Advertisement

Environmental Science and Pollution Research

, Volume 26, Issue 9, pp 9193–9202 | Cite as

Assessment of acute toxicity and cytotoxicity of fluorescent markers produced by cardanol and glycerol, which are industrial waste, to different biological models

  • Bruno Ivo Pelizaro
  • Felipe Camargo Braga
  • Bruno do Amaral Crispim
  • Luiz Guilherme Maiolino Lacerda de Barros
  • Lucas Roberto Pessatto
  • Edwin José Torres Oliveira
  • Juliana Miron Vani
  • Antonio Pancrácio de Souza
  • Alexeia Barufatti Grisolia
  • Andréia Conceição Milan Brochado Antoniolli-Silva
  • Dênis Pires de Lima
  • Jeandre Augusto dos Santos Jaques
  • Adilson BeatrizEmail author
  • Rodrigo Juliano OliveiraEmail author
Research Article
  • 154 Downloads

Abstract

The amphyphylic triazoanilines recently synthesized 1-(4-(3-aminophenyl)-1H-1,2,3- triazole-1-yl)-3-(3-pentadecylphenoxy)propan-2-ol (1) and 1-(4-(4-aminophenyl)-1H- 1,2,3-triazole-1-yl)-3-(3-pentadecylphenoxy)propan-2-ol (2), synthesized from cardanol and glycerol, have photophysical properties which allow their use in the development of fluorescent biomarkers with applicability in the biodiesel quality control. Based on this, the present research evaluated the toxic effects of both compounds in different biological models through the investigation of survival and mortality percentages as a measure of acute toxicity on Daphnia similis and Oreochromis niloticus, larvicidal assay against Aedes aegypti, and cytotoxic activity on mammary cells. Results demonstrate that these triazoanilines 1 and 2 have shown low acute toxicity to the biological models investigated in this study up to the following concentrations: 4.0 mg L-1 (D. similis), 4.0 mg L-1 (A. aegypti larvae), 1.0 mg L-1 (O. niloticus), and 1.0 mg mL-1 (mammary cells). This fact suggests the potential for safe use of compounds 1 and 2 as fluorescent markers for the monitoring of biodiesel quality, even in the case of environmental exposure. Besides all of that, the reuse of cardanol and glycerol, both industrial wastes, favors the maintenance of environmental health and is in agreement with the assumptions of green chemistry.

Graphical abstract

Keywords

Ecotoxicity Daphnia similis Aedes aegypti Oreochromis niloticus Mammary cells Biofuels 

Notes

Funding information

This study was sponsored by Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul – FUNDECT, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance code 001, and Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq.

Compliance with ethical standards

All procedures and protocols followed approved guidelines for the ethical treatment of vertebrate animals, according to the Ethics Committee in Animals Experimentation from the Federal University of Grande Dourados under protocol # 09/2017-2.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. ABNT - Associação Brasileira de Normas Técnicas (2004) NBR 12713: Ecotoxicologia aquática – Toxicidade aguda – Método de ensaio com Daphnia spp (Cladocera, Crustacea). 21 pGoogle Scholar
  2. ABNT - Associação Brasileira de Normas Técnicas (2016) NBR 15088: Ecotoxicologia aquática - Toxicidade aguda - Método de ensaio com peixes (Cyprinidae). 25 pGoogle Scholar
  3. Afifi M, Saddick S, Abu Zinada OA (2016) Toxicity of silver nanoparticles on the brain of Oreochromis niloticus and Tilapia zillii. Saudi J Biol Sci 23:754–760.  https://doi.org/10.1016/j.sjbs.2016.06.008 CrossRefGoogle Scholar
  4. Bhanu PV, Pankaj KK (2017) Monitoring petroleum fuel adulteration: a review of analytical methods. Trends Anal Chem 92:1–11.  https://doi.org/10.3390/s18051551 CrossRefGoogle Scholar
  5. Barnsley JE, Shillito GE, Larsen CB, Van der Salm H, Wang LE, Lucas NT, Gordon KC (2016) Benzo [c][1,2,5] thiadiazole donor−acceptor dyes: a synthetic, spectroscopic, and computational study. J Phys Chem A 120:1853–1866.  https://doi.org/10.1021/acs.jpca.6b00447 CrossRefGoogle Scholar
  6. Beatriz A, Araújo YJK, Lima DP (2011) Glicerol: um breve histórico e aplicação em sínteses estereosseletivas. Quim Nova 2:306–319.  https://doi.org/10.1590/S0100-40422011000200025 CrossRefGoogle Scholar
  7. Beatriz A, De Lima D, Souza AP, Galdino DT, Silva ECR, Ito FM, Gomes RS, Arruda EJ. Processo de produção e uso de misturas de surfactantes iônicos do líquido da casca da castanha do caju e do óleo de mamoma como larvicida (2015); Brasil. Patente: Privilégio de inovação. Número do registro: BR10201500723. Data de depósito: 16/03/2015. Instituição de registro: INPI – Instituto Nacional da Propriedade IndustrialGoogle Scholar
  8. Bendary E, Francis RR, Ali HMG, Sarwat MI, El Hady S (2013) Antioxidant and structure-activity relationships (SARs) of some phenolic and anilines compounds. Ann Agric Sci 58:173–181.  https://doi.org/10.1016/j.aoas.2013.07.002 CrossRefGoogle Scholar
  9. Bluhm K, Heger S, Seiler TB, Hallare AV, Schäffer A, Hollert H (2012) Toxicological and ecotoxicological potencies of biofuels used for the transport sector - a literature review. Energy Environ Sci 5:7381–7392.  https://doi.org/10.1039/c2ee03033k CrossRefGoogle Scholar
  10. Braga FC, Prasad AN, da Silva Gomes R, do Nascimento VA, Oliveira SL, Caires ARL, de Lima DP, Beatriz A (2017) Design, synthesis and fluorescence analysis of potential fluorescent markers based on cardanol and glycerol. Dyes Pigments 141:235–244.  https://doi.org/10.1016/j.dyepig.2017.02.032 CrossRefGoogle Scholar
  11. Brazil (2005) Ministério do Meio Ambiente. Conselho Nacional do Meio Ambiente. Resolução n° 357, de 17 de março de 2005. Dispõe sobre a classificação dos corpos de água e diretrizes para o seu enquadramento, bem com estabelece as condições e padrões de lançamento de efluentes, e dá outras providências. Diário Oficial da União, Brasília, DF, 18 mar. 2005. Seção 1:58–63Google 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 111:131–137.  https://doi.org/10.1016/j.ecoenv.2014.10.005 CrossRefGoogle Scholar
  13. Carvalho GHF, Andrade MA, Araújo CN, Santos ML, Castro NA, Charneau S, Monnerat R, Santana JM, Bastos IMD (2019) Larvicidal and pupicidal activities of eco-friendly phenolic lipid products from Anacardium occidentale nutshell against arbovirus vectors. Environ Sci Pollut Res.  https://doi.org/10.1007/s11356-018-3905-y
  14. Durjava MK, Kolar B, Arnus L, Papa E, Kovarich S, Sahlin U, Peijnenburg W (2013) Experimental assessment of the environmental fate and effects of triazoles and benzotriazole. Atla 41:65–75Google Scholar
  15. Ezzedinne R, Banaw AA, Tovmasyan A, Craik JD, Haberle IB, Benov LT (2013) Effect of molecular characteristics on cellular uptake, subcellular localization,and phototoxicity of Zn (II) N-alkylpyridylporphyrins. J Biol Chem 288:36579–36588.  https://doi.org/10.1074/jbc.M113.511642 CrossRefGoogle Scholar
  16. Fabris C, Soncin M, Jori G, Habluetzel A, Lucantoni L, Sawadogo S, Guidolina L, Coppellottia O (2012) Effects of a new photoactivatable cationic porphyrin on ciliated protozoa and branchiopod crustaceans, potential components of freshwater ecosystems polluted by pathogenic agents and their vectors. Photochem Photobiol Sci 11:294–301.  https://doi.org/10.1039/C1PP05154G CrossRefGoogle Scholar
  17. Fargione J, Hill J, Tilman D, Polasky S, Hawthorne P (2008) Land clearing and the bio-fuel carbon debt. Science 319:1235–1238.  https://doi.org/10.1126/science.1152747 CrossRefGoogle Scholar
  18. Figueira ACB, Oliveira KT, Serra OA (2011) New porphyrins tailored as biodiesel fluorescent markers. Dyes Pigments 91:383–388.  https://doi.org/10.1016/j.dyepig.2011.05.020 CrossRefGoogle Scholar
  19. Garaventa F, Gambardella C, Di Fino A, Pittore M, Faimali M (2010) Swimming speed alteration of Artemia sp. and Brachionus plicatilis as a sub-lethal behavioural end-point for ecotoxicological surveys. Ecotoxicology 19:512–519.  https://doi.org/10.1007/s10646-010-0461-8 CrossRefGoogle Scholar
  20. García JI, Garcia-Marin H, Pires E (2014) Glycerol based solvents: synthesis, properties and applications. Green Chem 16:1007–1033.  https://doi.org/10.1039/C3GC41857J CrossRefGoogle Scholar
  21. Golovanov AA, Odin IS, Bekin VV, Vologzhanina AV, Bushmarinov IS, Zlotskiic SS, Gerasimov YL, Purygind PP (2016) Azolyl-substituted 1,2,3-Triazoles. Russ J Org Chem 52:414–420.  https://doi.org/10.1134/S1070428016030209 CrossRefGoogle Scholar
  22. Heger S, Miaomiao D, Bauer K, Schäffer A, Hollert H (2018) Comparative ecotoxicity of potencial biofuels to water flea (Daphnia magna), zebrafish (Danio rerio) and Chinese hamster (Cricetulus griseus) V79 cells. Sci Total Environ 631-632:216–222.  https://doi.org/10.1016/j.scitotenv.2018.03.028 CrossRefGoogle Scholar
  23. Horton N, Mathew P (2014) Novel use of proliferating cell nuclear antigen as a biomarker of metastatic Cancer Available from: https://digitalcommons.hsc.unt.edu/rad/RAD14/Cancer/14/
  24. Kalligeros S, Zannikos F, Stournas S, Lois E (2003) Fuel adulteration issues in Greece. Energy 28:15–26.  https://doi.org/10.1016/S0360-5442(02)00091-9 CrossRefGoogle Scholar
  25. Kanyathare B, Peiponen KE (2018) Hand-held refractometer-based measurement and excess permittivity analysis method for detection of diesel oils adulterated by kerosene in field conditions. Sensors 18:1551.  https://doi.org/10.3390/s18051551 CrossRefGoogle Scholar
  26. Kos I, Rebouças JS, De Freitas-Silva G, Salvemini D, Vujaskovic Z (2009) Lipophilicity of potente porphyrin- based antioxidants:comparison of ortho and meta isomers of Mn (III) N-alkyl pyridyl porphyrins. Free Radic Biol Med 47:72–78.  https://doi.org/10.1016/j.freeradbiomed.2009.04.002 CrossRefGoogle Scholar
  27. Kozubek A, Tyman JHP (1999) Resorcinolic lipids the natural non-isoprenoid phenolic Amphiphiles and their biological activity. Chem Rev 99:1–25.  https://doi.org/10.1021/cr970464o CrossRefGoogle Scholar
  28. Kozubek A (1995) Determination of octanol/water partition coefficients for long-chain homologs of Orcinol from cereal grains. Acta Biochim Pol 42:247–252.  https://doi.org/10.1016/j.foodchem.2007.12.011 CrossRefGoogle Scholar
  29. Kumar NP, Nekkanti S, Kumari SS, Sharma P, Shankaraiah N (2017) Design and synthesis of 1,2,3-triazolo-phenanthrene hybrids as cytotoxic agents. Bioorg Med Chem Letters 27:2369–2376.  https://doi.org/10.1016/j.bmcl.2017.04.022 CrossRefGoogle Scholar
  30. Lakomska I, Hoffmann K, Wojtczak A, Sitkowski J, Maj E, Wietrzyk J (2014) Cytotoxic malonate platinum (II) complexes with 1,2,4-triazolo[1,5-α] pyrimidine derivatives: structural characterization and mechanism of the suppression of tumor cell growth. J Inorg Biochem 141:188–197.  https://doi.org/10.1016/j.jinorgbio.2014.08.005 CrossRefGoogle Scholar
  31. Larsen PS, Madsen CV, Riisgård HU (2008) Effect of temperature and viscosity on swimming velocity of the copepod Acartia tonsa: brine shrimp Artemia salina and rotifer Brachionus plicatilis. AquatBiol 4:47–54.  https://doi.org/10.3354/ab00093 CrossRefGoogle Scholar
  32. Lee HL, Er HM, Radhakrishnan AK (2009) In vitro anti-proliferative and antioxidante activities of stem extracts of pereskia bleo (Kunth) DC (Cactaceae). Malaysian J Sci 28:225–239.  https://doi.org/10.22452/mjs.vol28no3.1 CrossRefGoogle Scholar
  33. Li X, Lin Y, Yuan Y, Liu K, Qian X (2011) Novel efficient anticancer agents and DNA-intercalators of 1,2,3-triazol-1,8-naphthalimides: design, synthesis, and biological activity. Tetrahedron 67:2299–2304.  https://doi.org/10.1016/j.tet.2011.01.063 CrossRefGoogle Scholar
  34. Libralato G, Prato E, Migliore L, Cicero AM, Manfra L (2016) A review of toxicity testing protocols and endpoints with Artemia spp. Ecol Indic 69:35–49.  https://doi.org/10.1016/j.ecolind.2016.04.017 CrossRefGoogle Scholar
  35. Linsinger T, Koomen G, Emteborg H, Roebben G, Kramer G, Lamberty A (2004) Validation of the European Union’s reference method for the determination of solvent yellow 124 in gas oil and kerosene. Energy Fuel 18:1851–1854 b) Krutak JJ, Cushaman MR, Waever MA. US Patent No 5525516, 1996 c) Friswell MR. US Patent No. 5156653, 1992.  https://doi.org/10.1021/ef049820d
  36. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65(1–2):55–63CrossRefGoogle Scholar
  37. OECD. OECD 203 fish acute toxicity test. OECD guidelines for the testing of chemicals, Section 2, 1992:10Google Scholar
  38. OECD. OECD 202 Daphnia sp. Acute immobilisation test. OECD guidelines for the testing of chemicals, Section 6, 2004Google Scholar
  39. Ordoudi SA, Tsimidou MZ, Vafiadis AP, BakalBassis EG (2006) Structure-DPPH. Scavenging activity relationships: parallel study of catechol and guaiacol acid derivatives. J Agric Food Chem 54:5763–5768.  https://doi.org/10.1021/jf060132x CrossRefGoogle Scholar
  40. Pang YP, Brimijoin S, Ragsdale DW, Zhu KY, Suranyi R (2012) Novel and viable acetylcholinesterase target site for developing effective and environmentally safe insecticides. Curr Drug Targets 13:471–482CrossRefGoogle Scholar
  41. Perales E, García JI, Pires E, Aldea L, Lomba L, Giner B (2017) Ecotoxicity and QSAR studies of glycerol ethers in Daphnia magna. Chemosphere 183:277–285.  https://doi.org/10.1016/j.chemosphere.2017.05.107 CrossRefGoogle Scholar
  42. Pimentel MF, Pires D, Lima D, Martins LR, Beatriz A, Santaella ST et al (2009) Ecotoxicological analysis of cashew nut industry effluents, specifically two of its major phenolic components, cardol and cardanol. Pan-Am J Aquat Sci 4:363–368Google Scholar
  43. Puangmalee S, Petsom A, Thamyongkit PA (2009) Porphyrin derivative from cardanol as a diesel fluorescent marker. Dyes Pigments 82:26–30.  https://doi.org/10.1016/j.dyepig.2008.10.015 CrossRefGoogle Scholar
  44. Schweich LDC, Oliveira EJTD, Pesarini JR, Hermeto LC, Camassola M, Nardi NB et al (2017) All-trans retinoic acid induces mitochondria-mediated apoptosis of human adipose-derived stem cells and affects the balance of the adipogenic differentiation. Biomed Pharmacother 96:1267–1274.  https://doi.org/10.1007/s11356-017-8662-9 CrossRefGoogle Scholar
  45. Shemesh A, Kundu K, Peleg R, Yossef R, Kaplanov I, Ghosh S, Khrapunsky Y, Gershoni-Yahalom O, Rabinski T, Cerwenka A, Atlas R, Porgador A (2018) NKp44-derived peptide binds proliferating cell nuclear antigen and mediates tumor cell death. Front Immunol 9(1114).  https://doi.org/10.3389/fimmu.2018.01114
  46. Stasiuk M, Kozubek A (2010) “Biological activity of phenolic lipids”, Birkhäuser Verlag, Based/Switzerland Cell Mol Life Sci 67:841–860.  https://doi.org/10.1007/s00018-009-0193-1
  47. Su N-N, Xiong LX, Yu SJ, Zhang X, Cui C, Li ZM, Zhao WG (2013) Larvicidal activity and click synthesis of 2-Alkoxyl-2-(1,2,3-Triazole-1-yl) acetamide library. Comb Chem High Throughput Screen 16:484–493.  https://doi.org/10.2174/1386207311316060009 CrossRefGoogle Scholar
  48. Tyman JHP (2001) The chemistry and biochemistry of anarcardic acids. Recent research in lipids. Transworld Res 5:125–145Google Scholar
  49. Vani JM, Monreal MTFD, Auharek SA, Cunha-Laura AL, de Arruda EJ, Lima AR, da Silva CM, Antoniolli-Silva ACMB, de Lima DP, Beatriz A, Oliveira RJ (2018) The mixture of cashew nut shell liquid and castor oil results in an efficient larvicide against Aedes aegypti that does not alter embryo-fetal development, reproductive performance or DNA integrity. PLoS One 13(3):e0193509.  https://doi.org/10.1371/journal.pone.0193509 CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Bruno Ivo Pelizaro
    • 1
    • 2
  • Felipe Camargo Braga
    • 3
  • Bruno do Amaral Crispim
    • 4
  • Luiz Guilherme Maiolino Lacerda de Barros
    • 5
  • Lucas Roberto Pessatto
    • 1
    • 6
  • Edwin José Torres Oliveira
    • 1
    • 6
  • Juliana Miron Vani
    • 7
  • Antonio Pancrácio de Souza
    • 8
  • Alexeia Barufatti Grisolia
    • 4
  • Andréia Conceição Milan Brochado Antoniolli-Silva
    • 1
    • 7
  • Dênis Pires de Lima
    • 3
  • Jeandre Augusto dos Santos Jaques
    • 2
  • Adilson Beatriz
    • 3
    Email author
  • Rodrigo Juliano Oliveira
    • 1
    • 6
    • 7
    Email author
  1. 1.Stem Cell, Cell Therapy and Toxicological Genetics Research Centre (CeTroGen)“Maria Aparecida Pedrossian” University Hospital, Brazilian Hospital Services Company (EBSERH)Campo GrandeBrazil
  2. 2.Master’s Program in Pharmacy, Faculty of Pharmaceutical Sciences, Food and Nutrition – FACFANFederal University of Mato Grosso do SulCampo GrandeBrazil
  3. 3.Chemistry Institute – INQUI, SINTMOL LaboratoryFederal University of Mato Grosso do SulCampo GrandeBrazil
  4. 4.Laboratory of Ecotoxicology and Genotoxicity (LECOGEN), Faculty of Biological and Environmental Sciences – FCBAFederal University of Grande DouradosDouradosBrazil
  5. 5.Laboratory of Environmental Quality, Faculty of Engineering Architecture and Urbanism and Geography – FAENGFederal University of Mato Grosso do SulCampo GrandeBrazil
  6. 6.Graduate Programme in Genetics and Molecular Biology, Department of General BiologyState University of Londrina (UEL)LondrinaBrazil
  7. 7.Graduate Programme in Health and Development in the Central-West Region, School of Medicine (FAMED) “Dr. Hélio Mandetta”Federal University of Mato Grosso do Sul (UFMS)Campo GrandeBrazil
  8. 8.Biosciences Institute- INBIOFederal University of Mato Grosso do SulCampo GrandeBrazil

Personalised recommendations