Abstract
The use of insecticides to control vector mosquitoes is still a necessary practice in many countries. Due to the negative impacts and increasing mosquito resistance to synthetic insecticides, environmentally friendly alternatives are needed. In this context, products derived from the technical cashew nut shell liquid (tCNSL) have shown promise as larvicides to control Aedes aegypti. Our objective was to develop 5 new self-emulsifiable bioactive derivatives from partial tCNSL neutralization reactions with 2 inorganic and 3 organic bases, and to determine their larvicidal activities against Ae. aegypti. We also evaluated their antimicrobial activities and ecotoxicological potential. All five bioactive derivatives of tCNSL had larvicidal activity against Ae. aegypti. Four bioactive derivatives had some bacteriostatic activity, but none had fungicidal activity. Although the five bioactive derivatives are toxic against aquatic organisms, in general they were less toxic against Pseudokirchneriella subcapitata, Daphnia similis, and Oreochromis niloticus, than the larvicides recommended by World Health Organization (WHO). Considering the development of low-cost multifunctional bioproducts it is suggested that the bioactive derivative obtained from tCNSL that was partially neutralized whit NaOH (tCNSLNa) can be incorporated into sanitizing products for Ae. aegypti domestic control.
Graphical Abstract
Similar content being viewed by others
Data Availability
The analyzes developed and the data generated from this research are included in this article, in addition to containing supplementary information (appendix).
Code Availability
Not applicable.
References
Chapagain, B.P., Saharan, V., Wiesman, Z.: Larvicidal activity of saponins from Balanites aegyptiaca callus against Aedes aegypti mosquito. Bioresour. Technol. 99, 1165–1168 (2008). https://doi.org/10.1016/j.biortech.2007.02.023
Benelli, G., Murugan, K., Panneerselvam, C., Madhiyazhagan, P., Conti, B., Nicoletti, M.: Old ingredients for a new recipe? Neem cake, a low-cost botanical by-product in the fight against mosquito-borne diseases. Parasitol. Res. 114, 391–397 (2015). https://doi.org/10.1007/s00436-014-4286-x
Bardach, A.E., García-Perdomo, H.A., Alcaraz, A., López, E.T., Gándara, R.A.R., Ruvinsky, S., Ciapponi, A.: Interventions for the control of Aedes aegypti in Latin America and the Caribbean: systematic review and meta-analysis. Trop. Med. Int. Health 24, 530–552 (2019). https://doi.org/10.1111/tmi.13217
Lucia, A., Toloza, A.C., Fanucce, M., Fernández-Peña, L., Ortega, F., Rubio, R.G., Coviella, C., Guzmán, E.: Nanoemulsions based on thymol-eugenol mixtures: characterization, stability and larvicidal activity against Aedes aegypti. Bull. Insectol. 73, 153–160 (2020)
Benelli, G., Jeffries, C.L., Walker, T.: Biological control of mosquito vectors: past, present, and future. Insects 7, 52 (2016). https://doi.org/10.3390/insects7040052
Benelli, G., Duggan, M.F.: Management of arthropod vector data–social and ecological dynamics facing the one health perspective. Acta Trop. 182, 80–91 (2018). https://doi.org/10.1016/j.actatropica.2018.02.015
Jorge, M.R., Crispim, B.A., Merey, F.M., Barufatti, A., Cabrini, I., Dantas, F.G.S., Oliveira, K.M.P., Kummrow, F., Beatriz, A., Santos, T., Dias, D., Ventura, J., Nogueira, C.R., Gomes, R.S., Arruda, E.J.: Sulphonates’ mixtures and emulsions obtained from technical cashew nut shell liquid and cardanol for control of Aedes aegypti (Diptera: Culicidae). Environ. Sci. Pollut. Res. 27, 27870–27884 (2020). https://doi.org/10.1007/s11356-020-08998-5
Lucia, A., Toloza, A.C., Guzmán, E., Ortega, F., Rubio, R.G.: Novel polymeric micelles for insect pest control: encapsulation of essential oil monoterpenes inside a triblock copolymer shell for head lice control. PeerJ 5, e3171 (2017). https://doi.org/10.7717/peerj.3171
Lomonaco, D., Mele, G., Mazzetto, S.E.: Cashew nutshell liquid (CNSL): from an agro-industrial waste to a sustainable alternative to petrochemical resources. In: Anilkumar, P. (ed.) Cashew nut shell liquid, pp. 19–38. Springer, Heidelberg (2017)
Guissoni, A.C.P., Silva, I.G., Geris, R., Cunha, L.C.D., Silva, H.H.G.D.: Atividade larvicida de Anacardium occidentale como alternativa ao controle de Aedes aegypti e sua toxicidade em Rattus norvegicus. Rev. Bras. Plantas Med. 15, 363–367 (2013). https://doi.org/10.1590/S1516-05722013000300008
Dourado, D.M., Rosa, A.C., Porto, K.R.A., Roel, A.R., Cardoso, C.A.L., Favero, S., Matias, R.: Effects of cashew nut shell liquid (CNSL) component upon Aedes aegypti Lin. (Diptera: Culicidae) larvae’s midgut. Afr. J. Biotechnol. 14, 829–834 (2015). https://doi.org/10.5897/AJB2014.14347
Lomonaco, D., Santiago, G.M.P., Ferreira, Y.S., Arriaga, Â.M.C., Mazzetto, S.E., Mele, G., Vasapollo, G.: Study of technical CNSL and its main components as new green larvicides. Green Chem. 11, 31–33 (2009). https://doi.org/10.1039/B811504D
Balachandran, V.S., Jadhav, S.R., Vemula, P.K., John, G.: Recent advances in cardanol chemistry in a nutshell: from a nut to nanomaterials. Chem. Soc. Rev. 42, 427–438 (2013). https://doi.org/10.1039/C2CS35344J
Mgaya, J., Shombe, G.B., Masikane, S.C., Mlowe, S., Mubofu, E.B., Revaprasadu, N.: Cashew nut shell: a potential bio-resource for the production of bio-sourced chemicals, materials and fuels. Green Chem. 21, 1186–1201 (2019). https://doi.org/10.1039/C8GC02972E
Torres, R.C., Garbo, A.G., Walde, R.Z.M.L.: Characterization and bioassay for larvicidal activity of Anacardium occidentale (cashew) shell waste fractions against dengue vector Aedes aegypti. Parasitol. Res. 114, 3699–3702 (2015). https://doi.org/10.1007/s00436-015-4598-5
Almanzor, B.L.J., Ho, H.T., Carvajal, T.M.: Ecdysis period and rate deviations of dengue mosquito vector, Aedes aegypti reared in different artificial water-holding containers. J. Vector Borne Dis. 53, 37–45 (2016)
Dhar-Chowdhury, P., Haque, C.E., Lindsay, R., Hossain, S.: Socioeconomic and ecological factors influencing Aedes aegypti prevalence, abundance, and distribution in Dhaka, Bangladesh. Am. J. Trop. Med. Hyg. 94, 1223–1233 (2016). https://doi.org/10.4269/ajtmh.15-0639
Kumar, G., Singh, R.K., Pande, V., Dhiman, R.C.: Impact of container material on the development of Aedes aegypti larvae at different temperatures. J. Vector Borne. Dis. 53, 144–148 (2016)
Lucia, A., Girard, C., Fanucce, M., Coviella, C., Rubio, R.G., Ortega, F., Guzmán, E.: Development of an environmentally friendly larvicidal formulation based on essential oil compound blend to control Aedes aegypti larvae: correlations between physicochemical properties and insecticidal activity. ACS Sustain. Chem. Eng. 8, 10995–11006 (2020). https://doi.org/10.1021/acssuschemeng.0c03778
Lucia, A., Guzmán, E.: Emulsions containing essential oils, their components or volatile semiochemicals as promising tools for insect pest and pathogen management. Adv. Colloid Interface Sci. 287, 102330 (2021). https://doi.org/10.1016/j.cis.2020.102330
Laurens, A., Fourneau, C., Hocquemiller, R., Cavé, A., Bories, C., Loiseau, P.M.: Antivectorial activities of cashew nut shell extracts from Anacardium occidentale L. Phytother. Res. 11, 145–146 (1997). https://doi.org/10.1002/(SICI)1099-1573(199703)11:2%3c145::AID-PTR40%3e3.0.CO;2-%23
Matos, J.E.X., Silva, F.J.A., Vieira, P.B.: Solventes para extração do líquido da castanha de caju (LCC) e compatibilidade ambiental. Rev. Technol. 29, 101–109 (2008)
WHO—World Health Organization. Guidelines for laboratory and field testing of mosquito larvicides. https://apps.who.int/iris/handle/10665/69101 (2005). Accessed 25 March 2020.
Anjolette, A.F.F., Macoris, M.L.G.: Técnicas para manutenção de Aedes aegypti em laboratório. BEPA 156, 19–29 (2016)
R Core Team: R studio: integrated development for R. R Studio Inc., Boston (2019)
WHO—World Health Organization. Dengue guidelines for diagnosis, treatment, prevention and control: new edition. https://apps.who.int/iris/handle/10665/44188 (2009). Accessed 25 March 2020.
CLSI—Clinical and Laboratory Standards Institute: Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard, 9th edn. CLSI, Wayne (2012)
CLSI: CLSI document M07–A9. Clinical and Laboratory Standards Institute, Wayne (2012)
CLSI—Clinical and Laboratory Standards Institute: Reference method for broth dilution antifungal susceptibility testing of yeasts, approved standard. CLSI document M27–A3, 3rd edn. Clinical and Laboratory Standards Institute, Wayne (2008)
Bagiu, R.V., Vlaicu, B., Butnariu, M.: Chemical composition and in vitro antifungal activity screening of the Allium ursinum L. (Liliaceae). Int. J. Mol. Sci. 13, 1426–1436 (2012). https://doi.org/10.3390/ijms13021426
OECD—Organisation for Economic Cooperation and Development: Test No. 201: guideline for testing of chemicals, freshwater alga and cyanobacteria growth inhibition. OECD guidelines for test chemicals. Associação Brasileira de Normas Técnicas, Rio de Janeiro (2011)
ABNT—Associação Brasileira de Normas Técnicas: ABNT NBR 12648—Ecotoxicologia aquática—Toxicidade crônica—Método de ensaio com algas (Chlorophyceae). Associação Brasileira de Normas Técnicas, Rio de Janeiro (2018)
ABNT—Associação Brasileira de Normas Técnicas: ABNT NBR 12713—Ecotoxicologia aquática—Toxicidade aguda—Método de ensaio com Daphnia spp (Crustacea, Cladocera). Associação Brasileira de Normas Técnicas, Rio de Janeiro (2016)
OECD—Organisation for Economic Cooperation and Development: Test No. 202: Daphnia sp. acute immobilisation test. OECD guidelines for test chemicals. OECD, Paris (2004)
OECD—Organisation for Economic Cooperation and Development: Test No. 203: fish, acute toxicity test. OECD guidelines for test chemicals. OECD, Paris (1992)
ABNT—Associação Brasileira de Normas Técnicas: ABNT NBR 15088—Ecotoxicologia aquática—Toxicidade aguda—Método de ensaio com peixes (Cyprinidae). Associação Brasileira de Normas Técnicas, Rio de Janeiro (2016)
Norberg-King, T.J.: A linear interpolation method for sublethal toxicity: the inhibition concentration (ICp) approach. Version 2.0. National Effluent Toxicity Assessment Center Technical Report 03–93 (1993)
Hamilton, M.A., Russo, R.C., Thurston, R.V.: Trimmed Spearman-Karber method for estimating median lethal concentrations in toxicity bioassays. Environ. Sci. Technol. 11, 714–719 (1977). https://doi.org/10.1021/es60130a004
OECD—Organisation for Economic Cooperation and Development: Harmonised integrated classification system for human health and environmental hazards of chemical substances and mixtures. OECD series on testing and assessment No. 33. OECD, Paris (2002)
Komalamisra, N., Trongtokit, Y., Rongsriyam, Y., Apiwathnasorn, C.: Screening for larvicidal activity in some Thai plants against four mosquito vector species. Southeast Asian J. Trop. Med. Public Health 36, 1412–1422 (2005)
Carvalho, G.H.F., Andrade, M.A., Araújo, C.N., Santos, M.L., Castro, N.A., Charneau, S., Monnerat, R., Santana, J.M., Bastos, I.M.D.: Larvicidal and pupicidal activities of eco-friendly phenolic lipid products from Anacardium occidentale nut shell against arbovirus vectors. Environ. Sci. Pollut. Res. 26, 5514–5523 (2019). https://doi.org/10.1007/s11356-018-3905-y
Paiva, D.R., Lima, D.P., Avvari, N.P., Arruda, E.J., Cabrini, I., Marques, M.R., Santos, E.A., Biaggio, F.C., Sangi, D.P., Beatriz, A.: A potent larvicidal agent against Aedes aegypti mosquito from cardanol. An. Acad. Bras. Ciênc. 89, 373–382 (2017). https://doi.org/10.1590/0001-3765201720160615
Lenardão, E.J., Freitag, R.A., Dabdoub, M.J., Batista, A.C.F., Silveira, C.D.C.: “Green Chemistry”: os 12 princípios da química verde e sua inserção nas atividades de ensino e pesquisa. Quím. Nova 26, 123–129 (2003). https://doi.org/10.1590/S0100-40422003000100020
Attanasi, O.A., Berretta, S., Fiani, C., Filippone, P., Mele, G., Saladino, R.: Synthesis and reactions of nitro derivatives of hydrogenated cardanol. Tetrahedron 62, 6113–6120 (2006). https://doi.org/10.1016/j.tet.2006.03.105
Oliveira, M.S.C., Morais, S.M., Magalhães, D.V., Batista, W.P., Vieira, I.G.P., Craveiro, A.A., Manezes, J.E.S.A., Carvalho, A.F.U., Lima, G.P.G.: Antioxidant, larvicidal and antiacetylcholinesterase activities of cashew nut shell liquid constituents. Acta Trop. 117, 165–170 (2011). https://doi.org/10.1016/j.actatropica.2010.08.003
Vani, J.M., Monreal, M.T.F.D., Auharek, S.A., Cunha-Laura, A.L., Arruda, E.J., Lima, A.R., Silva, C.M., Antoniolli-Silva, A.C.M.B., Lima, D.P., Beatriz, A., Oliveira, R.J.: 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, e0193509 (2018). https://doi.org/10.1371/journal.pone.0193509
Kala, S., Sogan, N., Verma, P., Naik, S.N., Agarwal, A., Patanjali, P.K., Kumar, J.: Nanoemulsion of cashew nut shell liquid bio-waste: mosquito larvicidal activity and insights on possible mode of action. S. Afr. J. Bot. 127, 293–300 (2019). https://doi.org/10.1016/j.sajb.2019.10.006
Raraswati, G.R., Sudarsono, S., Mulyaningsih, B.: Larvicidal activity of a mixture of cashew nut shell liquid and water-soluble extract of soap nut fruit (Sapindus rarak DC.) against 3rd instar larvae of Aedes aegypti. Biol. Med. Nat. Prod. Chem. 3, 53–57 (2014). https://doi.org/10.14421/biomedich.2014.32.53-57
Kanehashi, S., Masuda, R., Yokoyama, K., Kanamoto, T., Nakashima, H., Miyakoshi, T.: Development of a cashew nut shell liquid (CNSL)-based polymer for antibacterial activity. J. Appl. Polym. Sci. 132, 42725 (2015). https://doi.org/10.1002/app.42725
Khatib, S.K., Bullón, J., Vivas, J., Bahsas, A., Rosales-Oballos, Y., Marquez, R., Forgiarini, A., Salager, J.L.: Synthesis, characterization, evaluation of interfacial properties and antibacterial activities of dicarboxylate anacardic acid derivatives from cashew nut shell liquid of Anacardium occidentale L. J. Surfact. Deterg. 23, 503–512 (2020). https://doi.org/10.1002/jsde.12384
Ashraf, M.S., Rathinasamy, K.: Antibacterial and anticancer activity of the purified cashew nut shell liquid: implications in cancer chemotherapy and wound healing. Nat. Prod. Res. 32, 2856–2860 (2018). https://doi.org/10.1080/14786419.2017.1380022
Pimentel, M., Lima, D., Martins, L., Beatriz, A., Santaella, S., Costa-Lotufo, L.: Ecotoxicological analysis of cashew nut industry effluents, specifically two of its major phenolic components, cardol and cardanol. Pan-Am. J. Aquat. Sci. 4, 363–368 (2009)
Leite, A.D.S., Dantas, A.F., Oliveira, G.L.D.S., Gomes Júnior, A.L., Lima, S.G., Citó, A.M.G.L., Freitas, R.M., Melo-Cavalcante, A.A.C., Lopes, J.A.D.: Evaluation of toxic, cytotoxic, mutagenic, and antimutagenic activities of natural and technical cashew nut shell liquids using the Allium cepa and Artemia salina bioassays. Biomed. Res. Int. 2015, 626835 (2015). https://doi.org/10.1155/2015/626835
Afsset, A., Assessment, R.: La lutte antivectorielle dans le cadre de l’épidémie de chikungunya sur l’Île de la Réunion. Évaluation des risques et de l’efficacité des produits larvicides. Maisons-Alfort, Paris (2007). https://www.anses.fr/en/system/files/BIOC2006et0008Ra.pdf.
PPDB—Pesticide Properties DataBase. http://sitem.herts.ac.uk/aeru/ppdb/ (2012). Accessed 25 March 2020
WHO—World Health Organization. Who specifications and evaluations for public health pesticides temephos, O,O,O’O’-tetramethyl O,O’-thiodi-p-phenylene bis(phosphorothioate). https://www.who.int/whopes/quality/Temephos_eval_only_June_2011.pdf?ua=1 (2011). Accessed 25 March 2020
Vieira Santos, V.S., Caixeta, E.S., Campos Júnior, E.O.D., Pereira, B.B.: Ecotoxicological effects of larvicide used in the control of Aedes aegypti on nontarget organisms: redefining the use of piriproxifeno. J. Toxicol. Environ. Health Part A 80, 155–160 (2017). https://doi.org/10.1080/15287394.2016.1266721
WHO—World Health Organization. Who specifications and evaluations for public health pesticides diflubenzuron, 1-(4-chlorophenyl)-3-(2,6-difluorobenzoyl)urea. https://www.who.int/pq-vector-control/prequalified-lists/DIFLUBENZURON.pdf?ua=1 (2017). Accessed 25 March 2020
Nagaraju, B., Sudhakar, P., Anitha, A., Haribabu, G., Rathnamma, V.V.: Toxicity evaluation and behavioral studies of fresh water fish Labeo rohita exposed to Rimon. J. Res. Pharm. Biomed. Sci. 2, 722–727 (2011)
Abe, F.R., Machado, A.A., Coleone, A.C., Cruz, C., Machado-Neto, J.G.: Toxicity of diflubenzuron and temephos on freshwater fishes: ecotoxicological assays with Oreochromis niloticus and Hyphessobrycon eques. Water Air Soil Pollut. 230, 77 (2019). https://doi.org/10.1007/s11270-019-4128-7
Acknowledgements
We are grateful for financial support for this study and a postgraduate scholarship from the Support Foundation for the Development of Education, Science and Technology of the State of Mato Grosso do Sul (FUNDECT), the National Council for Scientific and Technological Development (CNPq), and the Coordination for the Improvement of Higher Education Personnel (CAPES). The UFGD provided logistical support and infrastructure. We thank the Laboratory of Ecotoxicology and Genotoxicity (LECOGEN) for all support during the development of this study. The RESIBRAS (Fortaleza, CE, Brazil) supplied the technical cashew nut shell liquid from which the bioactive compounds were synthesized. The SUCEN (Marília, SP, Brazil) and the Biosciences Institute of the UFMS (Campo Grande, MS, Brazil) supplied Ae. aegypti Rockefeller eggs. AQUAFORTE (Dourados, MS) donated O. niloticus fingerlings.
Funding
Coordination for the Improvement of Higher Education Personnel (CAPES), National Council for Scientific and Technological Development (CNPq), and Foundation to Support the Development of Education, Science and Technology of the State of Mato Grosso do Sul (FUNDECT).
Author information
Authors and Affiliations
Contributions
HSN: formulation, methodology, validation, research, writing—proofreading and editing, visualization. BAC: conceptualization, methodology, research, validation, writing—revision and editing, resources, supervision, project administration. FMM: methodology, research, writing—proofreading and editing, visualization. FK: formal analysis, writing—proofreading and editing, visualization. RAP: methodology, resource, writing—review, visualization. CALC: methodology, research, writing—revision and editing. DLVO: methodology, research, writing—revision and editing. KMPO: methodology, validation, review, visualization. FGSD: methodology, validation, writing—proofreading and editing. EJA: conceptualization, methodology, validation, formal analysis, research, resources, writing—proofreading and editing, visualization, acquisition of funding. AB: conceptualization, methodology, validation, resources, formal analysis, writing—proofreading and editing, supervision, acquisition of financing, project administration. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare they have no conflicts of interest.
Ethical Approval
All experimental procedures using Oreochromis niloticus for the development of this study followed the ethical principles of the Animal Ethics Committee of the Federal University of Grande Dourados (CEUA/UFGD), under protocol nº 09/2017-2.
Consent to Participate
Not applicable.
Consent for Publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Nascimento, H.d., Crispim, B.d., Merey, F.M. et al. Self-emulsifiable Bioactive Derivatives of Technical Cashew Nut Shell Liquid (tCNSL) Developed to Control Aedes aegypti Populations. Waste Biomass Valor 13, 2539–2552 (2022). https://doi.org/10.1007/s12649-022-01683-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12649-022-01683-3