In vitro evaluation of the antifungal activity of copaib tree resin oil (Copaifera reticulata Ducke) and its nanoemulsion on a wild strain of Aspergillus fumigatus Fresenius isolated from the Brazil nut tree (Bertholletia excelsa Bompl.)

Authors

DOI:

https://doi.org/10.33448/rsd-v12i4.40852

Keywords:

Amazonia; Copaifera reticulate; Alternate control; Medicinal plant.

Abstract

Copaiba tree species are widely distributed in the Amazon and Midwest regions of Brazil. Its oil is used as an anti-inflammatory of the urinary tract, in pulmonary disorders, anti-ulcer, anti-asthmatic, expectorant, pneumonia, sinusitis, dysentery, urinary incontinence, cystitis and leukorrhea and as an antitumor. The objective of this work was to evaluate the antifungal activity of Copaifera reticulata Ducke oilresin and its nanoemulsion compared to the already known antifungal of synthetic origin itraconazole on the wild strain of Aspergillus Fumigatus Fresen. isolated from Bertholletia excelsa Bonpl. The fungitoxicity of both the oil and the nanoemulsion were determined by the Poison Food technique. Using Itraconazole (brand: Prati; Batch: 16A43N) at a concentration of 1.6 µg/mL, as a positive control and Tween 20 at a concentration of 1.6 µg/ml, as a negative control and the fungus in a culture medium without the oil, as a control. The treatments were carried out in triplicate and the mycelial growth record was evaluated every 24h, 48h and 72h, measuring the transversal and longitudinal diameters, for the analysis of the Mycelial Growth Inhibition Percentage (% PIC) and daily radial growth of the fungal colony. The experimental design was completely randomized, in a factorial scheme, 7 x 1 x 3 x 3 (concentrations x fungus x control x repetitions). It was verified that both the copaiba oilresin and its nanoemulsion are potential candidates in the control of A. fumigatus. Besides not being observed any type of resistance of A. fumigatus regarding the action of Itraconazole.

Author Biographies

Ana Cláudia Lira Guedes, Empresa Brasileira de Pesquisa Agropecuária – Embrapa Amapá

Forestry/Non-timber thematic core

Anna Eliza Maciel de Faria Mota Oliveira, Universidade Federal do Amapá

Adjunct Professor C Level III of the Pharmacy Course at the Federal University of Amapá (UNIFAP)

José Carlos Tavares de Carvalho, Universidade Federal do Amapá

Drug Laboratory Coordinator

References

Alencar, E. N., Xavier-Júnior, F, H., Morais, A. R., Dantas, T. R., Verissimo, L. M., Rehder, V. L., Chaves, G. M., Oliveira, A. G. & Egitol, E. S. (2015). Chemical Characterization and Antimicrobial Activity Evaluation of Natural Oil Nanostructured Emulsions. Journal Nanoscience Nanotechnology. (1), 880-8.

Baquião, A. C., Zorzete, P., Reis, T. A., Assunção, E., Vergueiro, S. & Correa, B. (2012). Mycoflora and mycotoxins in field samples of Brazil nuts. Food Control, 28, 224-229.

Braga, W. F., Resende, C. M., Antunes, O. A. C. & Pinto, A. C. (1998). Terpenoids from Copaiba cearensis. Phytochemistry, 49, 263-264.

Calderari, T. O., Iamanaka, B. T., Frisvad, J. C., Pitt, J. I., Sartori, D., Pereira, J. L., Fungaro, M. H. P. & Taniwaki, M.H. (2013). The biodiversity of Aspergillus section Flavi in Brazil nuts: from rainforest to consumer. International Journal Food Microbiology. 160, 267-272.

Camargo, M. F. P. (2008). Desenvolvimento de nanoemulsão à base de óleo de maracujá (Passiflora edulis) e óleo essencial de lavanda (Lavandula officinalis) e avaliação da atividade antiinflamatória tópica. Dissertação (Mestrado), Ciências Farmacêuticas, Universidade de São Paulo, Ribeirão Preto.

Cardinelli, C. C., Almeida e Silva, J. E., Ribeiro, R., Veiga-Júnior, V. F., Santos, E. P. dos & Freitas, Z. M. F. de. (2023). Plants, 12, 1054. https://doi.org/10.3390/plants12051054.

Cascon, V. & Gilbert, B. (2000). Characterization of the chemical composition of oleoresins of Copaifera guianensis Desf. Copaifera duckei Dwyer and Copaifera multijuga Hayne. Phytochemistry, 55, 773-778.

Costa, A. K. F., Freire, F. C. O., Vieira, I. G. P., Andrade, J. A. & Mendes, F. N. P. (2009). Fungos associados à castanha-do-Brasil (Bertholletia excelsa Humb. & Bompl) e ao amendoim (Arachis hypogaea L.) comercializados em Fortaleza (Ceará). Revista de Ciências Agronômicas, Fortaleza, 40(3), 455-460, jul-set.

Denning, D. W. & Stevens, D. A. (1990). Antifungal and surgical treatment of invasive aspergillosis: review of 2121 published cases. Rev. Infectology Disease. 12, 1147–1201.

Deus, R., Alves, C. & Arruda, M. (2011). Avaliação do efeito antifúngico do óleo resina e do óleo essencial de copaíba (Copaifera multijuga Hayne). Revista Brasileira de Plantas Medicinais. 13 (1) 1-7.

Dias, D. O., Colombo, M., Kelmann, R. G., Sousa, T. P., Bassiani, V. L., Teixeira, H. F, Veiga-Júnior, V. F., Limberger, R. P. & Koester, L. S. (2012). optimization of headspace solid-phase microextraction for analysis of β-cayophyllene in a nanoemulsion dosage form prepared with copaíba (Copaifera multijuga Hayne) oil. Analitical Chimical Acta. 721, 79-84.

Diefenbach, A. L., Muniz, F. W. M. G., Oballe, H. J. R. & Rösing, C. K. (2018). Antimicrobial activity of copaiba oil (Copaifera ssp.) on oral pathogens: Systematic review. Phytotherapy Research, 32(4), 586–596.

Farnsworth, N. R. (1996). Biological and phytochemical screening of plants. Journal of Pharmaceutical Science, 55(3), 225-76.

Fernandez, P., André, V., Rieger, J. & Kuhnle, A. (2004). Nanoemulsions formation by emulsions phase inversion. Colloids and Surfaces A: Physiochemical and Engineering Aspects, Amsterdam, 251, 53-58.

Ferreira, D. F. (2014). Sisvar: a Guide for its Bootstrap procedures in multiples comparisons. Ciênc. Agrotec. 38(2), 109-112. http://dx.doi.org/10.1590/S1413-70542014000200001.

Flora e Funga do Brasil. (2023). Base de dados. Jardim Botânico do Rio de Janeiro (JBRJ). Disponível em: http://floradobrasil.jbrj.gov.br/.

Fonseca, R. Y. G, Barros, F. M, Apel, M.vA, Poser, G. L, Andriolli, J. O, Filho, P. C, Souza, D. F. & Lobo, I. P. (2015). Physicochemical and antimicrobial properties of copaiba oil: implications on product quality control, Acta Sci. Pol. Technol. Aliment. 14(3), 215-225.

Fortí, J. A. (1997). Aspectos patológicos, epidemiológicos y culturales de Acremonium cucurbitacearum Alfaro-García, W. Gams et J. García-Jiménez. Tesis (doctoral), Universidad Politécnica de Valencia, Escuela Técnica Superior de Ingenieros Agrónomos, Departamento de Produccíon Vegetal, Valencia, p. 183.

Global Biodiversity Information Facility - GBIF. (2023). Base de dados. http://gbif.org

Gonçalves, S. S., Stchigel, A. M., Cano, J. F., Godoy-Martinez, P. C, Colombo, A. L. & Guarro, J. (2012). Aspergillus novoparasiticus: a new clinical species of the section Flavi. Medical Mycology, 50,152–160.

Goren, A. C, Piozzi, F., Akcicek, E., Klhç, T., Çankçl, S., Mozio, Glu, E. & Setzer, W. N. (2011). Essential Oil composition of twenty-two Stachys species (mountain tea) and their biological activities, Phytochemical Lettuce. 4(4), 448-453.

Gurgel, E. S. C., Oliveira, M. S., Souza, M. C., Silva, S. G., Mendonça, M. S. & Souza Filho, A.P.S. (2019). Chemical compositions and herbicidal (phytotoxic) activity of essential oils of three Copaifera species (Leguminosae-Caesalpinoideae) from Amazon-Brazil. Industrial Crops and Products, 142, 111850. 10.1016/J.INDCROP.2019.111850

Iamanaka, B. T., Nakano, F., Lemes, D. P., Ferrati, L. S. & Taniwaki, M. H. (2014). Aflatoxin evaluation in ready-to-eat Brazil nuts using reversed phase liquid chromatography and post column derivatisation. Food Additional Contam. A. 31, 917-923.

Kaur, S. & Singh, S. (2014). Biofilm formation by Aspergillus fumigatus. Review Article. The International Society for Human and Animal Mycology 2013. Medical Mycology, 52(1), 2-9.

Koshi, G. & Cherian, K. M. (1995). Aspergillus terréus, na uncomon fungus causing aortic root abcess and pseudoaneurysm. Indian Heart Journal, 47, 265-7.

Leandro, L. M., Vargas, F. S., Barbosa, P. C., Neves, J. K, Silva, J. A. & Veiga-Júnior, V. F. (2012). Chemistry and biological activities of terpenoids from copaiba (Copaifera spp.) oleoresins, Molecules, 17(4), 3866—3889.

Lima, C. A. S., Povoas, I. M., Alves, W. K. S., Carvalho, F. T., Dias, N. da S., Anjos, T. R. dos, Andrade, K. R. N. C., Frasson, A. P. Z. de, Santos, M. D. dos & Carvalho, R. C. T. (2021). Atualizações sobre as propriedades medicinais do óleo de Copaíba (Copaifera spp.): uma Revisão Bibliográfica. Uniciencias, 25(2), 100-106. DOI: https://doi.org/10.17921/1415-5141.2021v25n2p100-106.

Lopes, A. J, Jansen, U., Capone, D. & Jansen, J. M. (2004). Aspergiloses pulmonares. Pulmão, RJ, 13(1), 257-67.

Martins-da-Silva, R. C. V., Silva, A. S. L., Fernandes, M. M. & Margalho, L. F. (2014). Noções morfológicas e taxonômicas para identificação botânica. Embrapa. 111p. Disponível em: https://www.embrapa.br/busca-de-publicacoes/-/publicacao/992543/nocoes-morfologicas-e-taxonomicas-para-identificacao-botanica

Midorikawa, G. E. O., Sousa, M. L. M. Silva, O. F., Dias, J. S. A., Kanzaki, L. I. B., Mesquita, R. M. L. C., Gonçalves, R. C., Álvares, V. S., Bittencourt, D. M. C. & Miller, R. N. G. (2014). Characterization of Aspergillus species on Brazil nut from the Brazilian Amazonian region and development of a PCR assay for identification at the genus level. BMC Microbiology, 14, 138.

Mowat, E., Lang, S., Williams, C., Mcculloch, E., Jones, B. & Ramage, G. (2008). Phase-dependent antifungal activity against Aspergillus fumigatus developing multicellular filamentous biofilms. Journal Antimicrobial Chemotherapical, 62, 1281–1284. 10.1093/jac/dkn402.

Mylonakis, E. & Calderwood, S. B. (2001). Infective endocarditis in adults. The New England Journal of Medicine, 345, 1318-30.

Ohsaki, A., Yana, L.T, Ito, A. S, Edatsugib, H., Iwatab, D. & Komoda, A. Y. (1994). The Isolation and in vivo Potent Antitumor Activity of Clerodane Diterpenoid from the Oleoresin of the Brazilian Medicinal Plant, Copaifera Langsdorfii Desfon. Biorganic & Medicinal Chemimy Letters, 24 (4), 889-2892.

Oliveira, J. M., Nunes, C. P. & Oliveira, P. C. (2002). Aspergilose. In: Siqueira-Bastista R, Gomes, A.P; Santos, S.S; Almeida, L.C; Figueiredo, C.E.S. Pacheco, S.J.B. Manual de infectologia. Rio de Janeiro: Revinter; p.461-4.

Paiva, L. A. F., Rao, V. S. N., Gramosa, N. V. & Silveira, E. R. (1998). Gastroprotective effect of Copaifera langsdorffii oleo-resin on experimetal gastric ulcer models in rats. Journal Ethnopharmacology, 62, 73-78.

Paiva, P. M, Guedes, M C. & Funi, C. (2011). Forest Ecology and Management, 261, 508-514.

Pieri, F. A., Mussi, M. C. & Moreira, M. A. S. (2009). Óleo de copaíba (Copaifera sp.): histórico, extração, aplicações industriais e propriedades medicinais. Revista Brasileira Plantas Medicinais, 11(4), 465-472.

Pinto, A. C., Braga, W. F., Rezende, C. M., Garrido, F. M. S., Veiga-Júnior, V. F., Bergter, L., Patitucci, M. L. & Antunes, O. A. C. (2000). Separation of Acid Diterpenes of Copaifera cearenses Huber ex Ducke by flash chromatography using potassium hydroxide impregnated silics gel. Journal Brazilian Chemical Society, 11, 355-360.

Pitt, J. L. & Hocking, A. D. (2009). Fungi and spolage. Edition. New York, Springer.

Rapper, K. B. & Fennell, D. L. (1973). The genus Aspergillus. Robert E. Krieger Publishing Co. Huntington, Nueva York.

Recio, M.C., Rios, J.L., & Villar, A. (1989). A review of some antimicrobial compounds isolated from medicinal plants reported in the literature 1978-1988. Phytotherapy Research, 4(3), 117-25.

Rodrigues, E. A. C. (1997). Infecções hospitalares: prevenção e controle. Sarvier. 28p.

Rodrigues, R. M. (1989). A Flora da Amazônia. Belém-PA: CEJUP. 462p.

Sajjadi, S., Zerfa, M. & Brooks, B. W. 2003. Phase inversion in p-xylene/warter emulsions with the non-ionic surfactan pair. Sorbitano monolaurate/ polyoxyethylene sorbitano monolaurate (Span 20/tween 20). Colloids and Surfaces A: Physicochemical and Engineering Aspects, 252, 27-32.

Santos, A. O, Ueda-Nakamura, T., Dias Filho, T., Veiga-Júnior, V. F., Pinto, A. C. & Nakamura, C. V. (2008). Antimicrobial activity of Brazilian copaiba oils obtained from different species of the Copaifera genus, Memorial Journal, 103(3), 277-281.

Selestino Neta, M. C, Vittorazzi, C., Guimarães, A. C, Martins, J. D. L, Fronza, M., Endringer, D. C. & Scherer, R. (2017). Effects of β-caryophyllene and Murraya paniculata essential Oil in the murine hepatoma cells and in the bacteria and fungi 24-h time-kill curve studies, Pharmacology Biology 55(1), 190-197.

Souza, A. B., Souza, M. G., Moreira, M. A, Moreira, M. R, Furtado, N. A, Martins, C.H, Bastos, J.K.R.A., dos Santos, V.C., Heleno, S.R., Ambrosio, R.C. & Veneziani, R.C.S. (2011). Antimicrobial evaluation of diterpenes from Copaifera langsdorffii oleoresin against periodontal anaerobic bacteria, Molecules. 16(11), 9611-9619.

Souza, P. A, Rangel, L. P., Oigman, S. S., Elias, M. M., Ferreira-Pereira, E. A., Lucas, N. C. & Leitão, G.G. (2010). Isolation of two bioactive diterpenic acids from Copaifera glycycarpa oleoresin by high-speed counter-current chromatography, Phytochemical Analitical, 21(6), 539-543.

Stevens, D. A. (2001). Aspergilose. In: Goldmam, L.; Bennett, J.C.; Drazen, J.M.; Gill, G.N.; Kokko, J. P; Mandell, G.L; Porruel, D. W & Schafer, A.I. Cecil Tratado de Medicina Interna. (pp. 2092-94). Guanabara Koogan.

Svetlichny, G, Külkamp-Guerreiro, I. C, Cunha, S. L, Silva, Fé Bueno, K., Pohlmann, A. R., Fuentefria, A. M., & Guterres, S. S. (2015). Pharmazie. Solid lipid nanoparticles containing copaiba Oil and allantoin: development and role of nanoencapsulation on the antifungal activity. Mar. 70(3), 155-64.

Van de Sande, W. W. J., Tavakol, M., Van Vianen, W. & Bakker-Woudenberg, I. A. J. M. (2010). The effects of antifungal agents to conidial and hyphal forms of Aspergillus fumigatus. Medical Mycology. Feb; 48(1), 48-55. 10.3109/13693780802713497.

Thomidis, T. & Filotheou, A. (2016). Evaluation of five essential oils as bio-fungicides on control of Pilidiella granati rot in pomegranate. Crop Protection. 89, 66-71. http://dx.doi.org/10.1016/j.cropro.2016.07.002.

Tobouti, P. L., De Andrade Martins, T. C., Pereira, T. J. & Mussi, M. C. M. (2017). Antimicrobial activity of copaiba oil: A review and a call for further research. Biomedicine & Pharmacotherapy, 94, 93–99.

Tropicos. (2023). Base de dados. Missouri Botanical Garden. http://www.tropicos.org.

Watanabe, A., Arai, T. & Majima, H. (2022). New mechanism and detection methods for azole-resistant Aspergillus fumigatus: Emerging antifungal resistant fungi. Medical Mycology, 60, S10.

Wei, T., Zheng, N., Zheng, H., Chen, Y., Hong, P., Liu, W. & Liu, M. (2022). Proteomic Perspective of Azole Resistance in Aspergillus fumigatus Biofilm Extracellular Matrix in Response to Itraconazole. Medical Mycology, 60, 10, Oct 16, myac084. 10.1093/mmy/myac084.

Veiga-Júnior, V. F, Rosas, E. C, Carvalho, M. V, Henriques, M. G & Pinto, A.C. (2007). Chemical composition and anti-inflammatory activity of copaiba oils from Copaifera cearensis huber ex ducke, Copaifera reticulata Ducke and Copaifera multijuga Hayne-a comparative study, Journal Ethnopharmacology, 112 (2), 248-254.

Veiga-Júnior, V. F. & Pinto, A.C. (2002). O gênero Copaifera L. Química Nova, 25, 273-286.

Verghese, S., Mullasari, A. & Padmaja, P. (1998). Fungal endocarditis cardiac surgery. Indian Heart Journal, 50, 418-22.

Published

31/03/2023

How to Cite

DIAS, J. do S. A. .; GUEDES, A. C. L. .; FERREIRA, I. M. .; OLIVEIRA, A. E. M. de F. M. .; CARVALHO, J. C. T. de . In vitro evaluation of the antifungal activity of copaib tree resin oil (Copaifera reticulata Ducke) and its nanoemulsion on a wild strain of Aspergillus fumigatus Fresenius isolated from the Brazil nut tree (Bertholletia excelsa Bompl.). Research, Society and Development, [S. l.], v. 12, n. 4, p. e9512440852, 2023. DOI: 10.33448/rsd-v12i4.40852. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/40852. Acesso em: 19 apr. 2024.

Issue

Section

Agrarian and Biological Sciences