Surface area of carbon-based nanoparticles prevails on dispersion for growth inhibition in amphibians

The attractive properties of carbon-based nanoparticles such as graphene and its derivatives or carbon nanotubes lead to their use in many application fields, whether they are raw or functionalized, such as oxidized. These particles may finally contaminate the aquatic compartment, which is a major receptacle of pollutants. The study of their impact on aquatic organisms is thus essential. At the nano scale, recent studies have highlighted that specific surface area should be used as the most relevant descriptor of toxicity instead of the conventional mass concentration. By using a dose-response model, this work compares the chronic toxicity observed on Xenopus laevis larvae after 12-day in vivo exposure to raw, oxidized carbon allotropes, or in the presence of chemical dispersant. We show that chemical dispersion does not influence the observed chronic toxicity, whether it is through surface chemistry (oxidation state) or through the addition of a dispersant. The biological hypothesis leading to growth inhibition are discussed. Finally, these results confirm that surface area is the more suited metric unit describing growth inhibition.

[1]  Christophe Laplanche,et al.  Surface Area of Carbon Nanoparticles: A Dose Metric for a More Realistic Ecotoxicological Assessment. , 2016, Nano letters.

[2]  G. Lespes,et al.  Size characterization of the associations between carbon nanotubes and humic acids in aqueous media by asymmetrical flow field-flow fractionation combined with multi-angle light scattering. , 2012, Chemosphere.

[3]  J. Heyder,et al.  Instillation of Six Different Ultrafine Carbon Particles Indicates a Surface Area Threshold Dose for Acute Lung Inflammation in Mice , 2005, Environmental health perspectives.

[4]  E. Abellán,et al.  Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver. , 2004, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[5]  Emmanuel Flahaut,et al.  Multi-walled carbon nanotubes, natural organic matter, and the benthic diatom Nitzschia palea: “A sticky story” , 2015, Nanotoxicology.

[6]  Richard D Handy,et al.  Toxicity of single walled carbon nanotubes to rainbow trout, (Oncorhynchus mykiss): respiratory toxicity, organ pathologies, and other physiological effects. , 2007, Aquatic toxicology.

[7]  Emmanuel Flahaut,et al.  Higher dispersion efficacy of functionalized carbon nanotubes in chemical and biological environments. , 2010, ACS nano.

[8]  Quan Wang,et al.  A review on applications of carbon nanotubes and graphenes as nano-resonator sensors , 2014 .

[9]  J. Dutil,et al.  Metabolic priorities during starvation: enzyme sparing in liver and white muscle of Atlantic cod, Gadus morhua L. , 2003, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[10]  G. Oberdörster,et al.  Nanotoxicology: An Emerging Discipline Evolving from Studies of Ultrafine Particles , 2005, Environmental health perspectives.

[11]  E. Vázquez,et al.  Interaction of graphene-related materials with human intestinal cells: an in vitro approach. , 2016, Nanoscale.

[12]  I. Griffiths.  THE FORM AND FUNCTION OF THE FORE‐GUT IN ANURAN LARVAE (AMPHIBIA, SALIENTIA) WITH PARTICULAR REFERENCE TO THE MANICOTTO GLANDULARE , 2009 .

[13]  Renato Grillo,et al.  Engineered nanoparticles and organic matter: a review of the state-of-the-art. , 2015, Chemosphere.

[14]  M. Feder,et al.  Temperature and the Balance between Aerial and Aquatic Respiration in Larvae of Rana berlandieri and Rana catesbeiana , 1983, Physiological Zoology.

[15]  Hongtao Yu,et al.  Mechanisms of nanotoxicity: Generation of reactive oxygen species , 2014, Journal of food and drug analysis.

[16]  N. Fierer,et al.  The Evolution of Stomach Acidity and Its Relevance to the Human Microbiome , 2015, PloS one.

[17]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[18]  Nicklas Raun Jacobsen,et al.  Bioaccumulation and ecotoxicity of carbon nanotubes , 2013, Chemistry Central Journal.

[19]  A. Rao,et al.  The influence of natural organic matter on the toxicity of multiwalled carbon nanotubes. , 2010, Environmental toxicology and chemistry.

[20]  C. Merino,et al.  Large-scale conversion of helical-ribbon carbon nanofibers to a variety of graphene-related materials , 2016 .

[21]  A. McQuarrie,et al.  Regression and Time Series Model Selection , 1998 .

[22]  Yong Liang,et al.  Oxidative stress and immunotoxicity induced by graphene oxide in zebrafish. , 2016, Aquatic toxicology.

[23]  Dan Du,et al.  Graphene-like 2D nanomaterial-based biointerfaces for biosensing applications. , 2017, Biosensors & bioelectronics.

[24]  Kinam Park,et al.  Combinatorial nanodiamond in pharmaceutical and biomedical applications. , 2016, International journal of pharmaceutics.

[25]  J. Sumpter,et al.  The effect of starvation on growth and plasma growth hormone concentrations of rainbow trout, Oncorhynchus mykiss. , 1991, General and comparative endocrinology.

[26]  E. Flahaut,et al.  Biocompatible polymer-assisted dispersion of multi walled carbon nanotubes in water, application to the investigation of their ecotoxicity using Xenopus laevis amphibian larvae , 2013 .

[27]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[28]  G. Hilken,et al.  Growth of Xenopus laevis under different laboratory rearing conditions. , 1995, Laboratory animals.

[29]  Inhwa Jung,et al.  Colloidal suspensions of highly reduced graphene oxide in a wide variety of organic solvents. , 2009, Nano letters.

[30]  Kai Yang,et al.  In vivo biodistribution and toxicology of functionalized nano-graphene oxide in mice after oral and intraperitoneal administration. , 2013, Biomaterials.

[31]  Huan-Cheng Chang,et al.  In vivo imaging and toxicity assessments of fluorescent nanodiamonds in Caenorhabditis elegans. , 2010, Nano letters.

[32]  C. Laplanche,et al.  Short term exposure to multi-walled carbon nanotubes induce oxidative stress and DNA damage in Xenopus laevis tadpoles. , 2014, Ecotoxicology and environmental safety.

[33]  Emmanuel Flahaut,et al.  Gram-scale CCVD synthesis of double-walled carbon nanotubes. , 2003, Chemical communications.

[34]  W. S. Hummers,et al.  Preparation of Graphitic Oxide , 1958 .

[35]  P. Vikesland,et al.  Moving beyond mass: the unmet need to consider dose metrics in environmental nanotoxicology studies. , 2012, Environmental science & technology.

[36]  Emmanuel Flahaut,et al.  Carbon nanotube ecotoxicity in amphibians: assessment of multiwalled carbon nanotubes and comparison with double-walled carbon nanotubes. , 2010, Nanomedicine.

[37]  W. P. Ball,et al.  Sorption of aqueous Zn[II] and Cd[II] by multiwall carbon nanotubes: the relative roles of oxygen-containing functional groups and graphenic carbon. , 2010, Langmuir : the ACS journal of surfaces and colloids.

[38]  Abha Misra.  Carbon Nanotubes for Sensing Applications , 2016 .

[39]  G. Lowry,et al.  Towards a definition of inorganic nanoparticles from an environmental, health and safety perspective. , 2009, Nature nanotechnology.

[40]  Jiayan Luo,et al.  Graphene oxide as surfactant sheets , 2010 .

[41]  Agnes B Kane,et al.  Adsorption of essential micronutrients by carbon nanotubes and the implications for nanotoxicity testing. , 2008, Small.

[42]  Miss A.O. Penney.  (b) , 1974, The New Yale Book of Quotations.

[43]  Omer Kalayci,et al.  Oxidative Stress and Antioxidant Defense , 2012, The World Allergy Organization journal.

[44]  Kun Yang,et al.  Adsorption of fulvic acid by carbon nanotubes from water. , 2009, Environmental pollution.

[45]  Xiaoxin L Chen,et al.  A Zebrafish Model for Studies on Esophageal Epithelial Biology , 2015, PloS one.

[46]  Emmanuel Flahaut,et al.  Characterisation and in vivo ecotoxicity evaluation of double-wall carbon nanotubes in larvae of the amphibian Xenopus laevis. , 2008, Aquatic toxicology.

[47]  G. G. Stokes.  "J." , 1890, The New Yale Book of Quotations.

[48]  Pedro J J Alvarez,et al.  Effect of soil sorption and aquatic natural organic matter on the antibacterial activity of a fullerene water suspension , 2008, Environmental toxicology and chemistry.

[49]  P. Lukanov,et al.  Double-walled carbon nanotubes: Quantitative purification assessment, balance between purification and degradation and solution filling as an evidence of opening , 2014 .

[50]  Shuk Han Cheng,et al.  Acute and long-term effects after single loading of functionalized multi-walled carbon nanotubes into zebrafish (Danio rerio). , 2009, Toxicology and applied pharmacology.

[51]  J. Pairon,et al.  Adverse effects of industrial multi-walled carbon nanotubes on human pulmonary cells , 2010 .

[52]  L. Gauthier.  The amphibian micronucleus test, a model for in vivo monitoring of genotoxic aquatic pollution , 1996 .

[53]  M. Elimelech,et al.  Environmental applications of carbon-based nanomaterials. , 2008, Environmental science & technology.

[54]  Menachem Elimelech,et al.  Influence of biomacromolecules and humic acid on the aggregation kinetics of single-walled carbon nanotubes. , 2010, Environmental science & technology.

[55]  M. Prato,et al.  Exfoliation of graphite with triazine derivatives under ball-milling conditions: preparation of few-layer graphene via selective noncovalent interactions. , 2014, ACS nano.

[56]  W. P. Ball,et al.  Influence of surface oxides on the colloidal stability of multi-walled carbon nanotubes: a structure-property relationship. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[57]  Yang Wang,et al.  Biomedical applications of the graphene-based materials. , 2016, Materials science & engineering. C, Materials for biological applications.

[58]  Petr Král,et al.  Sandwiched graphene--membrane superstructures. , 2010, ACS nano.

[59]  Agnes B Kane,et al.  Biological interactions of graphene-family nanomaterials: an interdisciplinary review. , 2012, Chemical research in toxicology.

[60]  Sławomir Boncel,et al.  Interactions of carbon nanotubes with aqueous/aquatic media containing organic/inorganic contaminants and selected organisms of aquatic ecosystems--A review. , 2015, Chemosphere.

[61]  Eric A. Grulke,et al.  Dispersion of Carbon Nanotubes in Liquids , 2003 .

[62]  K. Hoff,et al.  Xenopus laevis larvae (Amphibia, Anura) as model suspension feeders , 1982, Hydrobiologia.

[63]  Kun Yang,et al.  Effect of humic acids on physicochemical property and Cd(II) sorption of multiwalled carbon nanotubes. , 2012, Chemosphere.

[64]  Emmanuel Flahaut,et al.  Examining the impact of multi-layer graphene using cellular and amphibian models , 2016 .

[65]  E. Tardy,et al.  Biomonitoring of the genotoxic potential (micronucleus assay) and detoxifying activity (EROD induction) in the River Dadou (France), using the amphibian Xenopus laevis. , 2003, The Science of the total environment.

[66]  E. Petersen,et al.  Influence of polyethyleneimine graftings of multi-walled carbon nanotubes on their accumulation and elimination by and toxicity to Daphnia magna. , 2011, Environmental science & technology.

[67]  M. Feder,et al.  Aerial Versus Aquatic Oxygen Consumption in Larvae of the Clawed Frog, Xenopus Laevis , 1984 .