Production, Faculty of AgricultureZagazig UniversityZagazigEgypt
  8. 8.Department of Chemistry, Faculty of ScienceSuez Canal UniversityIsmailiaEgypt
  9. 9.Department of Chemistry, Faculty of ScienceMenoufia UniversityShebin El-KomEgypt
  10. 10.Pharmacognosy Group, Department of Medicinal ChemistryUppsala UniversityUppsalaSweden
  11. 11.Chrono-Environment Laboratory, UMR CNRS 6249Bourgogne Franche-Comté UniversityBesançon CedexFrance
  12. 12.Pharmacology Department, Faculty of Veterinary MedicineSuez Canal UniversityIsmailiaEgypt

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