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+Artigo • Hoehnea 49 • 2022 • https://doi.org/10.1590/2236-8906-111/2020 +   + copiar +
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+Prospecção química, atividade antioxidante, anticolinesterásica e antifúngica de extratos etanólicos de espécies de Senna Mill. (Fabaceae) +

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Chemical prospecting and antioxidant, anticholinesterase and antifungal activity of ethanol extracts from Senna Mill. species. (Fabaceae)

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+ Andréa Maria Neves Selene Maia de Morais Hélcio Silva dos Santos Marcílio Matos Ferreira Ricardo Carneiro Vera Cruz Elnatan Bezerra de Souza Lúcia Betânia da Silva Andrade Raquel Oliveira dos Santos Fontenelle Sobre os autores +
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RESUMO

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O objetivo deste trabalho foi avaliar o perfil químico, teor de fenóis totais e as atividades antioxidante, antiacetilcolinesterásica e antifúngica dos extratos etanólicos das folhas (EEF) e do caule (EEC) de cinco espécies de Senna, bem como avaliar a correlação entre o conteúdo de fenóis totais com a atividade sequestradora do radical livre DPPH e com a inibição da enzima acetilcolinesterase AChEI. No teste fitoquímico, evidenciou-se a presença de metabólitos secundários em todos os extratos. Os EEF e EEC de Senna trachypus, destacaram-se por apresentar os maiores valores de fenóis totais. Os EEF e EEC de S. trachypus mostraram a melhor ação sobre a enzima acetilcolinesterase. Todas as espécies apresentaram atividade antioxidante, em especial o EEF de S. trachypus. Foi observado correlação forte para as variáveis fenóis totais e atividade antioxidante (r = -0,71), muito forte para fenóis totais e antiacetilcolinesterase (r = -0,84) e atividade moderada para atividade antioxidante e antiacetilcolinesterase (0,43). Apenas os extratos de S. trachypus apresentaram atividade contra todos os dermatófitos, quando comparado às demais espécies. A espécie S. trachypus foi considerada a planta mais promissora para estudos subsequentes, a fim de encontrar compostos com ações farmacológicas.

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Palavras-chave:
acetilcolinesterase; dermatófitos; fitoquímica; produtos naturais; radicais livres

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ABSTRACT

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The objective of this work was to evaluate the chemical profile, total phenol content and the antioxidant, antiacetylcholinesterase and antifungal activities of ethanol extracts from leaves (EEF) and stem (EEC) of five species of Senna, as well as to evaluate the correlation between the content of total phenols with the DPPH free radical scavenging activity and with the inhibition of the acetylcholinesterase AChEI enzyme. The phytochemical test showed the presence of secondary metabolites in all extracts. The EEF and EEC of Senna trachypus, stood out for presenting the highest values of total phenols. S. trachypus EEF and EEC showed the best action on the acetylcholinesterase enzyme. All species showed antioxidant activity, especially the EEF from S. trachypus. A strong correlation was observed for the variables total phenols and antioxidant activity (r = -0.71), very strong for total phenols and anti-acetylcholinesterase (r = -0.84) and moderate activity for antioxidant and anti-acetylcholinesterase activity (r = 0.43). Only S. trachypus extracts showed activity against all dermatophytes, when compared to the other species. The species S. trachypus was considered the most promising plant for further studies, in order to find compounds with pharmacological actions.

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Keywords:
acetylcholinesterase; dermatophytes; phytochemistry; natural products; free radicals

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Introdução

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Senna Mill. é um gênero monofilético com distribuição pantropical e ampla variedade morfológica (Pellerin et al. 2019Pellerin, R.J., Waminal, N.E. & Kim, H.H. 2019. FISH mapping of rDNA and telomeric repeats in 10 Senna species. Horticulture, Environment, and Biotechnology 60: 253-260.). Possuindo aproximadamente 300 espécies, das quais 200 nas Américas, este gênero é o segundo maior da família Fabaceae (Queiroz 2009Queiroz, L.P. 2009. Leguminosas da Caatinga. Universidade Estadual de Feira de Santana, Feira de Santana, 467 p., Kim et al. 2018Kim, M.S., Lee, D.Y., Sung, S.H. & Jeon, W.K. 2018. Anti-cholinesterase activities of hydrolysable tannins and polyhydroxytriterpenoid derivatives from Terminalia chebula Retz. fruit. Fruit Rec Nat Prod 12: 284-289., Souza & Silva 2016Souza, A.O. & Silva, M.J. 2016. Senna (Leguminosae, Caesalpinioideae) na Floresta Nacional de Silvânia, Goiás, Brasil. Rodriguésia 67: 773-784. ). O gênero é representado no Brasil por 79 espécies, onde 29 são endêmicas, sendo a região Nordeste a que apresenta a maior riqueza de espécies com 53 registros (BFG 2018BFG. 2018. Brazilian Flora 2020: Innovation and collaboration to meet Target 1 of the Global Strategy for Plant Conservation (GSPC). Rodriguésia 1513-1527. ).

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Trata-se de um gênero muito expressivo na flora do semiárido, alcançando destaque no Domínio Fitogeográfico da Caatinga, onde são catalogadas 42 espécies (Souza & Bortoluzzi 2015Souza, V.C.; Bortoluzzi, R.L.C. 2015. Senna in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. ). As espécies de Senna são geralmente arbustos ou arvoretas, raramente ervas ou subarbustos anuais. Entre as suas características diagnósticas estão os nectários extraflorais convexos, interfoliolares, flores vistosas, com pétalas amarelo-brilhantes, anteras amarelas, rígidas, com deiscência abrindo por poros ou fendas, ausência de bractéolas no pedicelo, frutos deiscentes plano-compressos ou indeiscentes e cilíndricos (Queiroz 2009Queiroz, L.P. 2009. Leguminosas da Caatinga. Universidade Estadual de Feira de Santana, Feira de Santana, 467 p.).

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As espécies de Senna têm diversas aplicações medicinais e são eficazes no tratamento para uma série de doenças, como malária, micose, dengue, eczema, hepatite e dermatite, sendo também indicadas como anti-hipertensivo, vermífugo, laxante, abortivo e antitussígeno (Macedo et al. 2016Macedo, E.M., Alan, J.G., & Silva, M.G.V. 2016. Quimiodiversidade e propriedades biofarmacológicas de espécies de Senna nativas do Nordeste do Brasil. Revista Virtual de Química 8: 169-195., Bieski et al. 2015Bieski, I.G.C., Leonti, M., Arnason, J.T., Ferrier, J., Rapinski, M., Violante, I.M.P., Balogun,S.O., Pereira, J.F.C.A., Figueiredo, R.D.C.F., Lopes, C.R.A.S., Silva, D.R.D., Pacini, A., Albuquerque, U.P. & Martins, D.T.D.O. 2015. Ethnobotanical study of medicinal plants by population of valley of Juruena region, legal amazon, Mato Grosso, Brazil. Journal of Ethnopharmacology 173: 383-423., Kabir et al. 2014Kabir, M.H., Hasan, N., Rahman, M.M., Rahman, M.A., Khan, J.A., Hoque, N.T., Bhuiyan, M.R.Q., Mou, S.M.; Jahan, R. & Rahmatullah, M. 2014. A survey of medicinal plants used by the Deb barma clan of the Tripura tribe of Moulvibazar district, Bangladesh. Journal of Ethnobiology and Ethnomedicine 10: 1-19.). Além de suas aplicações farmacológicas, estudos têm revelado que espécies pertencentes a este gênero possuem, em sua composição, uma vasta diversidade de princípios bioativos que estão associadas a diferentes atividades biológicas. Neste sentido, podemos citar como exemplo as atividades antioxidantes, antitumoral, antibacterianas, antifúngicas e anti-inflamatórias (Neves et al. 2017Neves, A.M., Costa, O.S., Coutinho, M.G.S., Souza, E.B., Santos, H.S., Silva, M.G.V. & Fontenelle, R.O.S. 2017. Caracterização química e o potencial antimicrobiano de espécies do gênero Senna Mill (Fabaceae). Rev. Virtual Quim 9: 2506-2538.).

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As plantas são fontes alternativas promissoras de substâncias de interesse biológico e farmacológico, já que podem produzir, a partir de seu metabolismo secundário, uma enorme diversidade de substâncias, dentre estas, os compostos fenólicos. Alguns estudos têm revelado que os compostos fenólicos são responsáveis por várias atividades biológicas, incluindo atividade antifúngica. Esta atividade pode ser direta nos micro-organismos, ou sobre outros fatores necessários para a expressão da virulência ou patogenicidade (Rodrigues et al. 2019Rodrigues, F.C., Dos Santos, A.T.L., Machado, A.J.T., Bezerra, C.F., de Freitas, T.S., Coutinho, H.D.M., Morais-Braga, M.F.B., Bezerra, J.W.A., Duarte, A.E., Kamdem, J.P., Boligon, A.A., Campos, M.M.A., Barros, L.M. 2019. Chemical composition and anti-Candida potencial of the extracts of Tarenaya spinosa (Jacq.) Raf.(Cleomaceae). Comparative immunology, microbiology and infectious diseases 64: 14-19.).

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Os compostos fenólicos estão entre os metabólitos secundários mais estudados, notadamente por possuírem grande potencial para atividades antioxidantes, atuando na redução do risco de algumas doenças agudas e crônicas relacionadas ao estado redox do corpo humano, ocasionadas pelos radicais livres. Estas moléculas apresentam uma alta capacidade reativa, sendo consideradas perigosas para os organismos vivos, causando doenças prejudiciais, incluindo doenças neurodegenerativas, como o mal de Alzheimer (DA). Atualmente, uma das teorias mais aceitas na abordagem padrão no tratamento sintomático dessa demência é a “hipótese colinérgica”. Portanto, os inibidores da enzima acetilcolinesterase (AChEI) preservam os níveis de acetilcolina, melhorando a eficiência da transmissão colinérgica (Bardakci et al. 2019Bardakci, H., CeleP, E., Gözet, T., Kan, Y. & Kirmizibekmez, H. 2019. Phytochemical characterization and antioxidant activities of the fruit extracts of several Crataegus taxa. South African Journal of Botany 124: 5-13. , Lim et al. 2019Lim, S., Choi, A.H., Kwon, M., Joung, E.J., Shin, T., Lee, S.G., Kim, NG. & Kim, H. R. 2019. Evaluation of antioxidant activities of various solvent extract from Sargassum serratifolium and its major antioxidant components. Food Chemistry 278: 178-184.; Neagu et al. 2016Neagu, E., Radu, G.L., Albu, C., & Paun, G. 2016. Antioxidant activity, acetylcholinesterase and tyrosinase inhibitory potential of Pulmonaria officinalis and Centarium umbellatum extracts. Saudi Journal of Biological Sciences, 3: 578-585.).

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Por este motivo, a utilização de dietas ricas ou enriquecidas com antioxidantes podem prevenir, ou pelo menos amenizar, a deterioração orgânica por um excessivo estresse oxidativo. Além disso, o crescimento sobre a investigação científica envolvendo os efeitos antioxidantes de extratos brutos, frações purificadas, ou mesmo de compostos isolados, onde estão classificados os compostos fenólicos, são demonstrados em muitos estudos (Penido et al. 2017Penido, A.B., De Morais, S.M., Ribeiro, A.B., Alves, D.R., Rodrigues, A.L.M., dos Santos, L.H. & de Menezes, J.E.S.A. 2017. Medicinal plants from northeastern Brazil against Alzheimer’s disease. Evidence-Based Complementary and Alternative Medicine 2017: 1-7. , Morais et al. 2013Morais, S.M., Lima, K.S.B., Siqueira, S.M.C., Cavalcanti, E.S.B., Souza, M.S.T., Menezes, J.E.S.A., Trevisan, M.T.S. 2013. Correlação entre as atividades antiradical, antiacetilcolinesterase e teor de fenóis totais de extratos de plantas medicinais de farmácias vivas. Revista Brasileira de Plantas Medicinais 15: 575-582. ).

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Desta forma, investigar a atividade antifúngica e anticolinesterásica de extratos de espécies de Senna, analisando o seu potencial antioxidante, o seu teor de fenóis totais e o seu perfil fitoquímico, são maneiras de promover tanto o conhecimento acerca dessas espécies, como também potencializar o descobrimento de novos fitofármacos para o combate de inúmeras enfermidades. Assim, este trabalho avaliou o perfil fitoquímico, o teor de fenóis totais e as atividades antioxidante, anticolinesterásica e antifúngica dos extratos etanólicos de S. alata (L.) Roxb., S. obtusifolia (L.) H.S.Irwin & Barneby, S. occidentalis (L.) Link, S. siamea (Lam.) H.S.Irwin & Barneby e S. trachypus (Benth.) H.S.Irwin & Barneby, e a correlação entre o teor de fenóis totais e as atividades antioxidante e anticolinesterásica.

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Materiais e métodos

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Material vegetal e preparação dos extratos - Foram selecionadas para este estudo cinco espécies de Senna, sendo uma exótica naturalizada e quatro nativas, das quais uma é endêmica do Brasil, ocorrendo no Cerrado e na Caatinga (BFG 2018BFG. 2018. Brazilian Flora 2020: Innovation and collaboration to meet Target 1 of the Global Strategy for Plant Conservation (GSPC). Rodriguésia 1513-1527. ) (Tabela 1). As folhas e caules de Senna spp. foram coletados em diferentes locais da região Noroeste do Ceará. A identificação botânica das espécies foi realizada no Herbário Francisco José de Abreu Matos da Universidade Estadual Vale do Acaraú (HUVA), pelo professor Dr. Elnatan Bezerra de Souza. Para o preparo dos extratos, 200g das folhas e caule secos de cada espécie de um mesmo indivíduo foram triturados e imersos durante 10 dias em 500 mL de etanol e, na sequência o extrato foi filtrado e concentrado em um evaporador rotativo a (60°C) durante 2 h. Após este processo, foi mantido em banho-maria (40°C) até a eliminação total do solvente, obtendo-se o extrato etanólico das folhas (EEF) e extrato etanólico do caule (EEC) (Matos 2009Matos, F.J.A. 2009. Introdução à Fitoquímica Experimental. 3 ed. Fortaleza: UFC. 150p.).

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Identificação das espécies de Senna Mill. (Fabaceae) coletadas em diferentes locais da região noroeste do Estado do Ceará. *Exótica, **Endêmica do Brasil. Fonte: Herbário Francisco José de Abreu Matos (HUVA).
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Triagem fitoquímica - Os extratos etanólicos foram submetidos a triagem fitoquímica, tomando como referência a metodologia descrita por Matos (2009Matos, F.J.A. 2009. Introdução à Fitoquímica Experimental. 3 ed. Fortaleza: UFC. 150p.). Através deste ensaio preliminar, foi possível verificar as principais classes de metabólitos secundários por meio de reações químicas que resultaram no aparecimento de coloração e/ou precipitado, característico para cada classe de substância. Os ensaios foram conduzidos para as seguintes classes de substâncias: fenóis, taninos, flavonoides, saponinas, esteroides, triterpenoides e alcaloides. Todos os testes foram realizados em triplicata procedimentais.

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Determinação do teor de fenóis totais - O teor de fenóis totais nos extratos etanólicos foi determinado pelo método espectrofotométrico de Folin-Ciocateau, utilizando ácido gálico como padrão de referência (Kim et al. 2006Kim, K.H., Tsao, R., Yang, R. & Cui, S.W. 2006. Phenolic acid profiles and antioxidant activities of wheat bran extracts and the effect of hydrolysis conditions. Food Chemistry 95: 466-473.). Em cada tubo adicionou-se 0,2 mL de cada extrato nas concentrações (0,62; 0,31 e 0,15 mg mL-1) com 1 mL do reagente Folin-Ciocalteau agitado por 2 minutos e adicionado 0,8 mL de carbonato de sódio (Na2CO3) 7,5% (m/v). Para o tubo controle foi utilizado 1 mL do reagente Folin- Ciocalteau com 0,8 mL de Na2CO3 e 0,2 mL de etanol, em triplicata. Os tubos foram deixados em banho-maria a 37 ̊C por 30 minutos na ausência de luz. Logo em seguida, foi realizado a leitura dos tubos em comprimento de onda de 765 nm. O teor de fenóis foi calculado e expresso em mg de equivalente de ácido gálico por grama de extrato (EAG.g-1), com base numa curva padrão preparada com ácido gálico. Todos os testes foram realizados em triplicata.

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Atividade antioxidante - A atividade antioxidante dos extratos foi determinada pelo método de redução do radical 2,2’-difenil-1-picril-hidrazil (DPPH), segundo a metodologia modificada por Brand-Williams et al. (1995Brand-Williams, W., Cuvelier, M.E. & Berset, C.L.W.T. 1995. Use of a free radical method to evaluate antioxidant activity. LWT-Food Science and Technology 1: 25-30.), Sanchez-Moreno et al. (1998Sánchez‐Moreno, C., Larrauri, J.A. & Saura‐Calixto, F. 1998. A procedure to measure the antiradical efficiency of polyphenols. Journal of the Science of Food and Agriculture 76: 270-276.). Foram preparadas soluções etanólicas das amostras nas concentrações de 5,0; 2,5; 1,25; 0,62; 0,31 e 0,15 mg mL-1. Foram utilizados 100 µL dos extratos com 2,4 mL de DPPH (0,04 mg mL-1). Para o tubo controle foram utilizados 100 µL de etanol com 2,4 mL de DPPH em triplicata. O meio reacional ficou por 30 minutos na ausência da luz, e posteriormente foi realizada a leitura em comprimento de onda 515 nm. A atividade sequestradora do radical DPPH pelos extratos nas diferentes concentrações foi calculada pela expressão do índice de varredura em porcentagem (IV%): IV% = (Abs DPPH - Abs Amostra / Abs DPPH) x 100. A concentração efetiva para inibir 50% do radical livre DPPH (CE50) foi obtida com auxílio do Software Excel 2019, onde, a partir dos valores das concentrações finais da amostra e o índice de varredura (IV%), foram originados gráficos de dispersão cujas equações das retas foram utilizadas para se obter os valores da média e desvio padrão. Para fins de comparação, foi construída uma curva de calibração com diferentes porcentagens do flavonoide quercetina, que apresenta elevada atividade antioxidante em radical livre DPPH.

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Avaliação da atividade anticolinesterásica in vitro - O ensaio para verificação da inibição da enzima acetilcolinesterase (AChE) dos extratos foi realizado de acordo com a metodologia descrita por Ellman et al. (1961Ellman, G.L., Courtney, K.D., Andres Jr, V. & Featherstone, R.M. 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology: 7: 88-95.). Em placas estéreis de 96 poços, foram adicionados 25 µL de iodeto de acetiltiocolina (15 mM), 125 µL de 5,5’-ditiobis-[2-nitrobenzóico] na solução Tris/HCL (50 nM, pH 8, com 0,1 M de NaCL e 0,02 M de MgCL2 .6H2O. (3 mM, DTNB ou reagente de Ellman)), 50 µL da solução Tris/HCL (50 nM, pH 8, com 0,1% de albumina sérica bovina (BSA) e 25 µL dos extratos de Senna spp. na concentraçao de 0,2 mg.mL-1 em tampão Tris/HCL (50 mM, pH 8) de 0,2 mg.mL-1 (Rhee et al. 2001Rhee, I.K., van de Meent, M., Ingkaninan, K. & Verpoorte, R. 2001. Screening for acetylcholinesterase inhibitors from Amaryllidaceae using silica gel thin-layer chromatography in combination with bioactivity staining. Journal of Chromatography A 915: 217-223., Trevisan et al. 2003Trevisan, M.T.S., Macedo, F.V.V., Meent, M.V.D., Rhee, I.K. & Verpoorte, R. 2003. Seleção de plantas com atividade anticolinesterase para tratamento da doença de Alzheimer. Química Nova 26: 301-304.).

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A absorbância foi aferida a 405 nm durante 30 segundos. Em seguida, foram adicionados 25 µL da enzima acetilcolinesterase (0,25 U.mL-1) e a absorbância foi aferida por minuto até o total de 25 minutos de incubação da enzima. Como padrão negativo foram utilizadas todas as soluções, excetuando-se a amostra. O padrão utilizado como controle positivo foi a fisostigmina (0,22 mg.mL-1.) e todas as amostras foram analisadas em triplicata. A atividade anticolinesterásica dos extratos vegetais foi determinada de acordo com os valores de CI50 (Concentração inibitória capaz de inibir 50% da enzima acetilcolinesterase) como: alta potência (CI50 < 20 μg. mL-1); potência moderada (20 < CI50 < 200 μg.mL-1) e baixa potência (200 < CI50 < 1000 μg.mL-1) (Santos et al. 2018Santos, G.H.F., Amaral, A. & Da Silva, E.B. 2018. Antibacterial activity of irradiated extracts of Anacardium occidentale L. on multiresistant strains of Staphylococcus aureus. Applied Radiation and Isotopes 140: 327-332.).

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Ensaio antifúngico in vitro - No ensaio para verificação da concentração inibitória mínima (CIM) dos EE das espécies de Senna, foram utilizadas cepas de Trichophyton rubrum obtidas a partir da micoteca da Universidade Federal de Pernambuco e do Centro Especializado de Micologia Médica (CEMM) da Universidade Federal do Ceará. Para este ensaio foi utilizado o método de microdiluição em caldo, de acordo com a metodologia descrita por (Neves et al. 2019Neves, A.M., Silva, H.S., Souza, E.B., Fontenelle, R.O.S., Silva, A.C.S., Morais, S.M. 2019. Perfil fitoquímico e avaliação da atividade antifúngica da fração hexânica de Mitracarpus baturitensis (Rubiaceae). Essentia 20: 96-101. ) com as normas do protocolo Clinical Laboratory Standards Insitute do documento M38-A (CLSI M38-A2, 2008Clinical and Laboratory Standards Institute. 2008. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi (Approved Standard Document M38. CLSI), vol. M38-A2, Second ed. Clinical and Laboratory Standards Institute, Wayne, PA.). Em placas de 96 poços estéreis, foram adicionados 100 µL de meio RPMI em todos os poços e 10 mg mL-1 dos extratos de Senna spp. foi acrescentado a todos os poços da primeira coluna e, em sequência foram efetuadas as diluições seriadas. Finalmente, 100 µL do inóculo foi adicionado aos poços da placa. Como controle foi utilizado o Cetoconazol (Sigma, Chemical Co., USA). Para as análises de susceptibilidade, os extratos etanólicos foram testados em concentrações variando de 0,002 a 2,5 mg mL-1. As placas foram cobertas com parafilme e incubadas a 37 °C e a leitura visual foi realizada após cinco dias para T. rubrum. Procedimento realizado em duplicata. A CIM é definida como a menor concentração do extrato capaz de inibir 100% do crescimento fúngico visível (Fontenelle et al. 2007Fontenelle, R.O.S., Morais, S.M., Brito, E.H.S., Kerntopf, M.R., Brilhante, R.S.N., Cordeiro, R.A., Tomé, A.R., Queiroz, M.G.R., Nascimento, N.R.F. & Sidrim, J.J.C. 2007. Chemical composition, toxicological aspects and antifungal activity of essential oil from Lippia sidoides Cham. Journal of Antimicrobial Chemotherapy 59: 934-940. ). A concentração fungicida mínima (CFM) foi determinada por subcultura de 100 μL da solução de poços sem turbidez no meio Ágar Dextrose de Batata, a 28 °C. (Fontenelle et al. 2008Fontenelle, R.O.S., Morais, S.M., Brito, E.H.S., Brilhante, R.S.N., Cordeiro, R.A., Nascimento, N.R.F., Kerntopf, M.R., Sidrim, J.J.C. & Rocha, M.F.G. 2008. Antifungal activity of essential oils of Croton species from the Brazilian caatinga biome. Journal of Applied Microbiology 104: 1383-1390.).

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Análise estatística - Todas as determinações foram realizadas em triplicata e todos os resultados foram apresentados como média ± desvio-padrão (DP). Foram realizadas análises de variância (ANOVA) com duas repetições e o Teste Tukey, ao nível de significância de 5%, usando programa Graph Pad Prism® v5.01 (GraphPadSoftware, San Diego, CA, E.U.A.). As diferenças entre as médias foram consideradas significativas quando o valor obtido para "p" foi menor que 0,05 (p < 0,05).

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Para análises da correlação entre os dados, foi utilizado o coeficiente de correlação de Pearson no software Microsoft Excel 2019, a qual mede o grau da correlação linear entre duas variáveis quantitativas. A intensidade dessa correlação é dada pelo “r”, que é um índice adimensional com valores situados entre -1,0 e 1,0. Quando o valor de r estiver entre 0,00-0,19 a correlação é muito fraca; entre 0,20-0,39 é fraca; 0,40-0,59 é uma correlação moderada; entre 0,60-0,79 é forte e finalmente entre 0,80-1,0 diz-se que é uma correlação muito forte (Mukaka 2012Mukaka, M.M. 2012. Statistics corner: A guide to appropriate use of correlation coefficient in medical research. Malawi Med J. 24:69-71.).

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Resultados e discussãoTabela 3 +

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Os fito-constituintes ou fitoquímicos são compostos químicos que desempenham importantes funções nas plantas. A triagem fitoquímica em materiais vegetais é geralmente o ponto de partida para o isolamento e purificação de compostos naturais com bioatividade (Omoregie & Oikeh 2015Omoregie, E.S. & Oikeh, E.I. 2015. Comparative studies on the phytochemical composition, phenolic content and antioxidant activities of methanol leaf extracts of Spondias mombin and Polyathia longifolia. Jordan Journal of Biological Sciences 147: 1-5.). A triagem fitoquímica preliminar revelou a presença de fenóis, taninos, flavonoides e esteroides para todos os extratos estudados (Tabela 2). Entretanto, a presença de saponinas foi constatada apenas no EEF e EEC de S. alata e no EEF de S. trachypus. Já os alcaloides foram encontrados exclusivamente no EEF de S. alata e nenhuma das espécies apresentou triterpenoides.

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Triagem fitoquímica do EEF e do EEC de espécies de Senna Mill. (Fabaceae). Presente: + Ausente: - EEF: Extrato etanólico da folha. EEC: Extrato etanólico do caule.
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Os metabólitos detectados nas espécies estudadas são consistentes com os metabólitos descritos na literatura para o gênero Senna, conhecido por apresentar flavonoides, alcaloides, taninos, esteroides e saponinas em sua composição (Onyegeme-Okerenta et al. 2017Onyegeme-Okerenta, B.M., Nwosu, T. & Wegwu, M.O. 2017. Proximate and phytochemical composition of leaf extract of Senna alata (L) Roxb. Journal of Pharmacognosy and Phytochemistry 6: 320-326., Ishaku et al. 2016Ishaku, G.A., Arabo, A.A., Bassey, E.E., Uwem, A.A.U.M. & Godwin, E.U. 2016. Physicochemical characterization and antibacterial activity of Senna occidentalis Linn. Journal of Chemistryand Chemical Sciences 6: 9-18. , Silva et al. 2014Silva, G.A., Monteiro, J.A., Ferreira, E.B., Fernandes, M.I.B., Pessoa, C.; Sampaio, C.G. & Silva, M.G.V. 2014. Total phenolic content, antioxidant and anticancer activities of four species of Senna Mill. From northeast Brazil. Int. J. Pharm. Pharm. Sci 6: 199-202., Sudi et al. 2011Sudi, I.Y., Ksgbiya, D.M., Muluh, E.K. & Clement, A. 2011. Nutritional and phytochemical screening of Senna obtusifolia indigenous to Mubi, Nigeria. Advances in Applied Science Research 2: 432-437., Bukar et al. 2009Bukar, A., Mukhtar, M. & HASSAN, A. 2009. Phytochemical screening and antibacterial activity of leaf extracts of Senna siamea (Lam) on Pseudomonas aeruginosa. Bayero Journal of Pure and Applied Sciences 1: 139-142. ). É possível perceber que na análise de prospecção química dos extratos houve uma variação de metabólitos secundários. Este fato pode estar atribuído a vários fatores, entre eles estão as diferentes condições ambientais, tais como clima, radiação solar, nutrição mineral, sazonalidade, ritmo circadiano, temperatura, disponibilidade hídrica, e também os tipos de solvente e a metodologia empregada no processo de extração, que podem interferir consideravelmente no conteúdo de praticamente todas as classes de metabólitos secundários (Gomes et al. 2016Gomes, E.M.C., Pena, R.D.C.M. & da Silva, S.S.S.M. 2016. Composição fitoquímica e ação fungicida de extratos brutos de Cinnamomum zeylanicum sobre Quambalaria eucalypti. Biota Amazônia. 6: 54-58., Bezerra et al. 2013Bezerra, A.S., Nörnberg, J.L., Lima, F.O., Rosa, M.B.D. & Carvalho, L.M.D. 2013. Parâmetros climáticos e variação de compostos fenólicos em cevada. Ciência Rural 9: 1546-1552., Gobbo-Neto & Lopes 2007Gobbo-Neto, L. & Lopes, N.P. 2007. Plantas medicinais: Fatores de influência no conteúdo de metabólitos secundários. Química Nova 30: 374-381.).

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Os teores de fenóis totais apresentaram diferenças significativas entre os extratos etanólicos das diferentes partes e espécies vegetais estudadas (Tabela 3). O conteúdo de fenóis totais para os EEF variou de 32,60 ± 0,53 a 184,8 ± 5,09 EAG/g, enquanto que para o EEC foram de 30,03± 1,00 a 191,3 ± 0,47 EAG/g. Os maiores níveis de fenóis totais foram detectados na espécie S. trachypus. Os dados da literatura sobre o conteúdo de compostos fenólicos obtidos a partir do extrato aquoso, etanólico e acetona da raiz de S. alata, apresentaram uma concentração de fenóis de 46,3, 78,21 e 21,42 mg EAG/g, respectivamente, e de flavonoides de 26,17, 39,29 e 9,65 mg de equivalente de quercetina por grama de extrato (EQ/g), respectivamente (Ita & Ndukwe 2017Ita, B.N., & Ndukwe, G.I. Antioxidant activity of Senna alata root extracts. 2017. J Nat Prod Resour 3: 94-96. ). Já o extrato etanólico preparado a partir das folhas de S. obtusifolia por Ali et al. (2019Ali, I., Yisa, J. & Jacob, J.O. 2019. Corrosion inhibitory potential of ethanol extract of Senna obtusifolia on Mild Steel in 5M HCl. Journal of Chemical Society of Nigeria 44: 187-198. ), apresentou um teor de fenóis e de flavonoides de 14,39 mg/g e 2,85 mg/g, respectivamente, demonstrando possuir teor de compostos fenólicos inferior ao das mostras de S. obtusifolia encontradas no presente estudo. Além disso, o conteúdo de polifenóis encontrado no extrato etanólico e nas frações obtidas a partir das folhas de S. occidentalis por Yakubu et al. (2018Yakubu, O.E., Otitoju, O., Imarenezor, E.P.K., Tatah, S.V. & Habibu, B. 2018. Fractionation and determination of antioxidant activities, of the Leaves of Senna Occidentalis ethanol extract. Pharmacology, 6: 26-30.) variou de 139 mg/mL a 206 mg/mL e de flavonoides de 104 a 142 mg/mL. Já para os extratos preparados a partir das folhas e casca do caule de S. siamea revelaram um teor de fenóis totais de 10,21 ± 0,25 g/g e 24,77 ± 0,15 g/g, respectivamente. Por outro lado, o teor de flavonoides foi de 0,08 ± 0,01 g/g para as folhagens, e de 0,04 ± 0,01 g/g para a casca do caule (Kwada & Tella 2009Kwada, A.D. & Tella, I.O. 2009. Determination of infochemicals and the phytochemical screening of the foliage and stem-bark of Senna siamea (lam.) in Yola, Adamawa State. Journal of Medicinal Plants Research 3: 630-640.). Para os extratos etanólicos das folhas e raízes de S. trachypus o teor de fenóis totais encontrado foi de 322,09 ± 2,83 EAG/g e de 1277,34 ± 79,54 EAG/g, respectivamente (Silva et al. 2014Silva, G.A., Monteiro, J.A., Ferreira, E.B., Fernandes, M.I.B., Pessoa, C.; Sampaio, C.G. & Silva, M.G.V. 2014. Total phenolic content, antioxidant and anticancer activities of four species of Senna Mill. From northeast Brazil. Int. J. Pharm. Pharm. Sci 6: 199-202.).Senna.

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Teor de fenóis totais, atividade antioxidante e inibição da enzima acetilcolinesterase de espécies de Senna Mill. (Fabaceae).
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Os resultados da atividade antioxidante dos extratos de Senna spp. mostraram que os valores de CE50 para o EEF variaram de 0,63 ± 0,01 a 8,20 ± 0,07 µg/mL, sendo o EEF de S. trachypus o que apresentou menor CE50 com atividade antirradicalar superior ao da quercetina e, portanto, maior potencial antioxidante (Villano et al. 2007Villano, D., Fernandez-Pachón, M.S., Moya, M.L., Troncoso, A.M. & García-Parrilla, M.C. 2007. Radical scavenging ability of polyphenolic compounds towards DPPH free radical. Talanta, 71: 230-235. ). Já para o EEC os valores de CE50 variaram de 0,83 ± 0,01 a 11,19 ± 0,15 µg/mL (Tabela 3). Foi observado que o EEC de S. siamea apresentou capacidade antirradicalar próximo à quercetina. Semelhantes aos nossos resultados, estudos anteriores revelaram que as espécies de S. alata, S. obtusifolia, S. occidentalis, S. siamea e S. trachypus, apresentaram potencial antioxidante e que esta atividade está atribuída à presença de compostos fenólicos (Coelho et al. 2017Coelho, E.M.P., Barbosa, M.C., Mito, M.S., Mantovanelli, G.C., Oliveira, R.S., & Ishii-Iwamoto, E.L. 2017. The activity of the antioxidant defense system of the weed species Senna obtusifolia L. and its resistance to allelochemical stress. Journal of Chemical Ecology 7: 725-738., Ita & Ndukwe 2017Ita, B.N., & Ndukwe, G.I. Antioxidant activity of Senna alata root extracts. 2017. J Nat Prod Resour 3: 94-96. , Barnaby et al. 2016Barnaby, A.G., Reid, R. & Warren, D. 2016. Antioxidant activity, total phenolics and fatty acid profile of Delonix regia, Cassia fistula, Spathodea campanulata, Senna siamea and Tibouchina granulosa. J Anal Pharm Res 3: 00056., Odeja et al. 2015Odeja, O., Obi, G., Ogwuche, C.E., Elemike, E.E. & Oderinlo, Y. 2015. Phytochemical Screening, Antioxidant and Antimicrobial activities of Senna occidentalis (L.) leaves Extract. Clinical Phytoscience 1: 1-6., Silva et al. 2014Silva, G.A., Monteiro, J.A., Ferreira, E.B., Fernandes, M.I.B., Pessoa, C.; Sampaio, C.G. & Silva, M.G.V. 2014. Total phenolic content, antioxidant and anticancer activities of four species of Senna Mill. From northeast Brazil. Int. J. Pharm. Pharm. Sci 6: 199-202.).

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Os resultados obtidos na análise de inibição da enzima acetilcolinesterase foram comparados ao do alcaloide fisostigmina que foi o primeiro inibidor descoberto. Os experimentos de inibição da enzima acetilcolinesterase in vitro para as espécies de Senna produziram apenas resultados com potência moderada (Tabela 3). Relatos confirmam a atividade antiacetilcolinesterásica de vários taninos isolados do fruto Terminalia chebula Retz., (Combretaceae) que exibiram um efeito de inibição contra a enzima acetilcolinesterase in vitro (Kim et al. 2018Kim, M.S., Lee, D.Y., Sung, S.H. & Jeon, W.K. 2018. Anti-cholinesterase activities of hydrolysable tannins and polyhydroxytriterpenoid derivatives from Terminalia chebula Retz. fruit. Fruit Rec Nat Prod 12: 284-289.). Outros compostos, como saponinas, alcaloides e compostos fenólicos, também são relatados na literatura como inibidores da enzima acetilcolinesterase (Paiva et al. 2021Paiva, J.R., Queiroz, S.A.S., Pereira, R.D.C.A., Ribeiro, P.R.V., Alves, F.E.G., Silva, L.M.A., Zocolo, G.J., Brito, E.S., Alves, D.R., Morais, S.M., Tavares, J., Pinto, F.C.L., Andrade, G.M., Pessoa, O.D.L., & Canuto, K.M. 2021. Chemical composition and anticholinesterase activity of cultivated bulbs from Hippeastrum elegans, a potential tropical source of bioactive alkaloids. Phytochemistry Letters 43: 27-34., Kozachok et al. 2020Kozachok, S., Pecio, Ł., Orhan, I.E., Deniz, F.S.S., Marchyshyn, S., & Oleszek, W. 2020. Reinvestigation of Herniaria glabra L. saponins and their biological activity. Phytochemistry 169: 112162., Adedayo et al. 2015Adedayo, B.C., Oboh, G., Oyeleye, S.I., Ejakpovi, I.I., Boligon, A.A., & Athayde, M.L. 2015. Blanching alters the phenolic constituents and in vitro antioxidant and anticholinesterases properties of fireweed (Crassocephalum crepidioides). Journal of Taibah University Medical Sciences 10: 419-426.). Estas classes de compostos foram detectadas na triagem fitoquímica, embora provavelmente as concentrações nos extratos eram muito baixas para dar resultados satisfatórios no ensaio. Os extratos foliares e do caule de S. trachypus apresentaram os valores mais satisfatórios de inibição da enzima acetilcolinesterase, indicando que o isolamento de metabólitos pode levar a potenciais agentes antiacetilcolinesterásicos. Na literatura, não foram encontrados estudos do potencial anticolinesterásico paras as espécies de Senna referenciadas, sendo este o primeiro relato de estudo de atividade de inibição para esta enzima.

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Para os extratos de Senna spp., foi observada forte correlação negativa entre os valores de fenóis totais e CE50 (r = - 0,71), mostrando que quanto maior os teores de fenóis totais, menor a CE50 e, consequentemente, maior o potencial antioxidante, uma vez que a CE50 está inversamente relacionada à capacidade antioxidante de um composto (Villano et al. 2007Villano, D., Fernandez-Pachón, M.S., Moya, M.L., Troncoso, A.M. & García-Parrilla, M.C. 2007. Radical scavenging ability of polyphenolic compounds towards DPPH free radical. Talanta, 71: 230-235. ). Dentre os extratos analisados podemos observar na figura 1 o EEF de S. trachypus.

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+Figura 1.
Correlação entre o teor de fenóis totais e CE50 de espécies de Senna Mill. (Fabaceae). Símbolos cheios: folhas. Símbolos vazados: caule.
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Na correlação da atividade de inibição da enzima acetilcolinesterase, representada pelo CI50 com teor de fenóis totais, observou-se uma correlação muito forte (r = -0,84) entre estas duas variáveis, evidenciando que ambas são inversamente proporcionais entre si, ou seja, à medida que o teor de fenóis totais aumenta o valor de CI50 diminui, como pode ser observado para o EEF de S. occidentalis (Figura 2). Isso demonstra que os compostos fenólicos podem ser determinantes nessa atividade, de modo que alguns estudos evidenciaram que flavonoides e outros compostos fenólicos possuem atividade anticolinesterásica (Amessis-Ouchemoukh et al. 2014Amessis-Ouchemoukh, N., Madani, K., Falé, P.L., Serralheiro, M.L., Araújo, M.E.M. 2014. Antioxidant capacity and phenolic contents of some Mediterranean medicinal plants and their potential role in the inhibition of cyclooxygenase-1 and acetylcholinesterase activities. Industrial Crops and Products, 53: 6-15.).

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+Figura 2.
Correlação entre o teor de fenóis totais e CI50 de espécies de Senna Mill. (Fabaceae). Símbolos cheios: folhas. Símbolos vazados: caule.
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Houve uma correlação moderada (r = 0,43) entre a CI50 e a CE50. Analisando a figura 3, é possível perceber que o EEF e EEC de S. alata e EEF de S. obtusifolia se destacam no gráfico, o que sugere uma grande capacidade dos antioxidantes, como os compostos fenólicos, presentes nos extratos analisados, de atuarem não só através da inibição da acetilcolinesterase (AChEI) mas também por mecanismos de redução de radicais livres.

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+Figura 3.
Correlação entre CI50 e a CE50 de espécies de Senna Mill. (Fabaceae). Símbolos cheios: folhas. Símbolos vazados: caule.
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Os extratos etanólicos das folhas e caule de S. alata, S. obtusifolia, S. occidentalis e S. siamea, apresentaram efeito inibitório contra algumas cepas de T. rubrum. A maioria dos extratos foram eficazes em diferentes concentrações, com CIM que variaram de 0,07 mg/mL à 2,5 mg/mL e CFM de 0,15 a 5,0 mg/mL contra a grande maioria das cepas fúngicas testadas. Dentre os extratos testados, os de S. trachypus foram eficazes contra todas as cepas de T. rubrum com CIM que variaram de 0,31 a 0,62 mg/mL e o CFM de 0,62 a 1,25 mg/mL, para ambos os extratos (Tabela 4). A presença de compostos fitoquímicos tem sido associada às atividades antimicrobianas da maioria dos materiais vegetais. Algumas classes de metabólitos foram identificadas nesse estudo e podem ser associadas à atividade antimicrobiana (Santos et al. 2018Santos, T.C.D., Gomes, T.M., Pinto, B.A.S., Camara, A.L. & Paes, A.M.D.A. 2018. Naturally occurring acetylcholinesterase inhibitors and their potential use for Alzheimer's disease therapy. Frontiers in Pharmacology 9: 1192., Odeja et al. 2015Odeja, O., Obi, G., Ogwuche, C.E., Elemike, E.E. & Oderinlo, Y. 2015. Phytochemical Screening, Antioxidant and Antimicrobial activities of Senna occidentalis (L.) leaves Extract. Clinical Phytoscience 1: 1-6.).

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+Tabela 4.
Concentração Inibitória Mínima (CIM) e Concentração Fungicida Mínima (CFM) de extratos etanólicos (EEs) de espécies de Senna Mill. (Fabaceae) frente às espécies de Trichophyton rubrum. LABIMIC: Laboratório de Microbiologia; EEF: Extrato etanólico da folha; EEC: Extrato etanólico do caule; NI: Não inibiu.
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Estudos anteriores realizados com o extrato etanólico da casca do caule de S. alata contra fungos dermatofíticos, entre eles espécies de Trychophyton, revelou um CIM de 5,0 mg/mL para todos os dermatófitos testados (Sule et al. 2011Sule, W.F., Okonko, I.O., Omo-Ogun, S., Nwanze, J.C., Ojezele, M.O., Ojezele, O.J., Alli, J.A., Soyemi, E.T. & Olaonipekun, T.O. 2011. Phytochemical properties and in-vitro antifungal activity of Senna alata Linn. crude stem bark extract. Journal of Medicinal Plants Research, 5: 176-183.). A capacidade antifúngica de extratos de diferentes polaridades preparados a partir das folhas de S. obtusifolia apresentaram um CIM que variou de 500 a 2000 µg/mL contra diferentes espécies de fungos filamentosos (Doughari et al. 2008Doughari, J.H., El-mahmood, A.M. & Tyoyina, I. 2008. Antimicrobial activity of leaf extracts of Senna obtusifolia (L). African Journal of Pharmacy and Pharmacology 2: 7-13.). Os resultados obtidos de extratos foliares de polaridades diferentes de S. occidentalis revelaram que o extrato metanólico mostrou maior atividade antifúngica entre os demais extratos testados, em uma concentração inibitória mínima de 25 mg/mL (Odeja et al. 2015Odeja, O., Obi, G., Ogwuche, C.E., Elemike, E.E. & Oderinlo, Y. 2015. Phytochemical Screening, Antioxidant and Antimicrobial activities of Senna occidentalis (L.) leaves Extract. Clinical Phytoscience 1: 1-6.). Testes utilizando extratos preparados com solventes de diferentes polaridades a partir das folhas de S. siamea apresentaram CIM que variaram de 0,032 a 0,128 mg/mL contra o fungo Cryptococcus gattii (Nnadi et al. 2019Nnadi, N.E., Anukam, N.C., Ayika, P.D., Rotdung, K., Gokum, S.S., Ayanbimpe, G.M., Nvau, J. & Enweani, I. 2019. The in Vitro antifungal activity of some Nigeria medicinal plants against Cryptococcus gattii. IOSR Journal of Pharmacy 9: 16-24. ). Na literatura, não foram encontrados estudos do potencial antifúngico para a espécie de S. trachypus, sendo este o primeiro registro de atividade antifúngica para a referida espécie.

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Pesquisas têm revelado que o potencial antifúngico de extratos vegetais está intimamente relacionado, entre outros fatores, com as suas variações quantitativas de compostos fenólicos, dentre eles os flavonoides. Nosso estudo confirmou que as espécies estudadas possuem propriedades antifúngicas, e que seus efeitos sobre os dermatófitos fundamentam-se em seus teores de compostos fenólicos encontrados, e os demais outros metabólitos secundários aqui não estudados. Os efeitos antifúngicos atribuídos aos compostos fenólicos podem resultar na ruptura da membrana celular, ou ainda, inibir a divisão celular e o desenvolvimento das hifas por meio de genes específicos, além de interferir nas vias metabólicas e/ou induzir a apoptose por perturbar a homeostase redox (Lagrouh et al. 2017Lagrouh, F., Dakka, N. & Bakri, Y. 2017.The antifungal activity of Moroccan plants and the mechanism of action of secondary metabolites from plants. Journal de Mycologie Medicale 27: 303-311., Mohamed et al. 2017Mohamed, M.S., Saleh, A.M., Abdel-Farid, I.B. & El-Naggar, S.A. 2017. Growth, hydrolases and ultrastructure of Fusarium oxysporum as affected by phenolic rich extracts from several xerophytic plants. Pesticide Biochemistry and Physiology 141: 57-64. ).

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Foram detectados, nos EEF e EEC das espécies de Senna, a presença de metabólitos secundários, alto teor de fenóis totais e capacidade antioxidante para todas as espécies, em especial S. trachypus. Para a atividade anticolinesterase apenas a espécie de S. trachypus manifestou uma melhor ação inibitória. Nas condições experimentais utilizadas, evidenciou-se atividade antifúngica das espécies frente a maioria dos dermatófitos testados, em especial os extratos de S. trachypus. Foi observada também correlação forte, muito forte e moderada entre as variáveis fenóis totais e atividade antioxidante, fenóis totais e antiacetilcolinesterase e atividade antioxidante e antiacetilcolinesterase, respectivamente. Os resultados apontam que S. trachypus, espécie endêmica da Caatinga, é a mais promissora entre todas as plantas estudadas, representando uma fonte potencial para a obtenção de compostos químicos úteis para estudos clínicos e farmacológicos, visando o desenvolvimento de novos agentes farmacológicos naturais.

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Agradecimentos

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Os autores agradecem a Universidade Estadual do Ceará (UECE) e a Universidade Estadual Vale do Acaraú (UVA) pelo apoio técnico, e a Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP) pelo apoio financeiro concedido (processos PBI3-0139-00252.01.00/18; BP4-0172-00170.01.00/20).

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  • Pellerin, R.J., Waminal, N.E. & Kim, H.H. 2019. FISH mapping of rDNA and telomeric repeats in 10 Senna species. Horticulture, Environment, and Biotechnology 60: 253-260.
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  • Penido, A.B., De Morais, S.M., Ribeiro, A.B., Alves, D.R., Rodrigues, A.L.M., dos Santos, L.H. & de Menezes, J.E.S.A. 2017. Medicinal plants from northeastern Brazil against Alzheimer’s disease. Evidence-Based Complementary and Alternative Medicine 2017: 1-7.
    • +
  • Queiroz, L.P. 2009. Leguminosas da Caatinga. Universidade Estadual de Feira de Santana, Feira de Santana, 467 p.
    • +
  • Rhee, I.K., van de Meent, M., Ingkaninan, K. & Verpoorte, R. 2001. Screening for acetylcholinesterase inhibitors from Amaryllidaceae using silica gel thin-layer chromatography in combination with bioactivity staining. Journal of Chromatography A 915: 217-223.
    • +
  • Rodrigues, F.C., Dos Santos, A.T.L., Machado, A.J.T., Bezerra, C.F., de Freitas, T.S., Coutinho, H.D.M., Morais-Braga, M.F.B., Bezerra, J.W.A., Duarte, A.E., Kamdem, J.P., Boligon, A.A., Campos, M.M.A., Barros, L.M. 2019. Chemical composition and anti-Candida potencial of the extracts of Tarenaya spinosa (Jacq.) Raf.(Cleomaceae). Comparative immunology, microbiology and infectious diseases 64: 14-19.
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  • Santos, G.H.F., Amaral, A. & Da Silva, E.B. 2018. Antibacterial activity of irradiated extracts of Anacardium occidentale L. on multiresistant strains of Staphylococcus aureus Applied Radiation and Isotopes 140: 327-332.
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  • Santos, T.C.D., Gomes, T.M., Pinto, B.A.S., Camara, A.L. & Paes, A.M.D.A. 2018. Naturally occurring acetylcholinesterase inhibitors and their potential use for Alzheimer's disease therapy. Frontiers in Pharmacology 9: 1192.
    • +
  • Sánchez‐Moreno, C., Larrauri, J.A. & Saura‐Calixto, F. 1998. A procedure to measure the antiradical efficiency of polyphenols. Journal of the Science of Food and Agriculture 76: 270-276.
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  • Silva, G.A., Monteiro, J.A., Ferreira, E.B., Fernandes, M.I.B., Pessoa, C.; Sampaio, C.G. & Silva, M.G.V. 2014. Total phenolic content, antioxidant and anticancer activities of four species of Senna Mill. From northeast Brazil. Int. J. Pharm. Pharm. Sci 6: 199-202.
    • +
  • Souza, V.C.; Bortoluzzi, R.L.C. 2015. Senna in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro.
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  • Sudi, I.Y., Ksgbiya, D.M., Muluh, E.K. & Clement, A. 2011. Nutritional and phytochemical screening of Senna obtusifolia indigenous to Mubi, Nigeria. Advances in Applied Science Research 2: 432-437.
    • +
  • Sule, W.F., Okonko, I.O., Omo-Ogun, S., Nwanze, J.C., Ojezele, M.O., Ojezele, O.J., Alli, J.A., Soyemi, E.T. & Olaonipekun, T.O. 2011. Phytochemical properties and in-vitro antifungal activity of Senna alata Linn. crude stem bark extract. Journal of Medicinal Plants Research, 5: 176-183.
    • +
  • Souza, A.O. & Silva, M.J. 2016. Senna (Leguminosae, Caesalpinioideae) na Floresta Nacional de Silvânia, Goiás, Brasil. Rodriguésia 67: 773-784.
    • +
  • Trevisan, M.T.S., Macedo, F.V.V., Meent, M.V.D., Rhee, I.K. & Verpoorte, R. 2003. Seleção de plantas com atividade anticolinesterase para tratamento da doença de Alzheimer. Química Nova 26: 301-304.
    • +
  • Villano, D., Fernandez-Pachón, M.S., Moya, M.L., Troncoso, A.M. & García-Parrilla, M.C. 2007. Radical scavenging ability of polyphenolic compounds towards DPPH free radical. Talanta, 71: 230-235.
    • +
  • Yakubu, O.E., Otitoju, O., Imarenezor, E.P.K., Tatah, S.V. & Habibu, B. 2018. Fractionation and determination of antioxidant activities, of the Leaves of Senna Occidentalis ethanol extract. Pharmacology, 6: 26-30.
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Datas de Publicação

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  • +Publicação nesta coleção
    21 Fev 2022
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  • +Data do Fascículo
    2022
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Histórico

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  • +Recebido
    14 Out 2020
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  • +Aceito
    03 Dez 2021
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Creative Common - by 4.0
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Este é um artigo publicado em acesso aberto sob uma licença Creative Commons
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+ + + diff --git a/tests/fixtures/aplicacao-design-system/2236-8906-hoehnea-49-e1112020/2236-8906-hoehnea-49-e1112020.xml b/tests/fixtures/aplicacao-design-system/2236-8906-hoehnea-49-e1112020/2236-8906-hoehnea-49-e1112020.xml new file mode 100644 index 000000000..05a6983fa --- /dev/null +++ b/tests/fixtures/aplicacao-design-system/2236-8906-hoehnea-49-e1112020/2236-8906-hoehnea-49-e1112020.xml @@ -0,0 +1,2597 @@ + + +
+ + + hoehnea + + Hoehnea + Hoehnea + + 0073-2877 + 2236-8906 + + Instituto de Pesquisas Ambientais + + + + 10.1590/2236-8906-111/2020 + 00208 + + + Artigo + + + + Prospecção química, atividade antioxidante, anticolinesterásica e antifúngica de extratos etanólicos de espécies de Senna Mill. (Fabaceae) + + Chemical prospecting and antioxidant, anticholinesterase and antifungal activity of ethanol extracts from Senna Mill. species. (Fabaceae) + + + + + 0000-0002-7388-1844 + + Neves + Andréa Maria + + 1 + 4 + + + 0000-0002-2766-3790 + + Morais + Selene Maia de + + 1 + + + 0000-0001-5527-164X + + Santos + Hélcio Silva dos + + 2 + + + 0000-0003-2503-9772 + + Ferreira + Marcílio Matos + + 3 + + + 0000-0002-2035-0425 + + Cruz + Ricardo Carneiro Vera + + 3 + + + 0000-0002-5222-4378 + + Souza + Elnatan Bezerra de + + 3 + + + 0000-0002-4384-5738 + + Andrade + Lúcia Betânia da Silva + + 3 + + + 0000-0002-8865-5954 + + Fontenelle + Raquel Oliveira dos Santos + + 3 + + + + + Universidade Estadual do Ceará, Centro de Ciências e Tecnologia, Programa de Pós-graduação em Biotecnologia, Avenida Doutor Silas Muguba, 1700, Itaperi, 60740-000 Fortaleza, CE, Brasil + Universidade Estadual do Ceará + Centro de Ciências e Tecnologia + Programa de Pós-graduação em Biotecnologia + + 60740-000 + Fortaleza + CE + + Brasil + + + + Universidade Estadual Vale do Acaraú, Centro de Ciências Exatas e Tecnologia, Curso de Química, Avenida da Universidade, 850, Betânia, 62040-370 Sobral, CE, Brasil + Universidade Estadual Vale do Acaraú + Centro de Ciências Exatas e Tecnologia + Curso de Química + + 62040-370 + Sobral + CE + + Brasil + + + + Universidade Estadual Vale do Acaraú, Centro de Ciências Agrárias e Biológicas, Curso de Ciências Biológicas, Avenida da Universidade, 850, Betânia, 62040-370 Sobral, CE, Brasil + Universidade Estadual Vale do Acaraú + Centro de Ciências Agrárias e Biológicas + Curso de Ciências Biológicas + + 62040-370 + Sobral + CE + + Brasil + + + + Autor para correspondência: andreamarianeves@gmail.com + + + +

Catarina Carvalho Nievola

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Andréa Maria Neves: Contribuição substancial em todas as etapas da pesquisa e para a confecção do manuscrito. Selene Maia de Morais: Contribuição na realização do teste de acetilcolinesterase; Contribuição na revisão crítica do manuscrito, agregando conteúdo intelectual. Hélcio Silva dos Santos: Contribuição na preparação dos extratos; Contribuição na revisão crítica do manuscrito, agregando conteúdo intelectual. Marcílio Matos Ferreira: Contribuição para a coleta das espécies e preparação dos extratos. Ricardo Carneiro Vera Cruz: Contribuição na realização dos testes fitoquímicos e quantificação de fenóis totais. Elnatan Bezerra de Souza: Contribuição na coleta e identificação das espécies; Contribuição na revisão crítica do manuscrito, agregando conteúdo intelectual. Lúcia Betânia da Silva Andrade: Contribuição na realização da atividade antioxidante, para a interpretação dos dados, e para revisão crítica, agregando conteúdo intelectual. Raquel Oliveira dos Santos Fontenelle: Contribuição nos testes antifúngicos e para revisão crítica, agregando conteúdo intelectual.

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Os autores declaram não haver conflitos de interesse a informar.

+ + + + 21 + 02 + 2022 + + + 2022 + + 49 + e1112020 + + + 14 + 10 + 2020 + + + 03 + 12 + 2021 + + + + + Este é um artigo publicado em acesso aberto sob uma licença Creative Commons + + + + RESUMO +

O objetivo deste trabalho foi avaliar o perfil químico, teor de fenóis totais e as atividades antioxidante, antiacetilcolinesterásica e antifúngica dos extratos etanólicos das folhas (EEF) e do caule (EEC) de cinco espécies de Senna, bem como avaliar a correlação entre o conteúdo de fenóis totais com a atividade sequestradora do radical livre DPPH e com a inibição da enzima acetilcolinesterase AChEI. No teste fitoquímico, evidenciou-se a presença de metabólitos secundários em todos os extratos. Os EEF e EEC de Senna trachypus, destacaram-se por apresentar os maiores valores de fenóis totais. Os EEF e EEC de S. trachypus mostraram a melhor ação sobre a enzima acetilcolinesterase. Todas as espécies apresentaram atividade antioxidante, em especial o EEF de S. trachypus. Foi observado correlação forte para as variáveis fenóis totais e atividade antioxidante (r = -0,71), muito forte para fenóis totais e antiacetilcolinesterase (r = -0,84) e atividade moderada para atividade antioxidante e antiacetilcolinesterase (0,43). Apenas os extratos de S. trachypus apresentaram atividade contra todos os dermatófitos, quando comparado às demais espécies. A espécie S. trachypus foi considerada a planta mais promissora para estudos subsequentes, a fim de encontrar compostos com ações farmacológicas.

+ + + ABSTRACT +

The objective of this work was to evaluate the chemical profile, total phenol content and the antioxidant, antiacetylcholinesterase and antifungal activities of ethanol extracts from leaves (EEF) and stem (EEC) of five species of Senna, as well as to evaluate the correlation between the content of total phenols with the DPPH free radical scavenging activity and with the inhibition of the acetylcholinesterase AChEI enzyme. The phytochemical test showed the presence of secondary metabolites in all extracts. The EEF and EEC of Senna trachypus, stood out for presenting the highest values of total phenols. S. trachypus EEF and EEC showed the best action on the acetylcholinesterase enzyme. All species showed antioxidant activity, especially the EEF from S. trachypus. A strong correlation was observed for the variables total phenols and antioxidant activity (r = -0.71), very strong for total phenols and anti-acetylcholinesterase (r = -0.84) and moderate activity for antioxidant and anti-acetylcholinesterase activity (r = 0.43). Only S. trachypus extracts showed activity against all dermatophytes, when compared to the other species. The species S. trachypus was considered the most promising plant for further studies, in order to find compounds with pharmacological actions.

+ + + Palavras-chave: + acetilcolinesterase + dermatófitos + fitoquímica + produtos naturais + radicais livres + + + Keywords: + acetylcholinesterase + dermatophytes + phytochemistry + natural products + free radicals + + + + FUNCAP + PBI3-0139-00252.01.00/18 + BP4-0172-00170.01.00/20 + + + + + + + + + + + + + Introdução +

Senna Mill. é um gênero monofilético com distribuição pantropical e ampla variedade morfológica (Pellerin et al. 2019). Possuindo aproximadamente 300 espécies, das quais 200 nas Américas, este gênero é o segundo maior da família Fabaceae (Queiroz 2009, Kim et al. 2018, Souza & Silva 2016). O gênero é representado no Brasil por 79 espécies, onde 29 são endêmicas, sendo a região Nordeste a que apresenta a maior riqueza de espécies com 53 registros (BFG 2018).

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Trata-se de um gênero muito expressivo na flora do semiárido, alcançando destaque no Domínio Fitogeográfico da Caatinga, onde são catalogadas 42 espécies (Souza & Bortoluzzi 2015). As espécies de Senna são geralmente arbustos ou arvoretas, raramente ervas ou subarbustos anuais. Entre as suas características diagnósticas estão os nectários extraflorais convexos, interfoliolares, flores vistosas, com pétalas amarelo-brilhantes, anteras amarelas, rígidas, com deiscência abrindo por poros ou fendas, ausência de bractéolas no pedicelo, frutos deiscentes plano-compressos ou indeiscentes e cilíndricos (Queiroz 2009).

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As espécies de Senna têm diversas aplicações medicinais e são eficazes no tratamento para uma série de doenças, como malária, micose, dengue, eczema, hepatite e dermatite, sendo também indicadas como anti-hipertensivo, vermífugo, laxante, abortivo e antitussígeno (Macedo et al. 2016, Bieski et al. 2015, Kabir et al. 2014). Além de suas aplicações farmacológicas, estudos têm revelado que espécies pertencentes a este gênero possuem, em sua composição, uma vasta diversidade de princípios bioativos que estão associadas a diferentes atividades biológicas. Neste sentido, podemos citar como exemplo as atividades antioxidantes, antitumoral, antibacterianas, antifúngicas e anti-inflamatórias (Neves et al. 2017).

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As plantas são fontes alternativas promissoras de substâncias de interesse biológico e farmacológico, já que podem produzir, a partir de seu metabolismo secundário, uma enorme diversidade de substâncias, dentre estas, os compostos fenólicos. Alguns estudos têm revelado que os compostos fenólicos são responsáveis por várias atividades biológicas, incluindo atividade antifúngica. Esta atividade pode ser direta nos micro-organismos, ou sobre outros fatores necessários para a expressão da virulência ou patogenicidade (Rodrigues et al. 2019).

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Os compostos fenólicos estão entre os metabólitos secundários mais estudados, notadamente por possuírem grande potencial para atividades antioxidantes, atuando na redução do risco de algumas doenças agudas e crônicas relacionadas ao estado redox do corpo humano, ocasionadas pelos radicais livres. Estas moléculas apresentam uma alta capacidade reativa, sendo consideradas perigosas para os organismos vivos, causando doenças prejudiciais, incluindo doenças neurodegenerativas, como o mal de Alzheimer (DA). Atualmente, uma das teorias mais aceitas na abordagem padrão no tratamento sintomático dessa demência é a “hipótese colinérgica”. Portanto, os inibidores da enzima acetilcolinesterase (AChEI) preservam os níveis de acetilcolina, melhorando a eficiência da transmissão colinérgica (Bardakci et al. 2019, Lim et al. 2019; Neagu et al. 2016).

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Por este motivo, a utilização de dietas ricas ou enriquecidas com antioxidantes podem prevenir, ou pelo menos amenizar, a deterioração orgânica por um excessivo estresse oxidativo. Além disso, o crescimento sobre a investigação científica envolvendo os efeitos antioxidantes de extratos brutos, frações purificadas, ou mesmo de compostos isolados, onde estão classificados os compostos fenólicos, são demonstrados em muitos estudos (Penido et al. 2017, Morais et al. 2013).

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Desta forma, investigar a atividade antifúngica e anticolinesterásica de extratos de espécies de Senna, analisando o seu potencial antioxidante, o seu teor de fenóis totais e o seu perfil fitoquímico, são maneiras de promover tanto o conhecimento acerca dessas espécies, como também potencializar o descobrimento de novos fitofármacos para o combate de inúmeras enfermidades. Assim, este trabalho avaliou o perfil fitoquímico, o teor de fenóis totais e as atividades antioxidante, anticolinesterásica e antifúngica dos extratos etanólicos de S. alata (L.) Roxb., S. obtusifolia (L.) H.S.Irwin & Barneby, S. occidentalis (L.) Link, S. siamea (Lam.) H.S.Irwin & Barneby e S. trachypus (Benth.) H.S.Irwin & Barneby, e a correlação entre o teor de fenóis totais e as atividades antioxidante e anticolinesterásica.

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Material vegetal e preparação dos extratos - Foram selecionadas para este estudo cinco espécies de Senna, sendo uma exótica naturalizada e quatro nativas, das quais uma é endêmica do Brasil, ocorrendo no Cerrado e na Caatinga (BFG 2018) (Tabela 1). As folhas e caules de Senna spp. foram coletados em diferentes locais da região Noroeste do Ceará. A identificação botânica das espécies foi realizada no Herbário Francisco José de Abreu Matos da Universidade Estadual Vale do Acaraú (HUVA), pelo professor Dr. Elnatan Bezerra de Souza. Para o preparo dos extratos, 200g das folhas e caule secos de cada espécie de um mesmo indivíduo foram triturados e imersos durante 10 dias em 500 mL de etanol e, na sequência o extrato foi filtrado e concentrado em um evaporador rotativo a (60°C) durante 2 h. Após este processo, foi mantido em banho-maria (40°C) até a eliminação total do solvente, obtendo-se o extrato etanólico das folhas (EEF) e extrato etanólico do caule (EEC) (Matos 2009).

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+ + + + Identificação das espécies de <italic>Senna</italic> Mill. (Fabaceae) coletadas em diferentes locais da região noroeste do Estado do Ceará. <sup>*</sup>Exótica, <sup>**</sup>Endêmica do Brasil. Fonte: Herbário Francisco José de Abreu Matos (HUVA). + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +
EspéciesNome popularLocal de coletaNo. HUVA
S. alata (L.) Roxb.fedegoso-giganteSobral21547
S. obtusifolia (L.) H.S.Irwin & Barnebyfedegoso-brandoGraça21775
S. occidentalis (L.) Linkcafé-negroGraça21774
S. siamea (Lam.) H.S.Irwin & Barneby*cássia-de-siãoSobral21578
S. trachypus (Benth.) H.S.Irwin & Barneby**pau-de-besouroGraça21776
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Table 1Identification of Senna Senna Mill. (Fabaceae) species collected in different locations in northwestern Ceará State. * Exotic, ** Endemic to Brazil. Source: Herbário Francisco José de Abreu Matos (HUVA).

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Triagem fitoquímica - Os extratos etanólicos foram submetidos a triagem fitoquímica, tomando como referência a metodologia descrita por Matos (2009). Através deste ensaio preliminar, foi possível verificar as principais classes de metabólitos secundários por meio de reações químicas que resultaram no aparecimento de coloração e/ou precipitado, característico para cada classe de substância. Os ensaios foram conduzidos para as seguintes classes de substâncias: fenóis, taninos, flavonoides, saponinas, esteroides, triterpenoides e alcaloides. Todos os testes foram realizados em triplicata procedimentais.

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Determinação do teor de fenóis totais - O teor de fenóis totais nos extratos etanólicos foi determinado pelo método espectrofotométrico de Folin-Ciocateau, utilizando ácido gálico como padrão de referência (Kim et al. 2006). Em cada tubo adicionou-se 0,2 mL de cada extrato nas concentrações (0,62; 0,31 e 0,15 mg mL-1) com 1 mL do reagente Folin-Ciocalteau agitado por 2 minutos e adicionado 0,8 mL de carbonato de sódio (Na2CO3) 7,5% (m/v). Para o tubo controle foi utilizado 1 mL do reagente Folin- Ciocalteau com 0,8 mL de Na2CO3 e 0,2 mL de etanol, em triplicata. Os tubos foram deixados em banho-maria a 37 ̊C por 30 minutos na ausência de luz. Logo em seguida, foi realizado a leitura dos tubos em comprimento de onda de 765 nm. O teor de fenóis foi calculado e expresso em mg de equivalente de ácido gálico por grama de extrato (EAG.g-1), com base numa curva padrão preparada com ácido gálico. Todos os testes foram realizados em triplicata.

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Atividade antioxidante - A atividade antioxidante dos extratos foi determinada pelo método de redução do radical 2,2’-difenil-1-picril-hidrazil (DPPH), segundo a metodologia modificada por Brand-Williams et al. (1995), Sanchez-Moreno et al. (1998). Foram preparadas soluções etanólicas das amostras nas concentrações de 5,0; 2,5; 1,25; 0,62; 0,31 e 0,15 mg mL-1. Foram utilizados 100 µL dos extratos com 2,4 mL de DPPH (0,04 mg mL-1). Para o tubo controle foram utilizados 100 µL de etanol com 2,4 mL de DPPH em triplicata. O meio reacional ficou por 30 minutos na ausência da luz, e posteriormente foi realizada a leitura em comprimento de onda 515 nm. A atividade sequestradora do radical DPPH pelos extratos nas diferentes concentrações foi calculada pela expressão do índice de varredura em porcentagem (IV%): IV% = (Abs DPPH - Abs Amostra / Abs DPPH) x 100. A concentração efetiva para inibir 50% do radical livre DPPH (CE50) foi obtida com auxílio do Software Excel 2019, onde, a partir dos valores das concentrações finais da amostra e o índice de varredura (IV%), foram originados gráficos de dispersão cujas equações das retas foram utilizadas para se obter os valores da média e desvio padrão. Para fins de comparação, foi construída uma curva de calibração com diferentes porcentagens do flavonoide quercetina, que apresenta elevada atividade antioxidante em radical livre DPPH.

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Avaliação da atividade anticolinesterásica in vitro - O ensaio para verificação da inibição da enzima acetilcolinesterase (AChE) dos extratos foi realizado de acordo com a metodologia descrita por Ellman et al. (1961). Em placas estéreis de 96 poços, foram adicionados 25 µL de iodeto de acetiltiocolina (15 mM), 125 µL de 5,5’-ditiobis-[2-nitrobenzóico] na solução Tris/HCL (50 nM, pH 8, com 0,1 M de NaCL e 0,02 M de MgCL2 .6H2O. (3 mM, DTNB ou reagente de Ellman)), 50 µL da solução Tris/HCL (50 nM, pH 8, com 0,1% de albumina sérica bovina (BSA) e 25 µL dos extratos de Senna spp. na concentraçao de 0,2 mg.mL-1 em tampão Tris/HCL (50 mM, pH 8) de 0,2 mg.mL-1 (Rhee et al. 2001, Trevisan et al. 2003).

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A absorbância foi aferida a 405 nm durante 30 segundos. Em seguida, foram adicionados 25 µL da enzima acetilcolinesterase (0,25 U.mL-1) e a absorbância foi aferida por minuto até o total de 25 minutos de incubação da enzima. Como padrão negativo foram utilizadas todas as soluções, excetuando-se a amostra. O padrão utilizado como controle positivo foi a fisostigmina (0,22 mg.mL-1.) e todas as amostras foram analisadas em triplicata. A atividade anticolinesterásica dos extratos vegetais foi determinada de acordo com os valores de CI50 (Concentração inibitória capaz de inibir 50% da enzima acetilcolinesterase) como: alta potência (CI50 < 20 μg. mL-1); potência moderada (20 < CI50 < 200 μg.mL-1) e baixa potência (200 < CI50 < 1000 μg.mL-1) (Santos et al. 2018).

+

Ensaio antifúngico in vitro - No ensaio para verificação da concentração inibitória mínima (CIM) dos EE das espécies de Senna, foram utilizadas cepas de Trichophyton rubrum obtidas a partir da micoteca da Universidade Federal de Pernambuco e do Centro Especializado de Micologia Médica (CEMM) da Universidade Federal do Ceará. Para este ensaio foi utilizado o método de microdiluição em caldo, de acordo com a metodologia descrita por (Neves et al. 2019) com as normas do protocolo Clinical Laboratory Standards Insitute do documento M38-A (CLSI M38-A2, 2008). Em placas de 96 poços estéreis, foram adicionados 100 µL de meio RPMI em todos os poços e 10 mg mL-1 dos extratos de Senna spp. foi acrescentado a todos os poços da primeira coluna e, em sequência foram efetuadas as diluições seriadas. Finalmente, 100 µL do inóculo foi adicionado aos poços da placa. Como controle foi utilizado o Cetoconazol (Sigma, Chemical Co., USA). Para as análises de susceptibilidade, os extratos etanólicos foram testados em concentrações variando de 0,002 a 2,5 mg mL-1. As placas foram cobertas com parafilme e incubadas a 37 °C e a leitura visual foi realizada após cinco dias para T. rubrum. Procedimento realizado em duplicata. A CIM é definida como a menor concentração do extrato capaz de inibir 100% do crescimento fúngico visível (Fontenelle et al. 2007). A concentração fungicida mínima (CFM) foi determinada por subcultura de 100 μL da solução de poços sem turbidez no meio Ágar Dextrose de Batata, a 28 °C. (Fontenelle et al. 2008).

+

Análise estatística - Todas as determinações foram realizadas em triplicata e todos os resultados foram apresentados como média ± desvio-padrão (DP). Foram realizadas análises de variância (ANOVA) com duas repetições e o Teste Tukey, ao nível de significância de 5%, usando programa Graph Pad Prism® v5.01 (GraphPadSoftware, San Diego, CA, E.U.A.). As diferenças entre as médias foram consideradas significativas quando o valor obtido para "p" foi menor que 0,05 (p < 0,05).

+

Para análises da correlação entre os dados, foi utilizado o coeficiente de correlação de Pearson no software Microsoft Excel 2019, a qual mede o grau da correlação linear entre duas variáveis quantitativas. A intensidade dessa correlação é dada pelo “r”, que é um índice adimensional com valores situados entre -1,0 e 1,0. Quando o valor de r estiver entre 0,00-0,19 a correlação é muito fraca; entre 0,20-0,39 é fraca; 0,40-0,59 é uma correlação moderada; entre 0,60-0,79 é forte e finalmente entre 0,80-1,0 diz-se que é uma correlação muito forte (Mukaka 2012).

+ + + Resultados e discussão<xref ref-type="table" rid="t3">Tabela 3</xref> +

Os fito-constituintes ou fitoquímicos são compostos químicos que desempenham importantes funções nas plantas. A triagem fitoquímica em materiais vegetais é geralmente o ponto de partida para o isolamento e purificação de compostos naturais com bioatividade (Omoregie & Oikeh 2015). A triagem fitoquímica preliminar revelou a presença de fenóis, taninos, flavonoides e esteroides para todos os extratos estudados (Tabela 2). Entretanto, a presença de saponinas foi constatada apenas no EEF e EEC de S. alata e no EEF de S. trachypus. Já os alcaloides foram encontrados exclusivamente no EEF de S. alata e nenhuma das espécies apresentou triterpenoides.

+

+ + + + Triagem fitoquímica do EEF e do EEC de espécies de <italic>Senna</italic> Mill. (Fabaceae)<italic>.</italic> Presente: + Ausente: - EEF: Extrato etanólico da folha. EEC: Extrato etanólico do caule. + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +
Espécies
MetabólitosS. alataS. obtusifoliaS. occidentalisS. siameaS. trachypus
ExtratosEEFEECEEFEECEEFEECEEFEECEEFEEC
Flavonoides++++++++++
Fenóis++++++++++
Saponinas++------+-
Taninos++++++++++
Esteroides++++++++++
Alcaloides+---------
Triterpenoides----------
+ + +

Table 2. Phytochemical screening of EEF and EEC of Senna Mill. (Fabaceae) species. Present: + Absent: - EEF: Ethanol extract of the leaf. EEC: Ethanol extract from the stem.

+ + + +

+

Os metabólitos detectados nas espécies estudadas são consistentes com os metabólitos descritos na literatura para o gênero Senna, conhecido por apresentar flavonoides, alcaloides, taninos, esteroides e saponinas em sua composição (Onyegeme-Okerenta et al. 2017, Ishaku et al. 2016, Silva et al. 2014, Sudi et al. 2011, Bukar et al. 2009). É possível perceber que na análise de prospecção química dos extratos houve uma variação de metabólitos secundários. Este fato pode estar atribuído a vários fatores, entre eles estão as diferentes condições ambientais, tais como clima, radiação solar, nutrição mineral, sazonalidade, ritmo circadiano, temperatura, disponibilidade hídrica, e também os tipos de solvente e a metodologia empregada no processo de extração, que podem interferir consideravelmente no conteúdo de praticamente todas as classes de metabólitos secundários (Gomes et al. 2016, Bezerra et al. 2013, Gobbo-Neto & Lopes 2007).

+

Os teores de fenóis totais apresentaram diferenças significativas entre os extratos etanólicos das diferentes partes e espécies vegetais estudadas (Tabela 3). O conteúdo de fenóis totais para os EEF variou de 32,60 ± 0,53 a 184,8 ± 5,09 EAG/g, enquanto que para o EEC foram de 30,03± 1,00 a 191,3 ± 0,47 EAG/g. Os maiores níveis de fenóis totais foram detectados na espécie S. trachypus. Os dados da literatura sobre o conteúdo de compostos fenólicos obtidos a partir do extrato aquoso, etanólico e acetona da raiz de S. alata, apresentaram uma concentração de fenóis de 46,3, 78,21 e 21,42 mg EAG/g, respectivamente, e de flavonoides de 26,17, 39,29 e 9,65 mg de equivalente de quercetina por grama de extrato (EQ/g), respectivamente (Ita & Ndukwe 2017). Já o extrato etanólico preparado a partir das folhas de S. obtusifolia por Ali et al. (2019), apresentou um teor de fenóis e de flavonoides de 14,39 mg/g e 2,85 mg/g, respectivamente, demonstrando possuir teor de compostos fenólicos inferior ao das mostras de S. obtusifolia encontradas no presente estudo. Além disso, o conteúdo de polifenóis encontrado no extrato etanólico e nas frações obtidas a partir das folhas de S. occidentalis por Yakubu et al. (2018) variou de 139 mg/mL a 206 mg/mL e de flavonoides de 104 a 142 mg/mL. Já para os extratos preparados a partir das folhas e casca do caule de S. siamea revelaram um teor de fenóis totais de 10,21 ± 0,25 g/g e 24,77 ± 0,15 g/g, respectivamente. Por outro lado, o teor de flavonoides foi de 0,08 ± 0,01 g/g para as folhagens, e de 0,04 ± 0,01 g/g para a casca do caule (Kwada & Tella 2009). Para os extratos etanólicos das folhas e raízes de S. trachypus o teor de fenóis totais encontrado foi de 322,09 ± 2,83 EAG/g e de 1277,34 ± 79,54 EAG/g, respectivamente (Silva et al. 2014).Senna.

+

+ + + + Teor de fenóis totais, atividade antioxidante e inibição da enzima acetilcolinesterase de espécies de Senna Mill. (Fabaceae). + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +
EspéciesFenois1 mg EAG.g-1 de extrato DPPH2 CE50 (μg.mL-1) AChEI3 CI50 (μg.mL-1)
MédiaDespadMédiaDespadMédiaDespad
S. alata (Folhas)53,76 f± 0,743,70 e± 0,0449,42 f± 0,02
S. alata (Caule)43,44 g± 0,215,41 c± 0,0653,25 d± 0,02
S. obtusifolia (Folhas)76,32 e± 0,414,24 d± 0,0650,37 e± 0,32
S. obtusifolia (Caule)86,20 d± 0,993,00 g± 0,0556,90 c± 0,02
S. occidentalis (Folhas)32,60 h± 0,538,20 b± 0,0758,76 b± 0,78
S. occidentalis (Caule)30,03 h± 1,0011,19 a± 0,1557,26 c± 0,02
S. siamea (Folhas)51,73 f± 0,853,34 f± 0,0559,77 a± 0,26
S. siamea (Caule)111,7 c± 3,430,83 i± 0,0159,52 ab± 0,15
S. trachypus (Folhas)184,80 b± 5,090,63 k± 0,0132,40 g± 0,12
S. trachypus (Caule)191,3 a± 0,472,52 h± 0,0331,44 h± 0,14
Quercetina--1,03 i± 0,00--
Fisiostigmina----1,15 i± 0,00
+ + +

Total phenol content, antioxidant activity and acetylcholinesterase enzyme inhibition of Senna Mill. (Fabaceae) species.

+ + +

Todas as análises foram realizadas em triplicada e os resultados foram expressos como média ± desvio padrão. As diferenças entre os valores foram examinadas usando análise de variância (ANOVA) e os resultados foram comparados usando o teste de Tukey com 95% nível de confiança. Letras diferentes denotam diferença estatística entre os valores de cada coluna (p < 0,05). 1Miligrama equivalente ao Ácido Gálico por grama de extrato; 2Concentração efetiva para inibir 50% do radical livre DPPH (2,2 -difenil-1-picril-hidrazil); 3Concentração inibitória capaz de inibir 50% da acetilcolinesterase. (-) Testes não realizados.

+ + +

All analyzes were performed in triplicate and the results were expressed as mean ± standard deviation. The differences between the values ​​were examined using analysis of variance (ANOVA) and the results were compared using the Tukey test at 95% confidence level. Different letters denote statistical difference between the values ​​of each column (p <0.05). 1 milligram Equivalent to Gallic Acid per gram of extract; 2Effective concentration to inhibit 50% of the free radical DPPH (2,2 - diphenyl - 1 - picryl - hydrazil); 3Inhibitory concentration capable of inhibiting 50% of acetylcholinesterase. (-) Tests not performed.

+ + + +

+

Os resultados da atividade antioxidante dos extratos de Senna spp. mostraram que os valores de CE50 para o EEF variaram de 0,63 ± 0,01 a 8,20 ± 0,07 µg/mL, sendo o EEF de S. trachypus o que apresentou menor CE50 com atividade antirradicalar superior ao da quercetina e, portanto, maior potencial antioxidante (Villano et al. 2007). Já para o EEC os valores de CE50 variaram de 0,83 ± 0,01 a 11,19 ± 0,15 µg/mL (Tabela 3). Foi observado que o EEC de S. siamea apresentou capacidade antirradicalar próximo à quercetina. Semelhantes aos nossos resultados, estudos anteriores revelaram que as espécies de S. alata, S. obtusifolia, S. occidentalis, S. siamea e S. trachypus, apresentaram potencial antioxidante e que esta atividade está atribuída à presença de compostos fenólicos (Coelho et al. 2017, Ita & Ndukwe 2017, Barnaby et al. 2016, Odeja et al. 2015, Silva et al. 2014).

+

Os resultados obtidos na análise de inibição da enzima acetilcolinesterase foram comparados ao do alcaloide fisostigmina que foi o primeiro inibidor descoberto. Os experimentos de inibição da enzima acetilcolinesterase in vitro para as espécies de Senna produziram apenas resultados com potência moderada (Tabela 3). Relatos confirmam a atividade antiacetilcolinesterásica de vários taninos isolados do fruto Terminalia chebula Retz., (Combretaceae) que exibiram um efeito de inibição contra a enzima acetilcolinesterase in vitro (Kim et al. 2018). Outros compostos, como saponinas, alcaloides e compostos fenólicos, também são relatados na literatura como inibidores da enzima acetilcolinesterase (Paiva et al. 2021, Kozachok et al. 2020, Adedayo et al. 2015). Estas classes de compostos foram detectadas na triagem fitoquímica, embora provavelmente as concentrações nos extratos eram muito baixas para dar resultados satisfatórios no ensaio. Os extratos foliares e do caule de S. trachypus apresentaram os valores mais satisfatórios de inibição da enzima acetilcolinesterase, indicando que o isolamento de metabólitos pode levar a potenciais agentes antiacetilcolinesterásicos. Na literatura, não foram encontrados estudos do potencial anticolinesterásico paras as espécies de Senna referenciadas, sendo este o primeiro relato de estudo de atividade de inibição para esta enzima.

+

Para os extratos de Senna spp., foi observada forte correlação negativa entre os valores de fenóis totais e CE50 (r = - 0,71), mostrando que quanto maior os teores de fenóis totais, menor a CE50 e, consequentemente, maior o potencial antioxidante, uma vez que a CE50 está inversamente relacionada à capacidade antioxidante de um composto (Villano et al. 2007). Dentre os extratos analisados podemos observar na figura 1 o EEF de S. trachypus.

+

+ + + + Correlação entre o teor de fenóis totais e CE50 de espécies de <italic>Senna</italic> Mill. (Fabaceae). Símbolos cheios: folhas. Símbolos vazados: caule. + + + Figure 1. Correlation between total phenol content and EC50 of Senna Mill species. (Fabaceae). Symbols filled: leaves. Hollow symbols: stem. + +

+

Na correlação da atividade de inibição da enzima acetilcolinesterase, representada pelo CI50 com teor de fenóis totais, observou-se uma correlação muito forte (r = -0,84) entre estas duas variáveis, evidenciando que ambas são inversamente proporcionais entre si, ou seja, à medida que o teor de fenóis totais aumenta o valor de CI50 diminui, como pode ser observado para o EEF de S. occidentalis (Figura 2). Isso demonstra que os compostos fenólicos podem ser determinantes nessa atividade, de modo que alguns estudos evidenciaram que flavonoides e outros compostos fenólicos possuem atividade anticolinesterásica (Amessis-Ouchemoukh et al. 2014).

+

+ + + + Correlação entre o teor de fenóis totais e CI50 de espécies de <italic>Senna</italic> Mill. (Fabaceae). Símbolos cheios: folhas. Símbolos vazados: caule. + + + Figure 2. Correlation between total phenol content and IC50 of Senna Mill species. (Fabaceae). Symbols filled: leaves. Hollow symbols: stem. + +

+

Houve uma correlação moderada (r = 0,43) entre a CI50 e a CE50. Analisando a figura 3, é possível perceber que o EEF e EEC de S. alata e EEF de S. obtusifolia se destacam no gráfico, o que sugere uma grande capacidade dos antioxidantes, como os compostos fenólicos, presentes nos extratos analisados, de atuarem não só através da inibição da acetilcolinesterase (AChEI) mas também por mecanismos de redução de radicais livres.

+

+ + + + Correlação entre CI50 e a CE50 de espécies de <italic>Senna</italic> Mill. (Fabaceae). Símbolos cheios: folhas. Símbolos vazados: caule. + + + Figure 3. Correlation between IC50 and EC50 of Senna Mill species. (Fabaceae). Symbols filled: leaves. Hollow symbols: stem. + +

+

Os extratos etanólicos das folhas e caule de S. alata, S. obtusifolia, S. occidentalis e S. siamea, apresentaram efeito inibitório contra algumas cepas de T. rubrum. A maioria dos extratos foram eficazes em diferentes concentrações, com CIM que variaram de 0,07 mg/mL à 2,5 mg/mL e CFM de 0,15 a 5,0 mg/mL contra a grande maioria das cepas fúngicas testadas. Dentre os extratos testados, os de S. trachypus foram eficazes contra todas as cepas de T. rubrum com CIM que variaram de 0,31 a 0,62 mg/mL e o CFM de 0,62 a 1,25 mg/mL, para ambos os extratos (Tabela 4). A presença de compostos fitoquímicos tem sido associada às atividades antimicrobianas da maioria dos materiais vegetais. Algumas classes de metabólitos foram identificadas nesse estudo e podem ser associadas à atividade antimicrobiana (Santos et al. 2018, Odeja et al. 2015).

+

+ + + + Concentração Inibitória Mínima (CIM) e Concentração Fungicida Mínima (CFM) de extratos etanólicos (EEs) de espécies de <italic>Senna</italic> Mill. (Fabaceae) frente às espécies de <italic>Trichophyton rubrum</italic>. LABIMIC: Laboratório de Microbiologia; EEF: Extrato etanólico da folha; EEC: Extrato etanólico do caule; NI: Não inibiu. + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +
EspéciesExtratoT. rubrumT. rubrumT. rubrumT. rubrum
LABIMIC 5906 LABIMIC 6213 LABIMIC 6205 LABIMIC 6753
CIMCFM CIM CFMCIMCFMCIMCFM
(mg/mL) (mg/mL) (mg/mL) (mg/mL)
S. alataEEFNI-NI-NI-2,55,0
EEC0,310,622,55,0NI-NI-
S. obtusifoliaEEFNI-2,55,0NI-0,621,25
EECNI-1,252,5NI-0,621,25
S. occidentalisEEF0,070,150,310,62NI-0,310,62
EECNI-NI-NI-NI-
S. siameaEEF0,621,251,252,50,621,251,252,5
EECNI-2,55,0NI-2,55,0
S. trachypusEEF0,621,250,310,620,310,620,310,62
EEC0,621,250,310,620,310,620,310,62
Cetoconazol 2,0 1,0 1,0 0,5
+ + +

Table 4. Minimum Inhibitory Concentration (MIC) and Minimum Fungicidal Concentration (MFC) of ethanolic extracts (EEs) from Senna Mill. LABIMIC: Microbiology Laboratory; EEF: Ethanol extract of the leaf; EEC: Ethanol extract from the stem; NI: It didn't inhibit. (Fabaceae) species compared to Trichophyton rubrum species.

+ + + +

+

Estudos anteriores realizados com o extrato etanólico da casca do caule de S. alata contra fungos dermatofíticos, entre eles espécies de Trychophyton, revelou um CIM de 5,0 mg/mL para todos os dermatófitos testados (Sule et al. 2011). A capacidade antifúngica de extratos de diferentes polaridades preparados a partir das folhas de S. obtusifolia apresentaram um CIM que variou de 500 a 2000 µg/mL contra diferentes espécies de fungos filamentosos (Doughari et al. 2008). Os resultados obtidos de extratos foliares de polaridades diferentes de S. occidentalis revelaram que o extrato metanólico mostrou maior atividade antifúngica entre os demais extratos testados, em uma concentração inibitória mínima de 25 mg/mL (Odeja et al. 2015). Testes utilizando extratos preparados com solventes de diferentes polaridades a partir das folhas de S. siamea apresentaram CIM que variaram de 0,032 a 0,128 mg/mL contra o fungo Cryptococcus gattii (Nnadi et al. 2019). Na literatura, não foram encontrados estudos do potencial antifúngico para a espécie de S. trachypus, sendo este o primeiro registro de atividade antifúngica para a referida espécie.

+

Pesquisas têm revelado que o potencial antifúngico de extratos vegetais está intimamente relacionado, entre outros fatores, com as suas variações quantitativas de compostos fenólicos, dentre eles os flavonoides. Nosso estudo confirmou que as espécies estudadas possuem propriedades antifúngicas, e que seus efeitos sobre os dermatófitos fundamentam-se em seus teores de compostos fenólicos encontrados, e os demais outros metabólitos secundários aqui não estudados. Os efeitos antifúngicos atribuídos aos compostos fenólicos podem resultar na ruptura da membrana celular, ou ainda, inibir a divisão celular e o desenvolvimento das hifas por meio de genes específicos, além de interferir nas vias metabólicas e/ou induzir a apoptose por perturbar a homeostase redox (Lagrouh et al. 2017, Mohamed et al. 2017).

+

Foram detectados, nos EEF e EEC das espécies de Senna, a presença de metabólitos secundários, alto teor de fenóis totais e capacidade antioxidante para todas as espécies, em especial S. trachypus. Para a atividade anticolinesterase apenas a espécie de S. trachypus manifestou uma melhor ação inibitória. Nas condições experimentais utilizadas, evidenciou-se atividade antifúngica das espécies frente a maioria dos dermatófitos testados, em especial os extratos de S. trachypus. Foi observada também correlação forte, muito forte e moderada entre as variáveis fenóis totais e atividade antioxidante, fenóis totais e antiacetilcolinesterase e atividade antioxidante e antiacetilcolinesterase, respectivamente. Os resultados apontam que S. trachypus, espécie endêmica da Caatinga, é a mais promissora entre todas as plantas estudadas, representando uma fonte potencial para a obtenção de compostos químicos úteis para estudos clínicos e farmacológicos, visando o desenvolvimento de novos agentes farmacológicos naturais.

+ + + + + Agradecimentos +

Os autores agradecem a Universidade Estadual do Ceará (UECE) e a Universidade Estadual Vale do Acaraú (UVA) pelo apoio técnico, e a Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP) pelo apoio financeiro concedido (processos PBI3-0139-00252.01.00/18; BP4-0172-00170.01.00/20).

+ + + Literatura citada + + Ali, I., Yisa, J. & Jacob, J.O. 2019. Corrosion inhibitory potential of ethanol extract of Senna obtusifolia on Mild Steel in 5M HCl. Journal of Chemical Society of Nigeria 44: 187-198. + + + + Ali + I. + + + Yisa + J. + + + Jacob + J.O. + + + 2019 + Corrosion inhibitory potential of ethanol extract of Senna obtusifolia on Mild Steel in 5M HCl. + Journal of Chemical Society of Nigeria + 44 + 187 + 198 + + + + Adedayo, B.C., Oboh, G., Oyeleye, S.I., Ejakpovi, I.I., Boligon, A.A., & Athayde, M.L. 2015. Blanching alters the phenolic constituents and in vitro antioxidant and anticholinesterases properties of fireweed (Crassocephalum crepidioides). 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+Artigo • Hoehnea 49 • 2022 • https://doi.org/10.1590/2236-8906-111/2020 +   + copiar +
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+Prospecção química, atividade antioxidante, anticolinesterásica e antifúngica de extratos etanólicos de espécies de Senna Mill. (Fabaceae) +

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Chemical prospecting and antioxidant, anticholinesterase and antifungal activity of ethanol extracts from Senna Mill. species. (Fabaceae)

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+ Andréa Maria Neves Selene Maia de Morais Hélcio Silva dos Santos Marcílio Matos Ferreira Ricardo Carneiro Vera Cruz Elnatan Bezerra de Souza Lúcia Betânia da Silva Andrade Raquel Oliveira dos Santos Fontenelle Sobre os autores +
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RESUMO

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O objetivo deste trabalho foi avaliar o perfil químico, teor de fenóis totais e as atividades antioxidante, antiacetilcolinesterásica e antifúngica dos extratos etanólicos das folhas (EEF) e do caule (EEC) de cinco espécies de Senna, bem como avaliar a correlação entre o conteúdo de fenóis totais com a atividade sequestradora do radical livre DPPH e com a inibição da enzima acetilcolinesterase AChEI. No teste fitoquímico, evidenciou-se a presença de metabólitos secundários em todos os extratos. Os EEF e EEC de Senna trachypus, destacaram-se por apresentar os maiores valores de fenóis totais. Os EEF e EEC de S. trachypus mostraram a melhor ação sobre a enzima acetilcolinesterase. Todas as espécies apresentaram atividade antioxidante, em especial o EEF de S. trachypus. Foi observado correlação forte para as variáveis fenóis totais e atividade antioxidante (r = -0,71), muito forte para fenóis totais e antiacetilcolinesterase (r = -0,84) e atividade moderada para atividade antioxidante e antiacetilcolinesterase (0,43). Apenas os extratos de S. trachypus apresentaram atividade contra todos os dermatófitos, quando comparado às demais espécies. A espécie S. trachypus foi considerada a planta mais promissora para estudos subsequentes, a fim de encontrar compostos com ações farmacológicas.

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Palavras-chave:
acetilcolinesterase; dermatófitos; fitoquímica; produtos naturais; radicais livres

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ABSTRACT

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The objective of this work was to evaluate the chemical profile, total phenol content and the antioxidant, antiacetylcholinesterase and antifungal activities of ethanol extracts from leaves (EEF) and stem (EEC) of five species of Senna, as well as to evaluate the correlation between the content of total phenols with the DPPH free radical scavenging activity and with the inhibition of the acetylcholinesterase AChEI enzyme. The phytochemical test showed the presence of secondary metabolites in all extracts. The EEF and EEC of Senna trachypus, stood out for presenting the highest values of total phenols. S. trachypus EEF and EEC showed the best action on the acetylcholinesterase enzyme. All species showed antioxidant activity, especially the EEF from S. trachypus. A strong correlation was observed for the variables total phenols and antioxidant activity (r = -0.71), very strong for total phenols and anti-acetylcholinesterase (r = -0.84) and moderate activity for antioxidant and anti-acetylcholinesterase activity (r = 0.43). Only S. trachypus extracts showed activity against all dermatophytes, when compared to the other species. The species S. trachypus was considered the most promising plant for further studies, in order to find compounds with pharmacological actions.

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Keywords:
acetylcholinesterase; dermatophytes; phytochemistry; natural products; free radicals

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Introdução

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Senna Mill. é um gênero monofilético com distribuição pantropical e ampla variedade morfológica (Pellerin et al. 2019Pellerin, R.J., Waminal, N.E. & Kim, H.H. 2019. FISH mapping of rDNA and telomeric repeats in 10 Senna species. Horticulture, Environment, and Biotechnology 60: 253-260.). Possuindo aproximadamente 300 espécies, das quais 200 nas Américas, este gênero é o segundo maior da família Fabaceae (Queiroz 2009Queiroz, L.P. 2009. Leguminosas da Caatinga. Universidade Estadual de Feira de Santana, Feira de Santana, 467 p., Kim et al. 2018Kim, M.S., Lee, D.Y., Sung, S.H. & Jeon, W.K. 2018. Anti-cholinesterase activities of hydrolysable tannins and polyhydroxytriterpenoid derivatives from Terminalia chebula Retz. fruit. Fruit Rec Nat Prod 12: 284-289., Souza & Silva 2016Souza, A.O. & Silva, M.J. 2016. Senna (Leguminosae, Caesalpinioideae) na Floresta Nacional de Silvânia, Goiás, Brasil. Rodriguésia 67: 773-784. ). O gênero é representado no Brasil por 79 espécies, onde 29 são endêmicas, sendo a região Nordeste a que apresenta a maior riqueza de espécies com 53 registros (BFG 2018BFG. 2018. Brazilian Flora 2020: Innovation and collaboration to meet Target 1 of the Global Strategy for Plant Conservation (GSPC). Rodriguésia 1513-1527. ).

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Trata-se de um gênero muito expressivo na flora do semiárido, alcançando destaque no Domínio Fitogeográfico da Caatinga, onde são catalogadas 42 espécies (Souza & Bortoluzzi 2015Souza, V.C.; Bortoluzzi, R.L.C. 2015. Senna in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. ). As espécies de Senna são geralmente arbustos ou arvoretas, raramente ervas ou subarbustos anuais. Entre as suas características diagnósticas estão os nectários extraflorais convexos, interfoliolares, flores vistosas, com pétalas amarelo-brilhantes, anteras amarelas, rígidas, com deiscência abrindo por poros ou fendas, ausência de bractéolas no pedicelo, frutos deiscentes plano-compressos ou indeiscentes e cilíndricos (Queiroz 2009Queiroz, L.P. 2009. Leguminosas da Caatinga. Universidade Estadual de Feira de Santana, Feira de Santana, 467 p.).

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As espécies de Senna têm diversas aplicações medicinais e são eficazes no tratamento para uma série de doenças, como malária, micose, dengue, eczema, hepatite e dermatite, sendo também indicadas como anti-hipertensivo, vermífugo, laxante, abortivo e antitussígeno (Macedo et al. 2016Macedo, E.M., Alan, J.G., & Silva, M.G.V. 2016. Quimiodiversidade e propriedades biofarmacológicas de espécies de Senna nativas do Nordeste do Brasil. Revista Virtual de Química 8: 169-195., Bieski et al. 2015Bieski, I.G.C., Leonti, M., Arnason, J.T., Ferrier, J., Rapinski, M., Violante, I.M.P., Balogun,S.O., Pereira, J.F.C.A., Figueiredo, R.D.C.F., Lopes, C.R.A.S., Silva, D.R.D., Pacini, A., Albuquerque, U.P. & Martins, D.T.D.O. 2015. Ethnobotanical study of medicinal plants by population of valley of Juruena region, legal amazon, Mato Grosso, Brazil. Journal of Ethnopharmacology 173: 383-423., Kabir et al. 2014Kabir, M.H., Hasan, N., Rahman, M.M., Rahman, M.A., Khan, J.A., Hoque, N.T., Bhuiyan, M.R.Q., Mou, S.M.; Jahan, R. & Rahmatullah, M. 2014. A survey of medicinal plants used by the Deb barma clan of the Tripura tribe of Moulvibazar district, Bangladesh. Journal of Ethnobiology and Ethnomedicine 10: 1-19.). Além de suas aplicações farmacológicas, estudos têm revelado que espécies pertencentes a este gênero possuem, em sua composição, uma vasta diversidade de princípios bioativos que estão associadas a diferentes atividades biológicas. Neste sentido, podemos citar como exemplo as atividades antioxidantes, antitumoral, antibacterianas, antifúngicas e anti-inflamatórias (Neves et al. 2017Neves, A.M., Costa, O.S., Coutinho, M.G.S., Souza, E.B., Santos, H.S., Silva, M.G.V. & Fontenelle, R.O.S. 2017. Caracterização química e o potencial antimicrobiano de espécies do gênero Senna Mill (Fabaceae). Rev. Virtual Quim 9: 2506-2538.).

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As plantas são fontes alternativas promissoras de substâncias de interesse biológico e farmacológico, já que podem produzir, a partir de seu metabolismo secundário, uma enorme diversidade de substâncias, dentre estas, os compostos fenólicos. Alguns estudos têm revelado que os compostos fenólicos são responsáveis por várias atividades biológicas, incluindo atividade antifúngica. Esta atividade pode ser direta nos micro-organismos, ou sobre outros fatores necessários para a expressão da virulência ou patogenicidade (Rodrigues et al. 2019Rodrigues, F.C., Dos Santos, A.T.L., Machado, A.J.T., Bezerra, C.F., de Freitas, T.S., Coutinho, H.D.M., Morais-Braga, M.F.B., Bezerra, J.W.A., Duarte, A.E., Kamdem, J.P., Boligon, A.A., Campos, M.M.A., Barros, L.M. 2019. Chemical composition and anti-Candida potencial of the extracts of Tarenaya spinosa (Jacq.) Raf.(Cleomaceae). Comparative immunology, microbiology and infectious diseases 64: 14-19.).

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Os compostos fenólicos estão entre os metabólitos secundários mais estudados, notadamente por possuírem grande potencial para atividades antioxidantes, atuando na redução do risco de algumas doenças agudas e crônicas relacionadas ao estado redox do corpo humano, ocasionadas pelos radicais livres. Estas moléculas apresentam uma alta capacidade reativa, sendo consideradas perigosas para os organismos vivos, causando doenças prejudiciais, incluindo doenças neurodegenerativas, como o mal de Alzheimer (DA). Atualmente, uma das teorias mais aceitas na abordagem padrão no tratamento sintomático dessa demência é a “hipótese colinérgica”. Portanto, os inibidores da enzima acetilcolinesterase (AChEI) preservam os níveis de acetilcolina, melhorando a eficiência da transmissão colinérgica (Bardakci et al. 2019Bardakci, H., CeleP, E., Gözet, T., Kan, Y. & Kirmizibekmez, H. 2019. Phytochemical characterization and antioxidant activities of the fruit extracts of several Crataegus taxa. South African Journal of Botany 124: 5-13. , Lim et al. 2019Lim, S., Choi, A.H., Kwon, M., Joung, E.J., Shin, T., Lee, S.G., Kim, NG. & Kim, H. R. 2019. Evaluation of antioxidant activities of various solvent extract from Sargassum serratifolium and its major antioxidant components. Food Chemistry 278: 178-184.; Neagu et al. 2016Neagu, E., Radu, G.L., Albu, C., & Paun, G. 2016. Antioxidant activity, acetylcholinesterase and tyrosinase inhibitory potential of Pulmonaria officinalis and Centarium umbellatum extracts. Saudi Journal of Biological Sciences, 3: 578-585.).

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Por este motivo, a utilização de dietas ricas ou enriquecidas com antioxidantes podem prevenir, ou pelo menos amenizar, a deterioração orgânica por um excessivo estresse oxidativo. Além disso, o crescimento sobre a investigação científica envolvendo os efeitos antioxidantes de extratos brutos, frações purificadas, ou mesmo de compostos isolados, onde estão classificados os compostos fenólicos, são demonstrados em muitos estudos (Penido et al. 2017Penido, A.B., De Morais, S.M., Ribeiro, A.B., Alves, D.R., Rodrigues, A.L.M., dos Santos, L.H. & de Menezes, J.E.S.A. 2017. Medicinal plants from northeastern Brazil against Alzheimer’s disease. Evidence-Based Complementary and Alternative Medicine 2017: 1-7. , Morais et al. 2013Morais, S.M., Lima, K.S.B., Siqueira, S.M.C., Cavalcanti, E.S.B., Souza, M.S.T., Menezes, J.E.S.A., Trevisan, M.T.S. 2013. Correlação entre as atividades antiradical, antiacetilcolinesterase e teor de fenóis totais de extratos de plantas medicinais de farmácias vivas. Revista Brasileira de Plantas Medicinais 15: 575-582. ).

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Desta forma, investigar a atividade antifúngica e anticolinesterásica de extratos de espécies de Senna, analisando o seu potencial antioxidante, o seu teor de fenóis totais e o seu perfil fitoquímico, são maneiras de promover tanto o conhecimento acerca dessas espécies, como também potencializar o descobrimento de novos fitofármacos para o combate de inúmeras enfermidades. Assim, este trabalho avaliou o perfil fitoquímico, o teor de fenóis totais e as atividades antioxidante, anticolinesterásica e antifúngica dos extratos etanólicos de S. alata (L.) Roxb., S. obtusifolia (L.) H.S.Irwin & Barneby, S. occidentalis (L.) Link, S. siamea (Lam.) H.S.Irwin & Barneby e S. trachypus (Benth.) H.S.Irwin & Barneby, e a correlação entre o teor de fenóis totais e as atividades antioxidante e anticolinesterásica.

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Materiais e métodos

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Material vegetal e preparação dos extratos - Foram selecionadas para este estudo cinco espécies de Senna, sendo uma exótica naturalizada e quatro nativas, das quais uma é endêmica do Brasil, ocorrendo no Cerrado e na Caatinga (BFG 2018BFG. 2018. Brazilian Flora 2020: Innovation and collaboration to meet Target 1 of the Global Strategy for Plant Conservation (GSPC). Rodriguésia 1513-1527. ) (Tabela 1). As folhas e caules de Senna spp. foram coletados em diferentes locais da região Noroeste do Ceará. A identificação botânica das espécies foi realizada no Herbário Francisco José de Abreu Matos da Universidade Estadual Vale do Acaraú (HUVA), pelo professor Dr. Elnatan Bezerra de Souza. Para o preparo dos extratos, 200g das folhas e caule secos de cada espécie de um mesmo indivíduo foram triturados e imersos durante 10 dias em 500 mL de etanol e, na sequência o extrato foi filtrado e concentrado em um evaporador rotativo a (60°C) durante 2 h. Após este processo, foi mantido em banho-maria (40°C) até a eliminação total do solvente, obtendo-se o extrato etanólico das folhas (EEF) e extrato etanólico do caule (EEC) (Matos 2009Matos, F.J.A. 2009. Introdução à Fitoquímica Experimental. 3 ed. Fortaleza: UFC. 150p.).

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Identificação das espécies de Senna Mill. (Fabaceae) coletadas em diferentes locais da região noroeste do Estado do Ceará. *Exótica, **Endêmica do Brasil. Fonte: Herbário Francisco José de Abreu Matos (HUVA).
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Triagem fitoquímica - Os extratos etanólicos foram submetidos a triagem fitoquímica, tomando como referência a metodologia descrita por Matos (2009Matos, F.J.A. 2009. Introdução à Fitoquímica Experimental. 3 ed. Fortaleza: UFC. 150p.). Através deste ensaio preliminar, foi possível verificar as principais classes de metabólitos secundários por meio de reações químicas que resultaram no aparecimento de coloração e/ou precipitado, característico para cada classe de substância. Os ensaios foram conduzidos para as seguintes classes de substâncias: fenóis, taninos, flavonoides, saponinas, esteroides, triterpenoides e alcaloides. Todos os testes foram realizados em triplicata procedimentais.

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Determinação do teor de fenóis totais - O teor de fenóis totais nos extratos etanólicos foi determinado pelo método espectrofotométrico de Folin-Ciocateau, utilizando ácido gálico como padrão de referência (Kim et al. 2006Kim, K.H., Tsao, R., Yang, R. & Cui, S.W. 2006. Phenolic acid profiles and antioxidant activities of wheat bran extracts and the effect of hydrolysis conditions. Food Chemistry 95: 466-473.). Em cada tubo adicionou-se 0,2 mL de cada extrato nas concentrações (0,62; 0,31 e 0,15 mg mL-1) com 1 mL do reagente Folin-Ciocalteau agitado por 2 minutos e adicionado 0,8 mL de carbonato de sódio (Na2CO3) 7,5% (m/v). Para o tubo controle foi utilizado 1 mL do reagente Folin- Ciocalteau com 0,8 mL de Na2CO3 e 0,2 mL de etanol, em triplicata. Os tubos foram deixados em banho-maria a 37 ̊C por 30 minutos na ausência de luz. Logo em seguida, foi realizado a leitura dos tubos em comprimento de onda de 765 nm. O teor de fenóis foi calculado e expresso em mg de equivalente de ácido gálico por grama de extrato (EAG.g-1), com base numa curva padrão preparada com ácido gálico. Todos os testes foram realizados em triplicata.

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Atividade antioxidante - A atividade antioxidante dos extratos foi determinada pelo método de redução do radical 2,2’-difenil-1-picril-hidrazil (DPPH), segundo a metodologia modificada por Brand-Williams et al. (1995Brand-Williams, W., Cuvelier, M.E. & Berset, C.L.W.T. 1995. Use of a free radical method to evaluate antioxidant activity. LWT-Food Science and Technology 1: 25-30.), Sanchez-Moreno et al. (1998Sánchez‐Moreno, C., Larrauri, J.A. & Saura‐Calixto, F. 1998. A procedure to measure the antiradical efficiency of polyphenols. Journal of the Science of Food and Agriculture 76: 270-276.). Foram preparadas soluções etanólicas das amostras nas concentrações de 5,0; 2,5; 1,25; 0,62; 0,31 e 0,15 mg mL-1. Foram utilizados 100 µL dos extratos com 2,4 mL de DPPH (0,04 mg mL-1). Para o tubo controle foram utilizados 100 µL de etanol com 2,4 mL de DPPH em triplicata. O meio reacional ficou por 30 minutos na ausência da luz, e posteriormente foi realizada a leitura em comprimento de onda 515 nm. A atividade sequestradora do radical DPPH pelos extratos nas diferentes concentrações foi calculada pela expressão do índice de varredura em porcentagem (IV%): IV% = (Abs DPPH - Abs Amostra / Abs DPPH) x 100. A concentração efetiva para inibir 50% do radical livre DPPH (CE50) foi obtida com auxílio do Software Excel 2019, onde, a partir dos valores das concentrações finais da amostra e o índice de varredura (IV%), foram originados gráficos de dispersão cujas equações das retas foram utilizadas para se obter os valores da média e desvio padrão. Para fins de comparação, foi construída uma curva de calibração com diferentes porcentagens do flavonoide quercetina, que apresenta elevada atividade antioxidante em radical livre DPPH.

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Avaliação da atividade anticolinesterásica in vitro - O ensaio para verificação da inibição da enzima acetilcolinesterase (AChE) dos extratos foi realizado de acordo com a metodologia descrita por Ellman et al. (1961Ellman, G.L., Courtney, K.D., Andres Jr, V. & Featherstone, R.M. 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology: 7: 88-95.). Em placas estéreis de 96 poços, foram adicionados 25 µL de iodeto de acetiltiocolina (15 mM), 125 µL de 5,5’-ditiobis-[2-nitrobenzóico] na solução Tris/HCL (50 nM, pH 8, com 0,1 M de NaCL e 0,02 M de MgCL2 .6H2O. (3 mM, DTNB ou reagente de Ellman)), 50 µL da solução Tris/HCL (50 nM, pH 8, com 0,1% de albumina sérica bovina (BSA) e 25 µL dos extratos de Senna spp. na concentraçao de 0,2 mg.mL-1 em tampão Tris/HCL (50 mM, pH 8) de 0,2 mg.mL-1 (Rhee et al. 2001Rhee, I.K., van de Meent, M., Ingkaninan, K. & Verpoorte, R. 2001. Screening for acetylcholinesterase inhibitors from Amaryllidaceae using silica gel thin-layer chromatography in combination with bioactivity staining. Journal of Chromatography A 915: 217-223., Trevisan et al. 2003Trevisan, M.T.S., Macedo, F.V.V., Meent, M.V.D., Rhee, I.K. & Verpoorte, R. 2003. Seleção de plantas com atividade anticolinesterase para tratamento da doença de Alzheimer. Química Nova 26: 301-304.).

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A absorbância foi aferida a 405 nm durante 30 segundos. Em seguida, foram adicionados 25 µL da enzima acetilcolinesterase (0,25 U.mL-1) e a absorbância foi aferida por minuto até o total de 25 minutos de incubação da enzima. Como padrão negativo foram utilizadas todas as soluções, excetuando-se a amostra. O padrão utilizado como controle positivo foi a fisostigmina (0,22 mg.mL-1.) e todas as amostras foram analisadas em triplicata. A atividade anticolinesterásica dos extratos vegetais foi determinada de acordo com os valores de CI50 (Concentração inibitória capaz de inibir 50% da enzima acetilcolinesterase) como: alta potência (CI50 < 20 μg. mL-1); potência moderada (20 < CI50 < 200 μg.mL-1) e baixa potência (200 < CI50 < 1000 μg.mL-1) (Santos et al. 2018Santos, G.H.F., Amaral, A. & Da Silva, E.B. 2018. Antibacterial activity of irradiated extracts of Anacardium occidentale L. on multiresistant strains of Staphylococcus aureus. Applied Radiation and Isotopes 140: 327-332.).

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Ensaio antifúngico in vitro - No ensaio para verificação da concentração inibitória mínima (CIM) dos EE das espécies de Senna, foram utilizadas cepas de Trichophyton rubrum obtidas a partir da micoteca da Universidade Federal de Pernambuco e do Centro Especializado de Micologia Médica (CEMM) da Universidade Federal do Ceará. Para este ensaio foi utilizado o método de microdiluição em caldo, de acordo com a metodologia descrita por (Neves et al. 2019Neves, A.M., Silva, H.S., Souza, E.B., Fontenelle, R.O.S., Silva, A.C.S., Morais, S.M. 2019. Perfil fitoquímico e avaliação da atividade antifúngica da fração hexânica de Mitracarpus baturitensis (Rubiaceae). Essentia 20: 96-101. ) com as normas do protocolo Clinical Laboratory Standards Insitute do documento M38-A (CLSI M38-A2, 2008Clinical and Laboratory Standards Institute. 2008. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi (Approved Standard Document M38. CLSI), vol. M38-A2, Second ed. Clinical and Laboratory Standards Institute, Wayne, PA.). Em placas de 96 poços estéreis, foram adicionados 100 µL de meio RPMI em todos os poços e 10 mg mL-1 dos extratos de Senna spp. foi acrescentado a todos os poços da primeira coluna e, em sequência foram efetuadas as diluições seriadas. Finalmente, 100 µL do inóculo foi adicionado aos poços da placa. Como controle foi utilizado o Cetoconazol (Sigma, Chemical Co., USA). Para as análises de susceptibilidade, os extratos etanólicos foram testados em concentrações variando de 0,002 a 2,5 mg mL-1. As placas foram cobertas com parafilme e incubadas a 37 °C e a leitura visual foi realizada após cinco dias para T. rubrum. Procedimento realizado em duplicata. A CIM é definida como a menor concentração do extrato capaz de inibir 100% do crescimento fúngico visível (Fontenelle et al. 2007Fontenelle, R.O.S., Morais, S.M., Brito, E.H.S., Kerntopf, M.R., Brilhante, R.S.N., Cordeiro, R.A., Tomé, A.R., Queiroz, M.G.R., Nascimento, N.R.F. & Sidrim, J.J.C. 2007. Chemical composition, toxicological aspects and antifungal activity of essential oil from Lippia sidoides Cham. Journal of Antimicrobial Chemotherapy 59: 934-940. ). A concentração fungicida mínima (CFM) foi determinada por subcultura de 100 μL da solução de poços sem turbidez no meio Ágar Dextrose de Batata, a 28 °C. (Fontenelle et al. 2008Fontenelle, R.O.S., Morais, S.M., Brito, E.H.S., Brilhante, R.S.N., Cordeiro, R.A., Nascimento, N.R.F., Kerntopf, M.R., Sidrim, J.J.C. & Rocha, M.F.G. 2008. Antifungal activity of essential oils of Croton species from the Brazilian caatinga biome. Journal of Applied Microbiology 104: 1383-1390.).

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Análise estatística - Todas as determinações foram realizadas em triplicata e todos os resultados foram apresentados como média ± desvio-padrão (DP). Foram realizadas análises de variância (ANOVA) com duas repetições e o Teste Tukey, ao nível de significância de 5%, usando programa Graph Pad Prism® v5.01 (GraphPadSoftware, San Diego, CA, E.U.A.). As diferenças entre as médias foram consideradas significativas quando o valor obtido para "p" foi menor que 0,05 (p < 0,05).

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Para análises da correlação entre os dados, foi utilizado o coeficiente de correlação de Pearson no software Microsoft Excel 2019, a qual mede o grau da correlação linear entre duas variáveis quantitativas. A intensidade dessa correlação é dada pelo “r”, que é um índice adimensional com valores situados entre -1,0 e 1,0. Quando o valor de r estiver entre 0,00-0,19 a correlação é muito fraca; entre 0,20-0,39 é fraca; 0,40-0,59 é uma correlação moderada; entre 0,60-0,79 é forte e finalmente entre 0,80-1,0 diz-se que é uma correlação muito forte (Mukaka 2012Mukaka, M.M. 2012. Statistics corner: A guide to appropriate use of correlation coefficient in medical research. Malawi Med J. 24:69-71.).

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Resultados e discussãoTabela 3 +

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Os fito-constituintes ou fitoquímicos são compostos químicos que desempenham importantes funções nas plantas. A triagem fitoquímica em materiais vegetais é geralmente o ponto de partida para o isolamento e purificação de compostos naturais com bioatividade (Omoregie & Oikeh 2015Omoregie, E.S. & Oikeh, E.I. 2015. Comparative studies on the phytochemical composition, phenolic content and antioxidant activities of methanol leaf extracts of Spondias mombin and Polyathia longifolia. Jordan Journal of Biological Sciences 147: 1-5.). A triagem fitoquímica preliminar revelou a presença de fenóis, taninos, flavonoides e esteroides para todos os extratos estudados (Tabela 2). Entretanto, a presença de saponinas foi constatada apenas no EEF e EEC de S. alata e no EEF de S. trachypus. Já os alcaloides foram encontrados exclusivamente no EEF de S. alata e nenhuma das espécies apresentou triterpenoides.

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Triagem fitoquímica do EEF e do EEC de espécies de Senna Mill. (Fabaceae). Presente: + Ausente: - EEF: Extrato etanólico da folha. EEC: Extrato etanólico do caule.
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Os metabólitos detectados nas espécies estudadas são consistentes com os metabólitos descritos na literatura para o gênero Senna, conhecido por apresentar flavonoides, alcaloides, taninos, esteroides e saponinas em sua composição (Onyegeme-Okerenta et al. 2017Onyegeme-Okerenta, B.M., Nwosu, T. & Wegwu, M.O. 2017. Proximate and phytochemical composition of leaf extract of Senna alata (L) Roxb. Journal of Pharmacognosy and Phytochemistry 6: 320-326., Ishaku et al. 2016Ishaku, G.A., Arabo, A.A., Bassey, E.E., Uwem, A.A.U.M. & Godwin, E.U. 2016. Physicochemical characterization and antibacterial activity of Senna occidentalis Linn. Journal of Chemistryand Chemical Sciences 6: 9-18. , Silva et al. 2014Silva, G.A., Monteiro, J.A., Ferreira, E.B., Fernandes, M.I.B., Pessoa, C.; Sampaio, C.G. & Silva, M.G.V. 2014. Total phenolic content, antioxidant and anticancer activities of four species of Senna Mill. From northeast Brazil. Int. J. Pharm. Pharm. Sci 6: 199-202., Sudi et al. 2011Sudi, I.Y., Ksgbiya, D.M., Muluh, E.K. & Clement, A. 2011. Nutritional and phytochemical screening of Senna obtusifolia indigenous to Mubi, Nigeria. Advances in Applied Science Research 2: 432-437., Bukar et al. 2009Bukar, A., Mukhtar, M. & HASSAN, A. 2009. Phytochemical screening and antibacterial activity of leaf extracts of Senna siamea (Lam) on Pseudomonas aeruginosa. Bayero Journal of Pure and Applied Sciences 1: 139-142. ). É possível perceber que na análise de prospecção química dos extratos houve uma variação de metabólitos secundários. Este fato pode estar atribuído a vários fatores, entre eles estão as diferentes condições ambientais, tais como clima, radiação solar, nutrição mineral, sazonalidade, ritmo circadiano, temperatura, disponibilidade hídrica, e também os tipos de solvente e a metodologia empregada no processo de extração, que podem interferir consideravelmente no conteúdo de praticamente todas as classes de metabólitos secundários (Gomes et al. 2016Gomes, E.M.C., Pena, R.D.C.M. & da Silva, S.S.S.M. 2016. Composição fitoquímica e ação fungicida de extratos brutos de Cinnamomum zeylanicum sobre Quambalaria eucalypti. Biota Amazônia. 6: 54-58., Bezerra et al. 2013Bezerra, A.S., Nörnberg, J.L., Lima, F.O., Rosa, M.B.D. & Carvalho, L.M.D. 2013. Parâmetros climáticos e variação de compostos fenólicos em cevada. Ciência Rural 9: 1546-1552., Gobbo-Neto & Lopes 2007Gobbo-Neto, L. & Lopes, N.P. 2007. Plantas medicinais: Fatores de influência no conteúdo de metabólitos secundários. Química Nova 30: 374-381.).

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Os teores de fenóis totais apresentaram diferenças significativas entre os extratos etanólicos das diferentes partes e espécies vegetais estudadas (Tabela 3). O conteúdo de fenóis totais para os EEF variou de 32,60 ± 0,53 a 184,8 ± 5,09 EAG/g, enquanto que para o EEC foram de 30,03± 1,00 a 191,3 ± 0,47 EAG/g. Os maiores níveis de fenóis totais foram detectados na espécie S. trachypus. Os dados da literatura sobre o conteúdo de compostos fenólicos obtidos a partir do extrato aquoso, etanólico e acetona da raiz de S. alata, apresentaram uma concentração de fenóis de 46,3, 78,21 e 21,42 mg EAG/g, respectivamente, e de flavonoides de 26,17, 39,29 e 9,65 mg de equivalente de quercetina por grama de extrato (EQ/g), respectivamente (Ita & Ndukwe 2017Ita, B.N., & Ndukwe, G.I. Antioxidant activity of Senna alata root extracts. 2017. J Nat Prod Resour 3: 94-96. ). Já o extrato etanólico preparado a partir das folhas de S. obtusifolia por Ali et al. (2019Ali, I., Yisa, J. & Jacob, J.O. 2019. Corrosion inhibitory potential of ethanol extract of Senna obtusifolia on Mild Steel in 5M HCl. Journal of Chemical Society of Nigeria 44: 187-198. ), apresentou um teor de fenóis e de flavonoides de 14,39 mg/g e 2,85 mg/g, respectivamente, demonstrando possuir teor de compostos fenólicos inferior ao das mostras de S. obtusifolia encontradas no presente estudo. Além disso, o conteúdo de polifenóis encontrado no extrato etanólico e nas frações obtidas a partir das folhas de S. occidentalis por Yakubu et al. (2018Yakubu, O.E., Otitoju, O., Imarenezor, E.P.K., Tatah, S.V. & Habibu, B. 2018. Fractionation and determination of antioxidant activities, of the Leaves of Senna Occidentalis ethanol extract. Pharmacology, 6: 26-30.) variou de 139 mg/mL a 206 mg/mL e de flavonoides de 104 a 142 mg/mL. Já para os extratos preparados a partir das folhas e casca do caule de S. siamea revelaram um teor de fenóis totais de 10,21 ± 0,25 g/g e 24,77 ± 0,15 g/g, respectivamente. Por outro lado, o teor de flavonoides foi de 0,08 ± 0,01 g/g para as folhagens, e de 0,04 ± 0,01 g/g para a casca do caule (Kwada & Tella 2009Kwada, A.D. & Tella, I.O. 2009. Determination of infochemicals and the phytochemical screening of the foliage and stem-bark of Senna siamea (lam.) in Yola, Adamawa State. Journal of Medicinal Plants Research 3: 630-640.). Para os extratos etanólicos das folhas e raízes de S. trachypus o teor de fenóis totais encontrado foi de 322,09 ± 2,83 EAG/g e de 1277,34 ± 79,54 EAG/g, respectivamente (Silva et al. 2014Silva, G.A., Monteiro, J.A., Ferreira, E.B., Fernandes, M.I.B., Pessoa, C.; Sampaio, C.G. & Silva, M.G.V. 2014. Total phenolic content, antioxidant and anticancer activities of four species of Senna Mill. From northeast Brazil. Int. J. Pharm. Pharm. Sci 6: 199-202.).Senna.

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Teor de fenóis totais, atividade antioxidante e inibição da enzima acetilcolinesterase de espécies de Senna Mill. (Fabaceae).
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Os resultados da atividade antioxidante dos extratos de Senna spp. mostraram que os valores de CE50 para o EEF variaram de 0,63 ± 0,01 a 8,20 ± 0,07 µg/mL, sendo o EEF de S. trachypus o que apresentou menor CE50 com atividade antirradicalar superior ao da quercetina e, portanto, maior potencial antioxidante (Villano et al. 2007Villano, D., Fernandez-Pachón, M.S., Moya, M.L., Troncoso, A.M. & García-Parrilla, M.C. 2007. Radical scavenging ability of polyphenolic compounds towards DPPH free radical. Talanta, 71: 230-235. ). Já para o EEC os valores de CE50 variaram de 0,83 ± 0,01 a 11,19 ± 0,15 µg/mL (Tabela 3). Foi observado que o EEC de S. siamea apresentou capacidade antirradicalar próximo à quercetina. Semelhantes aos nossos resultados, estudos anteriores revelaram que as espécies de S. alata, S. obtusifolia, S. occidentalis, S. siamea e S. trachypus, apresentaram potencial antioxidante e que esta atividade está atribuída à presença de compostos fenólicos (Coelho et al. 2017Coelho, E.M.P., Barbosa, M.C., Mito, M.S., Mantovanelli, G.C., Oliveira, R.S., & Ishii-Iwamoto, E.L. 2017. The activity of the antioxidant defense system of the weed species Senna obtusifolia L. and its resistance to allelochemical stress. Journal of Chemical Ecology 7: 725-738., Ita & Ndukwe 2017Ita, B.N., & Ndukwe, G.I. Antioxidant activity of Senna alata root extracts. 2017. J Nat Prod Resour 3: 94-96. , Barnaby et al. 2016Barnaby, A.G., Reid, R. & Warren, D. 2016. Antioxidant activity, total phenolics and fatty acid profile of Delonix regia, Cassia fistula, Spathodea campanulata, Senna siamea and Tibouchina granulosa. J Anal Pharm Res 3: 00056., Odeja et al. 2015Odeja, O., Obi, G., Ogwuche, C.E., Elemike, E.E. & Oderinlo, Y. 2015. Phytochemical Screening, Antioxidant and Antimicrobial activities of Senna occidentalis (L.) leaves Extract. Clinical Phytoscience 1: 1-6., Silva et al. 2014Silva, G.A., Monteiro, J.A., Ferreira, E.B., Fernandes, M.I.B., Pessoa, C.; Sampaio, C.G. & Silva, M.G.V. 2014. Total phenolic content, antioxidant and anticancer activities of four species of Senna Mill. From northeast Brazil. Int. J. Pharm. Pharm. Sci 6: 199-202.).

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Os resultados obtidos na análise de inibição da enzima acetilcolinesterase foram comparados ao do alcaloide fisostigmina que foi o primeiro inibidor descoberto. Os experimentos de inibição da enzima acetilcolinesterase in vitro para as espécies de Senna produziram apenas resultados com potência moderada (Tabela 3). Relatos confirmam a atividade antiacetilcolinesterásica de vários taninos isolados do fruto Terminalia chebula Retz., (Combretaceae) que exibiram um efeito de inibição contra a enzima acetilcolinesterase in vitro (Kim et al. 2018Kim, M.S., Lee, D.Y., Sung, S.H. & Jeon, W.K. 2018. Anti-cholinesterase activities of hydrolysable tannins and polyhydroxytriterpenoid derivatives from Terminalia chebula Retz. fruit. Fruit Rec Nat Prod 12: 284-289.). Outros compostos, como saponinas, alcaloides e compostos fenólicos, também são relatados na literatura como inibidores da enzima acetilcolinesterase (Paiva et al. 2021Paiva, J.R., Queiroz, S.A.S., Pereira, R.D.C.A., Ribeiro, P.R.V., Alves, F.E.G., Silva, L.M.A., Zocolo, G.J., Brito, E.S., Alves, D.R., Morais, S.M., Tavares, J., Pinto, F.C.L., Andrade, G.M., Pessoa, O.D.L., & Canuto, K.M. 2021. Chemical composition and anticholinesterase activity of cultivated bulbs from Hippeastrum elegans, a potential tropical source of bioactive alkaloids. Phytochemistry Letters 43: 27-34., Kozachok et al. 2020Kozachok, S., Pecio, Ł., Orhan, I.E., Deniz, F.S.S., Marchyshyn, S., & Oleszek, W. 2020. Reinvestigation of Herniaria glabra L. saponins and their biological activity. Phytochemistry 169: 112162., Adedayo et al. 2015Adedayo, B.C., Oboh, G., Oyeleye, S.I., Ejakpovi, I.I., Boligon, A.A., & Athayde, M.L. 2015. Blanching alters the phenolic constituents and in vitro antioxidant and anticholinesterases properties of fireweed (Crassocephalum crepidioides). Journal of Taibah University Medical Sciences 10: 419-426.). Estas classes de compostos foram detectadas na triagem fitoquímica, embora provavelmente as concentrações nos extratos eram muito baixas para dar resultados satisfatórios no ensaio. Os extratos foliares e do caule de S. trachypus apresentaram os valores mais satisfatórios de inibição da enzima acetilcolinesterase, indicando que o isolamento de metabólitos pode levar a potenciais agentes antiacetilcolinesterásicos. Na literatura, não foram encontrados estudos do potencial anticolinesterásico paras as espécies de Senna referenciadas, sendo este o primeiro relato de estudo de atividade de inibição para esta enzima.

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Para os extratos de Senna spp., foi observada forte correlação negativa entre os valores de fenóis totais e CE50 (r = - 0,71), mostrando que quanto maior os teores de fenóis totais, menor a CE50 e, consequentemente, maior o potencial antioxidante, uma vez que a CE50 está inversamente relacionada à capacidade antioxidante de um composto (Villano et al. 2007Villano, D., Fernandez-Pachón, M.S., Moya, M.L., Troncoso, A.M. & García-Parrilla, M.C. 2007. Radical scavenging ability of polyphenolic compounds towards DPPH free radical. Talanta, 71: 230-235. ). Dentre os extratos analisados podemos observar na figura 1 o EEF de S. trachypus.

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Correlação entre o teor de fenóis totais e CE50 de espécies de Senna Mill. (Fabaceae). Símbolos cheios: folhas. Símbolos vazados: caule.
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Na correlação da atividade de inibição da enzima acetilcolinesterase, representada pelo CI50 com teor de fenóis totais, observou-se uma correlação muito forte (r = -0,84) entre estas duas variáveis, evidenciando que ambas são inversamente proporcionais entre si, ou seja, à medida que o teor de fenóis totais aumenta o valor de CI50 diminui, como pode ser observado para o EEF de S. occidentalis (Figura 2). Isso demonstra que os compostos fenólicos podem ser determinantes nessa atividade, de modo que alguns estudos evidenciaram que flavonoides e outros compostos fenólicos possuem atividade anticolinesterásica (Amessis-Ouchemoukh et al. 2014Amessis-Ouchemoukh, N., Madani, K., Falé, P.L., Serralheiro, M.L., Araújo, M.E.M. 2014. Antioxidant capacity and phenolic contents of some Mediterranean medicinal plants and their potential role in the inhibition of cyclooxygenase-1 and acetylcholinesterase activities. Industrial Crops and Products, 53: 6-15.).

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Correlação entre o teor de fenóis totais e CI50 de espécies de Senna Mill. (Fabaceae). Símbolos cheios: folhas. Símbolos vazados: caule.
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Houve uma correlação moderada (r = 0,43) entre a CI50 e a CE50. Analisando a figura 3, é possível perceber que o EEF e EEC de S. alata e EEF de S. obtusifolia se destacam no gráfico, o que sugere uma grande capacidade dos antioxidantes, como os compostos fenólicos, presentes nos extratos analisados, de atuarem não só através da inibição da acetilcolinesterase (AChEI) mas também por mecanismos de redução de radicais livres.

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Correlação entre CI50 e a CE50 de espécies de Senna Mill. (Fabaceae). Símbolos cheios: folhas. Símbolos vazados: caule.
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Os extratos etanólicos das folhas e caule de S. alata, S. obtusifolia, S. occidentalis e S. siamea, apresentaram efeito inibitório contra algumas cepas de T. rubrum. A maioria dos extratos foram eficazes em diferentes concentrações, com CIM que variaram de 0,07 mg/mL à 2,5 mg/mL e CFM de 0,15 a 5,0 mg/mL contra a grande maioria das cepas fúngicas testadas. Dentre os extratos testados, os de S. trachypus foram eficazes contra todas as cepas de T. rubrum com CIM que variaram de 0,31 a 0,62 mg/mL e o CFM de 0,62 a 1,25 mg/mL, para ambos os extratos (Tabela 4). A presença de compostos fitoquímicos tem sido associada às atividades antimicrobianas da maioria dos materiais vegetais. Algumas classes de metabólitos foram identificadas nesse estudo e podem ser associadas à atividade antimicrobiana (Santos et al. 2018Santos, T.C.D., Gomes, T.M., Pinto, B.A.S., Camara, A.L. & Paes, A.M.D.A. 2018. Naturally occurring acetylcholinesterase inhibitors and their potential use for Alzheimer's disease therapy. Frontiers in Pharmacology 9: 1192., Odeja et al. 2015Odeja, O., Obi, G., Ogwuche, C.E., Elemike, E.E. & Oderinlo, Y. 2015. Phytochemical Screening, Antioxidant and Antimicrobial activities of Senna occidentalis (L.) leaves Extract. Clinical Phytoscience 1: 1-6.).

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Concentração Inibitória Mínima (CIM) e Concentração Fungicida Mínima (CFM) de extratos etanólicos (EEs) de espécies de Senna Mill. (Fabaceae) frente às espécies de Trichophyton rubrum. LABIMIC: Laboratório de Microbiologia; EEF: Extrato etanólico da folha; EEC: Extrato etanólico do caule; NI: Não inibiu.
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Estudos anteriores realizados com o extrato etanólico da casca do caule de S. alata contra fungos dermatofíticos, entre eles espécies de Trychophyton, revelou um CIM de 5,0 mg/mL para todos os dermatófitos testados (Sule et al. 2011Sule, W.F., Okonko, I.O., Omo-Ogun, S., Nwanze, J.C., Ojezele, M.O., Ojezele, O.J., Alli, J.A., Soyemi, E.T. & Olaonipekun, T.O. 2011. Phytochemical properties and in-vitro antifungal activity of Senna alata Linn. crude stem bark extract. Journal of Medicinal Plants Research, 5: 176-183.). A capacidade antifúngica de extratos de diferentes polaridades preparados a partir das folhas de S. obtusifolia apresentaram um CIM que variou de 500 a 2000 µg/mL contra diferentes espécies de fungos filamentosos (Doughari et al. 2008Doughari, J.H., El-mahmood, A.M. & Tyoyina, I. 2008. Antimicrobial activity of leaf extracts of Senna obtusifolia (L). African Journal of Pharmacy and Pharmacology 2: 7-13.). Os resultados obtidos de extratos foliares de polaridades diferentes de S. occidentalis revelaram que o extrato metanólico mostrou maior atividade antifúngica entre os demais extratos testados, em uma concentração inibitória mínima de 25 mg/mL (Odeja et al. 2015Odeja, O., Obi, G., Ogwuche, C.E., Elemike, E.E. & Oderinlo, Y. 2015. Phytochemical Screening, Antioxidant and Antimicrobial activities of Senna occidentalis (L.) leaves Extract. Clinical Phytoscience 1: 1-6.). Testes utilizando extratos preparados com solventes de diferentes polaridades a partir das folhas de S. siamea apresentaram CIM que variaram de 0,032 a 0,128 mg/mL contra o fungo Cryptococcus gattii (Nnadi et al. 2019Nnadi, N.E., Anukam, N.C., Ayika, P.D., Rotdung, K., Gokum, S.S., Ayanbimpe, G.M., Nvau, J. & Enweani, I. 2019. The in Vitro antifungal activity of some Nigeria medicinal plants against Cryptococcus gattii. IOSR Journal of Pharmacy 9: 16-24. ). Na literatura, não foram encontrados estudos do potencial antifúngico para a espécie de S. trachypus, sendo este o primeiro registro de atividade antifúngica para a referida espécie.

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Pesquisas têm revelado que o potencial antifúngico de extratos vegetais está intimamente relacionado, entre outros fatores, com as suas variações quantitativas de compostos fenólicos, dentre eles os flavonoides. Nosso estudo confirmou que as espécies estudadas possuem propriedades antifúngicas, e que seus efeitos sobre os dermatófitos fundamentam-se em seus teores de compostos fenólicos encontrados, e os demais outros metabólitos secundários aqui não estudados. Os efeitos antifúngicos atribuídos aos compostos fenólicos podem resultar na ruptura da membrana celular, ou ainda, inibir a divisão celular e o desenvolvimento das hifas por meio de genes específicos, além de interferir nas vias metabólicas e/ou induzir a apoptose por perturbar a homeostase redox (Lagrouh et al. 2017Lagrouh, F., Dakka, N. & Bakri, Y. 2017.The antifungal activity of Moroccan plants and the mechanism of action of secondary metabolites from plants. Journal de Mycologie Medicale 27: 303-311., Mohamed et al. 2017Mohamed, M.S., Saleh, A.M., Abdel-Farid, I.B. & El-Naggar, S.A. 2017. Growth, hydrolases and ultrastructure of Fusarium oxysporum as affected by phenolic rich extracts from several xerophytic plants. Pesticide Biochemistry and Physiology 141: 57-64. ).

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Foram detectados, nos EEF e EEC das espécies de Senna, a presença de metabólitos secundários, alto teor de fenóis totais e capacidade antioxidante para todas as espécies, em especial S. trachypus. Para a atividade anticolinesterase apenas a espécie de S. trachypus manifestou uma melhor ação inibitória. Nas condições experimentais utilizadas, evidenciou-se atividade antifúngica das espécies frente a maioria dos dermatófitos testados, em especial os extratos de S. trachypus. Foi observada também correlação forte, muito forte e moderada entre as variáveis fenóis totais e atividade antioxidante, fenóis totais e antiacetilcolinesterase e atividade antioxidante e antiacetilcolinesterase, respectivamente. Os resultados apontam que S. trachypus, espécie endêmica da Caatinga, é a mais promissora entre todas as plantas estudadas, representando uma fonte potencial para a obtenção de compostos químicos úteis para estudos clínicos e farmacológicos, visando o desenvolvimento de novos agentes farmacológicos naturais.

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Agradecimentos

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Os autores agradecem a Universidade Estadual do Ceará (UECE) e a Universidade Estadual Vale do Acaraú (UVA) pelo apoio técnico, e a Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP) pelo apoio financeiro concedido (processos PBI3-0139-00252.01.00/18; BP4-0172-00170.01.00/20).

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Datas de Publicação

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  • +Publicação nesta coleção
    21 Fev 2022
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  • +Data do Fascículo
    2022
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Histórico

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  • +Recebido
    14 Out 2020
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  • +Aceito
    03 Dez 2021
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Autor para correspondência: Sobre os autores
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    RESUMO

    O objetivo deste trabalho foi avaliar o perfil químico, teor de fenóis totais e as atividades antioxidante, antiacetilcolinesterásica e antifúngica dos extratos etanólicos das folhas (EEF) e do caule (EEC) de cinco espécies de Senna, bem como avaliar a correlação entre o conteúdo de fenóis totais com a atividade sequestradora do radical livre DPPH e com a inibição da enzima acetilcolinesterase AChEI. No teste fitoquímico, evidenciou-se a presença de metabólitos secundários em todos os extratos. Os EEF e EEC de Senna trachypus, destacaram-se por apresentar os maiores valores de fenóis totais. Os EEF e EEC de S. trachypus mostraram a melhor ação sobre a enzima acetilcolinesterase. Todas as espécies apresentaram atividade antioxidante, em especial o EEF de S. trachypus. Foi observado correlação forte para as variáveis fenóis totais e atividade antioxidante (r = -0,71), muito forte para fenóis totais e antiacetilcolinesterase (r = -0,84) e atividade moderada para atividade antioxidante e antiacetilcolinesterase (0,43). Apenas os extratos de S. trachypus apresentaram atividade contra todos os dermatófitos, quando comparado às demais espécies. A espécie S. trachypus foi considerada a planta mais promissora para estudos subsequentes, a fim de encontrar compostos com ações farmacológicas.

    Palavras-chave:
    acetilcolinesterase; dermatófitos; fitoquímica; produtos naturais; radicais livres

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    Autor para correspondência: http://orcid.org/0000-0002-4384-5738 Raquel Oliveira dos Santos Fontenelle Sobre os autores +Sobre os autores
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      Introdução

      Por este motivo, a utilização de dietas ricas ou enriquecidas com antioxidantes podem prevenir, ou pelo menos amenizar, a deterioração orgânica por um excessivo estresse oxidativo. Além disso, o crescimento sobre a investigação científica envolvendo os efeitos antioxidantes de extratos brutos, frações purificadas, ou mesmo de compostos isolados, onde estão classificados os compostos fenólicos, são demonstrados em muitos estudos (Penido et al. 2017Penido, A.B., De Morais, S.M., Ribeiro, A.B., Alves, D.R., Rodrigues, A.L.M., dos Santos, L.H. & de Menezes, J.E.S.A. 2017. Medicinal plants from northeastern Brazil against Alzheimer’s disease. Evidence-Based Complementary and Alternative Medicine 2017: 1-7. , Morais et al. 2013Morais, S.M., Lima, K.S.B., Siqueira, S.M.C., Cavalcanti, E.S.B., Souza, M.S.T., Menezes, J.E.S.A., Trevisan, M.T.S. 2013. Correlação entre as atividades antiradical, antiacetilcolinesterase e teor de fenóis totais de extratos de plantas medicinais de farmácias vivas. Revista Brasileira de Plantas Medicinais 15: 575-582. ).

      Desta forma, investigar a atividade antifúngica e anticolinesterásica de extratos de espécies de Senna, analisando o seu potencial antioxidante, o seu teor de fenóis totais e o seu perfil fitoquímico, são maneiras de promover tanto o conhecimento acerca dessas espécies, como também potencializar o descobrimento de novos fitofármacos para o combate de inúmeras enfermidades. Assim, este trabalho avaliou o perfil fitoquímico, o teor de fenóis totais e as atividades antioxidante, anticolinesterásica e antifúngica dos extratos etanólicos de S. alata (L.) Roxb., S. obtusifolia (L.) H.S.Irwin & Barneby, S. occidentalis (L.) Link, S. siamea (Lam.) H.S.Irwin & Barneby e S. trachypus (Benth.) H.S.Irwin & Barneby, e a correlação entre o teor de fenóis totais e as atividades antioxidante e anticolinesterásica.

      Materiais e métodos

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      Material vegetal e preparação dos extratos - Foram selecionadas para este estudo cinco espécies de Senna, sendo uma exótica naturalizada e quatro nativas, das quais uma é endêmica do Brasil, ocorrendo no Cerrado e na Caatinga (BFG 2018BFG. 2018. Brazilian Flora 2020: Innovation and collaboration to meet Target 1 of the Global Strategy for Plant Conservation (GSPC). Rodriguésia 1513-1527. ) (Tabela 1). As folhas e caules de Senna spp. foram coletados em diferentes locais da região Noroeste do Ceará. A identificação botânica das espécies foi realizada no Herbário Francisco José de Abreu Matos da Universidade Estadual Vale do Acaraú (HUVA), pelo professor Dr. Elnatan Bezerra de Souza. Para o preparo dos extratos, 200g das folhas e caule secos de cada espécie de um mesmo indivíduo foram triturados e imersos durante 10 dias em 500 mL de etanol e, na sequência o extrato foi filtrado e concentrado em um evaporador rotativo a (60°C) durante 2 h. Após este processo, foi mantido em banho-maria (40°C) até a eliminação total do solvente, obtendo-se o extrato etanólico das folhas (EEF) e extrato etanólico do caule (EEC) (Matos 2009Matos, F.J.A. 2009. Introdução à Fitoquímica Experimental. 3 ed. Fortaleza: UFC. 150p.).

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      Material vegetal e preparação dos extratos - Foram selecionadas para este estudo cinco espécies de Senna, sendo uma exótica naturalizada e quatro nativas, das quais uma é endêmica do Brasil, ocorrendo no Cerrado e na Caatinga (BFG 2018BFG. 2018. Brazilian Flora 2020: Innovation and collaboration to meet Target 1 of the Global Strategy for Plant Conservation (GSPC). Rodriguésia 1513-1527. ) (Tabela 1). As folhas e caules de Senna spp. foram coletados em diferentes locais da região Noroeste do Ceará. A identificação botânica das espécies foi realizada no Herbário Francisco José de Abreu Matos da Universidade Estadual Vale do Acaraú (HUVA), pelo professor Dr. Elnatan Bezerra de Souza. Para o preparo dos extratos, 200g das folhas e caule secos de cada espécie de um mesmo indivíduo foram triturados e imersos durante 10 dias em 500 mL de etanol e, na sequência o extrato foi filtrado e concentrado em um evaporador rotativo a (60°C) durante 2 h. Após este processo, foi mantido em banho-maria (40°C) até a eliminação total do solvente, obtendo-se o extrato etanólico das folhas (EEF) e extrato etanólico do caule (EEC) (Matos 2009Matos, F.J.A. 2009. Introdução à Fitoquímica Experimental. 3 ed. Fortaleza: UFC. 150p.).

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      Materiais e métodos

      Ensaio antifúngico in vitro - No ensaio para verificação da concentração inibitória mínima (CIM) dos EE das espécies de Senna, foram utilizadas cepas de Trichophyton rubrum obtidas a partir da micoteca da Universidade Federal de Pernambuco e do Centro Especializado de Micologia Médica (CEMM) da Universidade Federal do Ceará. Para este ensaio foi utilizado o método de microdiluição em caldo, de acordo com a metodologia descrita por (Neves et al. 2019Neves, A.M., Silva, H.S., Souza, E.B., Fontenelle, R.O.S., Silva, A.C.S., Morais, S.M. 2019. Perfil fitoquímico e avaliação da atividade antifúngica da fração hexânica de Mitracarpus baturitensis (Rubiaceae). Essentia 20: 96-101. ) com as normas do protocolo Clinical Laboratory Standards Insitute do documento M38-A (CLSI M38-A2, 2008Clinical and Laboratory Standards Institute. 2008. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi (Approved Standard Document M38. CLSI), vol. M38-A2, Second ed. Clinical and Laboratory Standards Institute, Wayne, PA.). Em placas de 96 poços estéreis, foram adicionados 100 µL de meio RPMI em todos os poços e 10 mg mL-1 dos extratos de Senna spp. foi acrescentado a todos os poços da primeira coluna e, em sequência foram efetuadas as diluições seriadas. Finalmente, 100 µL do inóculo foi adicionado aos poços da placa. Como controle foi utilizado o Cetoconazol (Sigma, Chemical Co., USA). Para as análises de susceptibilidade, os extratos etanólicos foram testados em concentrações variando de 0,002 a 2,5 mg mL-1. As placas foram cobertas com parafilme e incubadas a 37 °C e a leitura visual foi realizada após cinco dias para T. rubrum. Procedimento realizado em duplicata. A CIM é definida como a menor concentração do extrato capaz de inibir 100% do crescimento fúngico visível (Fontenelle et al. 2007Fontenelle, R.O.S., Morais, S.M., Brito, E.H.S., Kerntopf, M.R., Brilhante, R.S.N., Cordeiro, R.A., Tomé, A.R., Queiroz, M.G.R., Nascimento, N.R.F. & Sidrim, J.J.C. 2007. Chemical composition, toxicological aspects and antifungal activity of essential oil from Lippia sidoides Cham. Journal of Antimicrobial Chemotherapy 59: 934-940. ). A concentração fungicida mínima (CFM) foi determinada por subcultura de 100 μL da solução de poços sem turbidez no meio Ágar Dextrose de Batata, a 28 °C. (Fontenelle et al. 2008Fontenelle, R.O.S., Morais, S.M., Brito, E.H.S., Brilhante, R.S.N., Cordeiro, R.A., Nascimento, N.R.F., Kerntopf, M.R., Sidrim, J.J.C. & Rocha, M.F.G. 2008. Antifungal activity of essential oils of Croton species from the Brazilian caatinga biome. Journal of Applied Microbiology 104: 1383-1390.).

      Análise estatística - Todas as determinações foram realizadas em triplicata e todos os resultados foram apresentados como média ± desvio-padrão (DP). Foram realizadas análises de variância (ANOVA) com duas repetições e o Teste Tukey, ao nível de significância de 5%, usando programa Graph Pad Prism® v5.01 (GraphPadSoftware, San Diego, CA, E.U.A.). As diferenças entre as médias foram consideradas significativas quando o valor obtido para "p" foi menor que 0,05 (p < 0,05).

      Para análises da correlação entre os dados, foi utilizado o coeficiente de correlação de Pearson no software Microsoft Excel 2019, a qual mede o grau da correlação linear entre duas variáveis quantitativas. A intensidade dessa correlação é dada pelo “r”, que é um índice adimensional com valores situados entre -1,0 e 1,0. Quando o valor de r estiver entre 0,00-0,19 a correlação é muito fraca; entre 0,20-0,39 é fraca; 0,40-0,59 é uma correlação moderada; entre 0,60-0,79 é forte e finalmente entre 0,80-1,0 diz-se que é uma correlação muito forte (Mukaka 2012Mukaka, M.M. 2012. Statistics corner: A guide to appropriate use of correlation coefficient in medical research. Malawi Med J. 24:69-71.).

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      Resultados e discussãoTabela 3 +

      Resultados e discussãoTabela 3

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      Os fito-constituintes ou fitoquímicos são compostos químicos que desempenham importantes funções nas plantas. A triagem fitoquímica em materiais vegetais é geralmente o ponto de partida para o isolamento e purificação de compostos naturais com bioatividade (Omoregie & Oikeh 2015Omoregie, E.S. & Oikeh, E.I. 2015. Comparative studies on the phytochemical composition, phenolic content and antioxidant activities of methanol leaf extracts of Spondias mombin and Polyathia longifolia. Jordan Journal of Biological Sciences 147: 1-5.). A triagem fitoquímica preliminar revelou a presença de fenóis, taninos, flavonoides e esteroides para todos os extratos estudados (Tabela 2). Entretanto, a presença de saponinas foi constatada apenas no EEF e EEC de S. alata e no EEF de S. trachypus. Já os alcaloides foram encontrados exclusivamente no EEF de S. alata e nenhuma das espécies apresentou triterpenoides.

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      Os fito-constituintes ou fitoquímicos são compostos químicos que desempenham importantes funções nas plantas. A triagem fitoquímica em materiais vegetais é geralmente o ponto de partida para o isolamento e purificação de compostos naturais com bioatividade (Omoregie & Oikeh 2015Omoregie, E.S. & Oikeh, E.I. 2015. Comparative studies on the phytochemical composition, phenolic content and antioxidant activities of methanol leaf extracts of Spondias mombin and Polyathia longifolia. Jordan Journal of Biological Sciences 147: 1-5.). A triagem fitoquímica preliminar revelou a presença de fenóis, taninos, flavonoides e esteroides para todos os extratos estudados (Tabela 2). Entretanto, a presença de saponinas foi constatada apenas no EEF e EEC de S. alata e no EEF de S. trachypus. Já os alcaloides foram encontrados exclusivamente no EEF de S. alata e nenhuma das espécies apresentou triterpenoides.

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      Resultados e discussãoOnyegeme-Okerenta et al. 2017Onyegeme-Okerenta, B.M., Nwosu, T. & Wegwu, M.O. 2017. Proximate and phytochemical composition of leaf extract of Senna alata (L) Roxb. Journal of Pharmacognosy and Phytochemistry 6: 320-326., Ishaku et al. 2016Ishaku, G.A., Arabo, A.A., Bassey, E.E., Uwem, A.A.U.M. & Godwin, E.U. 2016. Physicochemical characterization and antibacterial activity of Senna occidentalis Linn. Journal of Chemistryand Chemical Sciences 6: 9-18. , Silva et al. 2014Silva, G.A., Monteiro, J.A., Ferreira, E.B., Fernandes, M.I.B., Pessoa, C.; Sampaio, C.G. & Silva, M.G.V. 2014. Total phenolic content, antioxidant and anticancer activities of four species of Senna Mill. From northeast Brazil. Int. J. Pharm. Pharm. Sci 6: 199-202., Sudi et al. 2011Sudi, I.Y., Ksgbiya, D.M., Muluh, E.K. & Clement, A. 2011. Nutritional and phytochemical screening of Senna obtusifolia indigenous to Mubi, Nigeria. Advances in Applied Science Research 2: 432-437., Bukar et al. 2009Bukar, A., Mukhtar, M. & HASSAN, A. 2009. Phytochemical screening and antibacterial activity of leaf extracts of Senna siamea (Lam) on Pseudomonas aeruginosa. Bayero Journal of Pure and Applied Sciences 1: 139-142. ). É possível perceber que na análise de prospecção química dos extratos houve uma variação de metabólitos secundários. Este fato pode estar atribuído a vários fatores, entre eles estão as diferentes condições ambientais, tais como clima, radiação solar, nutrição mineral, sazonalidade, ritmo circadiano, temperatura, disponibilidade hídrica, e também os tipos de solvente e a metodologia empregada no processo de extração, que podem interferir consideravelmente no conteúdo de praticamente todas as classes de metabólitos secundários (Gomes et al. 2016Gomes, E.M.C., Pena, R.D.C.M. & da Silva, S.S.S.M. 2016. Composição fitoquímica e ação fungicida de extratos brutos de Cinnamomum zeylanicum sobre Quambalaria eucalypti. Biota Amazônia. 6: 54-58., Bezerra et al. 2013Bezerra, A.S., Nörnberg, J.L., Lima, F.O., Rosa, M.B.D. & Carvalho, L.M.D. 2013. Parâmetros climáticos e variação de compostos fenólicos em cevada. Ciência Rural 9: 1546-1552., Gobbo-Neto & Lopes 2007Gobbo-Neto, L. & Lopes, N.P. 2007. Plantas medicinais: Fatores de influência no conteúdo de metabólitos secundários. Química Nova 30: 374-381.).

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      Os teores de fenóis totais apresentaram diferenças significativas entre os extratos etanólicos das diferentes partes e espécies vegetais estudadas (Tabela 3). O conteúdo de fenóis totais para os EEF variou de 32,60 ± 0,53 a 184,8 ± 5,09 EAG/g, enquanto que para o EEC foram de 30,03± 1,00 a 191,3 ± 0,47 EAG/g. Os maiores níveis de fenóis totais foram detectados na espécie S. trachypus. Os dados da literatura sobre o conteúdo de compostos fenólicos obtidos a partir do extrato aquoso, etanólico e acetona da raiz de S. alata, apresentaram uma concentração de fenóis de 46,3, 78,21 e 21,42 mg EAG/g, respectivamente, e de flavonoides de 26,17, 39,29 e 9,65 mg de equivalente de quercetina por grama de extrato (EQ/g), respectivamente (Ita & Ndukwe 2017Ita, B.N., & Ndukwe, G.I. Antioxidant activity of Senna alata root extracts. 2017. J Nat Prod Resour 3: 94-96. ). Já o extrato etanólico preparado a partir das folhas de S. obtusifolia por Ali et al. (2019Ali, I., Yisa, J. & Jacob, J.O. 2019. Corrosion inhibitory potential of ethanol extract of Senna obtusifolia on Mild Steel in 5M HCl. Journal of Chemical Society of Nigeria 44: 187-198. ), apresentou um teor de fenóis e de flavonoides de 14,39 mg/g e 2,85 mg/g, respectivamente, demonstrando possuir teor de compostos fenólicos inferior ao das mostras de S. obtusifolia encontradas no presente estudo. Além disso, o conteúdo de polifenóis encontrado no extrato etanólico e nas frações obtidas a partir das folhas de S. occidentalis por Yakubu et al. (2018Yakubu, O.E., Otitoju, O., Imarenezor, E.P.K., Tatah, S.V. & Habibu, B. 2018. Fractionation and determination of antioxidant activities, of the Leaves of Senna Occidentalis ethanol extract. Pharmacology, 6: 26-30.) variou de 139 mg/mL a 206 mg/mL e de flavonoides de 104 a 142 mg/mL. Já para os extratos preparados a partir das folhas e casca do caule de S. siamea revelaram um teor de fenóis totais de 10,21 ± 0,25 g/g e 24,77 ± 0,15 g/g, respectivamente. Por outro lado, o teor de flavonoides foi de 0,08 ± 0,01 g/g para as folhagens, e de 0,04 ± 0,01 g/g para a casca do caule (Kwada & Tella 2009Kwada, A.D. & Tella, I.O. 2009. Determination of infochemicals and the phytochemical screening of the foliage and stem-bark of Senna siamea (lam.) in Yola, Adamawa State. Journal of Medicinal Plants Research 3: 630-640.). Para os extratos etanólicos das folhas e raízes de S. trachypus o teor de fenóis totais encontrado foi de 322,09 ± 2,83 EAG/g e de 1277,34 ± 79,54 EAG/g, respectivamente (Silva et al. 2014Silva, G.A., Monteiro, J.A., Ferreira, E.B., Fernandes, M.I.B., Pessoa, C.; Sampaio, C.G. & Silva, M.G.V. 2014. Total phenolic content, antioxidant and anticancer activities of four species of Senna Mill. From northeast Brazil. Int. J. Pharm. Pharm. Sci 6: 199-202.).Senna.

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      Os teores de fenóis totais apresentaram diferenças significativas entre os extratos etanólicos das diferentes partes e espécies vegetais estudadas (Tabela 3). O conteúdo de fenóis totais para os EEF variou de 32,60 ± 0,53 a 184,8 ± 5,09 EAG/g, enquanto que para o EEC foram de 30,03± 1,00 a 191,3 ± 0,47 EAG/g. Os maiores níveis de fenóis totais foram detectados na espécie S. trachypus. Os dados da literatura sobre o conteúdo de compostos fenólicos obtidos a partir do extrato aquoso, etanólico e acetona da raiz de S. alata, apresentaram uma concentração de fenóis de 46,3, 78,21 e 21,42 mg EAG/g, respectivamente, e de flavonoides de 26,17, 39,29 e 9,65 mg de equivalente de quercetina por grama de extrato (EQ/g), respectivamente (Ita & Ndukwe 2017Ita, B.N., & Ndukwe, G.I. Antioxidant activity of Senna alata root extracts. 2017. J Nat Prod Resour 3: 94-96. ). Já o extrato etanólico preparado a partir das folhas de S. obtusifolia por Ali et al. (2019Ali, I., Yisa, J. & Jacob, J.O. 2019. Corrosion inhibitory potential of ethanol extract of Senna obtusifolia on Mild Steel in 5M HCl. Journal of Chemical Society of Nigeria 44: 187-198. ), apresentou um teor de fenóis e de flavonoides de 14,39 mg/g e 2,85 mg/g, respectivamente, demonstrando possuir teor de compostos fenólicos inferior ao das mostras de S. obtusifolia encontradas no presente estudo. Além disso, o conteúdo de polifenóis encontrado no extrato etanólico e nas frações obtidas a partir das folhas de S. occidentalis por Yakubu et al. (2018Yakubu, O.E., Otitoju, O., Imarenezor, E.P.K., Tatah, S.V. & Habibu, B. 2018. Fractionation and determination of antioxidant activities, of the Leaves of Senna Occidentalis ethanol extract. Pharmacology, 6: 26-30.) variou de 139 mg/mL a 206 mg/mL e de flavonoides de 104 a 142 mg/mL. Já para os extratos preparados a partir das folhas e casca do caule de S. siamea revelaram um teor de fenóis totais de 10,21 ± 0,25 g/g e 24,77 ± 0,15 g/g, respectivamente. Por outro lado, o teor de flavonoides foi de 0,08 ± 0,01 g/g para as folhagens, e de 0,04 ± 0,01 g/g para a casca do caule (Kwada & Tella 2009Kwada, A.D. & Tella, I.O. 2009. Determination of infochemicals and the phytochemical screening of the foliage and stem-bark of Senna siamea (lam.) in Yola, Adamawa State. Journal of Medicinal Plants Research 3: 630-640.). Para os extratos etanólicos das folhas e raízes de S. trachypus o teor de fenóis totais encontrado foi de 322,09 ± 2,83 EAG/g e de 1277,34 ± 79,54 EAG/g, respectivamente (Silva et al. 2014Silva, G.A., Monteiro, J.A., Ferreira, E.B., Fernandes, M.I.B., Pessoa, C.; Sampaio, C.G. & Silva, M.G.V. 2014. Total phenolic content, antioxidant and anticancer activities of four species of Senna Mill. From northeast Brazil. Int. J. Pharm. Pharm. Sci 6: 199-202.).Senna.

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      Resultados e discussãoVillano et al. 2007Villano, D., Fernandez-Pachón, M.S., Moya, M.L., Troncoso, A.M. & García-Parrilla, M.C. 2007. Radical scavenging ability of polyphenolic compounds towards DPPH free radical. Talanta, 71: 230-235. ). Já para o EEC os valores de CE50 variaram de 0,83 ± 0,01 a 11,19 ± 0,15 µg/mL (Tabela 3). Foi observado que o EEC de S. siamea apresentou capacidade antirradicalar próximo à quercetina. Semelhantes aos nossos resultados, estudos anteriores revelaram que as espécies de S. alata, S. obtusifolia, S. occidentalis, S. siamea e S. trachypus, apresentaram potencial antioxidante e que esta atividade está atribuída à presença de compostos fenólicos (Coelho et al. 2017Coelho, E.M.P., Barbosa, M.C., Mito, M.S., Mantovanelli, G.C., Oliveira, R.S., & Ishii-Iwamoto, E.L. 2017. The activity of the antioxidant defense system of the weed species Senna obtusifolia L. and its resistance to allelochemical stress. Journal of Chemical Ecology 7: 725-738., Ita & Ndukwe 2017Ita, B.N., & Ndukwe, G.I. Antioxidant activity of Senna alata root extracts. 2017. J Nat Prod Resour 3: 94-96. , Barnaby et al. 2016Barnaby, A.G., Reid, R. & Warren, D. 2016. Antioxidant activity, total phenolics and fatty acid profile of Delonix regia, Cassia fistula, Spathodea campanulata, Senna siamea and Tibouchina granulosa. J Anal Pharm Res 3: 00056., Odeja et al. 2015Odeja, O., Obi, G., Ogwuche, C.E., Elemike, E.E. & Oderinlo, Y. 2015. Phytochemical Screening, Antioxidant and Antimicrobial activities of Senna occidentalis (L.) leaves Extract. Clinical Phytoscience 1: 1-6., Silva et al. 2014Silva, G.A., Monteiro, J.A., Ferreira, E.B., Fernandes, M.I.B., Pessoa, C.; Sampaio, C.G. & Silva, M.G.V. 2014. Total phenolic content, antioxidant and anticancer activities of four species of Senna Mill. From northeast Brazil. Int. J. Pharm. Pharm. Sci 6: 199-202.).

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      Os resultados obtidos na análise de inibição da enzima acetilcolinesterase foram comparados ao do alcaloide fisostigmina que foi o primeiro inibidor descoberto. Os experimentos de inibição da enzima acetilcolinesterase in vitro para as espécies de Senna produziram apenas resultados com potência moderada (Tabela 3). Relatos confirmam a atividade antiacetilcolinesterásica de vários taninos isolados do fruto Terminalia chebula Retz., (Combretaceae) que exibiram um efeito de inibição contra a enzima acetilcolinesterase in vitro (Kim et al. 2018Kim, M.S., Lee, D.Y., Sung, S.H. & Jeon, W.K. 2018. Anti-cholinesterase activities of hydrolysable tannins and polyhydroxytriterpenoid derivatives from Terminalia chebula Retz. fruit. Fruit Rec Nat Prod 12: 284-289.). Outros compostos, como saponinas, alcaloides e compostos fenólicos, também são relatados na literatura como inibidores da enzima acetilcolinesterase (Paiva et al. 2021Paiva, J.R., Queiroz, S.A.S., Pereira, R.D.C.A., Ribeiro, P.R.V., Alves, F.E.G., Silva, L.M.A., Zocolo, G.J., Brito, E.S., Alves, D.R., Morais, S.M., Tavares, J., Pinto, F.C.L., Andrade, G.M., Pessoa, O.D.L., & Canuto, K.M. 2021. Chemical composition and anticholinesterase activity of cultivated bulbs from Hippeastrum elegans, a potential tropical source of bioactive alkaloids. Phytochemistry Letters 43: 27-34., Kozachok et al. 2020Kozachok, S., Pecio, Ł., Orhan, I.E., Deniz, F.S.S., Marchyshyn, S., & Oleszek, W. 2020. Reinvestigation of Herniaria glabra L. saponins and their biological activity. Phytochemistry 169: 112162., Adedayo et al. 2015Adedayo, B.C., Oboh, G., Oyeleye, S.I., Ejakpovi, I.I., Boligon, A.A., & Athayde, M.L. 2015. Blanching alters the phenolic constituents and in vitro antioxidant and anticholinesterases properties of fireweed (Crassocephalum crepidioides). Journal of Taibah University Medical Sciences 10: 419-426.). Estas classes de compostos foram detectadas na triagem fitoquímica, embora provavelmente as concentrações nos extratos eram muito baixas para dar resultados satisfatórios no ensaio. Os extratos foliares e do caule de S. trachypus apresentaram os valores mais satisfatórios de inibição da enzima acetilcolinesterase, indicando que o isolamento de metabólitos pode levar a potenciais agentes antiacetilcolinesterásicos. Na literatura, não foram encontrados estudos do potencial anticolinesterásico paras as espécies de Senna referenciadas, sendo este o primeiro relato de estudo de atividade de inibição para esta enzima.

      +

      Os resultados da atividade antioxidante dos extratos de Senna spp. mostraram que os valores de CE50 para o EEF variaram de 0,63 ± 0,01 a 8,20 ± 0,07 µg/mL, sendo o EEF de S. trachypus o que apresentou menor CE50 com atividade antirradicalar superior ao da quercetina e, portanto, maior potencial antioxidante (Villano et al. 2007Villano, D., Fernandez-Pachón, M.S., Moya, M.L., Troncoso, A.M. & García-Parrilla, M.C. 2007. Radical scavenging ability of polyphenolic compounds towards DPPH free radical. Talanta, 71: 230-235. ). Já para o EEC os valores de CE50 variaram de 0,83 ± 0,01 a 11,19 ± 0,15 µg/mL (Tabela 3). Foi observado que o EEC de S. siamea apresentou capacidade antirradicalar próximo à quercetina. Semelhantes aos nossos resultados, estudos anteriores revelaram que as espécies de S. alata, S. obtusifolia, S. occidentalis, S. siamea e S. trachypus, apresentaram potencial antioxidante e que esta atividade está atribuída à presença de compostos fenólicos (Coelho et al. 2017Coelho, E.M.P., Barbosa, M.C., Mito, M.S., Mantovanelli, G.C., Oliveira, R.S., & Ishii-Iwamoto, E.L. 2017. The activity of the antioxidant defense system of the weed species Senna obtusifolia L. and its resistance to allelochemical stress. Journal of Chemical Ecology 7: 725-738., Ita & Ndukwe 2017Ita, B.N., & Ndukwe, G.I. Antioxidant activity of Senna alata root extracts. 2017. J Nat Prod Resour 3: 94-96. , Barnaby et al. 2016Barnaby, A.G., Reid, R. & Warren, D. 2016. Antioxidant activity, total phenolics and fatty acid profile of Delonix regia, Cassia fistula, Spathodea campanulata, Senna siamea and Tibouchina granulosa. J Anal Pharm Res 3: 00056., Odeja et al. 2015Odeja, O., Obi, G., Ogwuche, C.E., Elemike, E.E. & Oderinlo, Y. 2015. Phytochemical Screening, Antioxidant and Antimicrobial activities of Senna occidentalis (L.) leaves Extract. Clinical Phytoscience 1: 1-6., Silva et al. 2014Silva, G.A., Monteiro, J.A., Ferreira, E.B., Fernandes, M.I.B., Pessoa, C.; Sampaio, C.G. & Silva, M.G.V. 2014. Total phenolic content, antioxidant and anticancer activities of four species of Senna Mill. From northeast Brazil. Int. J. Pharm. Pharm. Sci 6: 199-202.).

      +

      Os resultados obtidos na análise de inibição da enzima acetilcolinesterase foram comparados ao do alcaloide fisostigmina que foi o primeiro inibidor descoberto. Os experimentos de inibição da enzima acetilcolinesterase in vitro para as espécies de Senna produziram apenas resultados com potência moderada (Tabela 3). Relatos confirmam a atividade antiacetilcolinesterásica de vários taninos isolados do fruto Terminalia chebula Retz., (Combretaceae) que exibiram um efeito de inibição contra a enzima acetilcolinesterase in vitro (Kim et al. 2018Kim, M.S., Lee, D.Y., Sung, S.H. & Jeon, W.K. 2018. Anti-cholinesterase activities of hydrolysable tannins and polyhydroxytriterpenoid derivatives from Terminalia chebula Retz. fruit. Fruit Rec Nat Prod 12: 284-289.). Outros compostos, como saponinas, alcaloides e compostos fenólicos, também são relatados na literatura como inibidores da enzima acetilcolinesterase (Paiva et al. 2021Paiva, J.R., Queiroz, S.A.S., Pereira, R.D.C.A., Ribeiro, P.R.V., Alves, F.E.G., Silva, L.M.A., Zocolo, G.J., Brito, E.S., Alves, D.R., Morais, S.M., Tavares, J., Pinto, F.C.L., Andrade, G.M., Pessoa, O.D.L., & Canuto, K.M. 2021. Chemical composition and anticholinesterase activity of cultivated bulbs from Hippeastrum elegans, a potential tropical source of bioactive alkaloids. Phytochemistry Letters 43: 27-34., Kozachok et al. 2020Kozachok, S., Pecio, Ł., Orhan, I.E., Deniz, F.S.S., Marchyshyn, S., & Oleszek, W. 2020. Reinvestigation of Herniaria glabra L. saponins and their biological activity. Phytochemistry 169: 112162., Adedayo et al. 2015Adedayo, B.C., Oboh, G., Oyeleye, S.I., Ejakpovi, I.I., Boligon, A.A., & Athayde, M.L. 2015. Blanching alters the phenolic constituents and in vitro antioxidant and anticholinesterases properties of fireweed (Crassocephalum crepidioides). Journal of Taibah University Medical Sciences 10: 419-426.). Estas classes de compostos foram detectadas na triagem fitoquímica, embora provavelmente as concentrações nos extratos eram muito baixas para dar resultados satisfatórios no ensaio. Os extratos foliares e do caule de S. trachypus apresentaram os valores mais satisfatórios de inibição da enzima acetilcolinesterase, indicando que o isolamento de metabólitos pode levar a potenciais agentes antiacetilcolinesterásicos. Na literatura, não foram encontrados estudos do potencial anticolinesterásico paras as espécies de Senna referenciadas, sendo este o primeiro relato de estudo de atividade de inibição para esta enzima.

      Para os extratos de Senna spp., foi observada forte correlação negativa entre os valores de fenóis totais e CE50 (r = - 0,71), mostrando que quanto maior os teores de fenóis totais, menor a CE50 e, consequentemente, maior o potencial antioxidante, uma vez que a CE50 está inversamente relacionada à capacidade antioxidante de um composto (Villano et al. 2007Villano, D., Fernandez-Pachón, M.S., Moya, M.L., Troncoso, A.M. & García-Parrilla, M.C. 2007. Radical scavenging ability of polyphenolic compounds towards DPPH free radical. Talanta, 71: 230-235. ). Dentre os extratos analisados podemos observar na figura 1 o EEF de S. trachypus.

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      @@ -129,10 +132,10 @@

      Resultados e discussãoFigura 2). Isso demonstra que os compostos fenólicos podem ser determinantes nessa atividade, de modo que alguns estudos evidenciaram que flavonoides e outros compostos fenólicos possuem atividade anticolinesterásica (Amessis-Ouchemoukh et al. 2014Amessis-Ouchemoukh, N., Madani, K., Falé, P.L., Serralheiro, M.L., Araújo, M.E.M. 2014. Antioxidant capacity and phenolic contents of some Mediterranean medicinal plants and their potential role in the inhibition of cyclooxygenase-1 and acetylcholinesterase activities. Industrial Crops and Products, 53: 6-15.).

      +

      Na correlação da atividade de inibição da enzima acetilcolinesterase, representada pelo CI50 com teor de fenóis totais, observou-se uma correlação muito forte (r = -0,84) entre estas duas variáveis, evidenciando que ambas são inversamente proporcionais entre si, ou seja, à medida que o teor de fenóis totais aumenta o valor de CI50 diminui, como pode ser observado para o EEF de S. occidentalis (Figura 2). Isso demonstra que os compostos fenólicos podem ser determinantes nessa atividade, de modo que alguns estudos evidenciaram que flavonoides e outros compostos fenólicos possuem atividade anticolinesterásica (Amessis-Ouchemoukh et al. 2014Amessis-Ouchemoukh, N., Madani, K., Falé, P.L., Serralheiro, M.L., Araújo, M.E.M. 2014. Antioxidant capacity and phenolic contents of some Mediterranean medicinal plants and their potential role in the inhibition of cyclooxygenase-1 and acetylcholinesterase activities. Industrial Crops and Products, 53: 6-15.).

      -
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      @@ -140,10 +143,10 @@

      Resultados e discussãofigura 3, é possível perceber que o EEF e EEC de S. alata e EEF de S. obtusifolia se destacam no gráfico, o que sugere uma grande capacidade dos antioxidantes, como os compostos fenólicos, presentes nos extratos analisados, de atuarem não só através da inibição da acetilcolinesterase (AChEI) mas também por mecanismos de redução de radicais livres.

      +

      Houve uma correlação moderada (r = 0,43) entre a CI50 e a CE50. Analisando a figura 3, é possível perceber que o EEF e EEC de S. alata e EEF de S. obtusifolia se destacam no gráfico, o que sugere uma grande capacidade dos antioxidantes, como os compostos fenólicos, presentes nos extratos analisados, de atuarem não só através da inibição da acetilcolinesterase (AChEI) mas também por mecanismos de redução de radicais livres.

      -
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      @@ -151,10 +154,10 @@

      Resultados e discussãoTabela 4). A presença de compostos fitoquímicos tem sido associada às atividades antimicrobianas da maioria dos materiais vegetais. Algumas classes de metabólitos foram identificadas nesse estudo e podem ser associadas à atividade antimicrobiana (Santos et al. 2018Santos, T.C.D., Gomes, T.M., Pinto, B.A.S., Camara, A.L. & Paes, A.M.D.A. 2018. Naturally occurring acetylcholinesterase inhibitors and their potential use for Alzheimer's disease therapy. Frontiers in Pharmacology 9: 1192., Odeja et al. 2015Odeja, O., Obi, G., Ogwuche, C.E., Elemike, E.E. & Oderinlo, Y. 2015. Phytochemical Screening, Antioxidant and Antimicrobial activities of Senna occidentalis (L.) leaves Extract. Clinical Phytoscience 1: 1-6.).

      +

      Os extratos etanólicos das folhas e caule de S. alata, S. obtusifolia, S. occidentalis e S. siamea, apresentaram efeito inibitório contra algumas cepas de T. rubrum. A maioria dos extratos foram eficazes em diferentes concentrações, com CIM que variaram de 0,07 mg/mL à 2,5 mg/mL e CFM de 0,15 a 5,0 mg/mL contra a grande maioria das cepas fúngicas testadas. Dentre os extratos testados, os de S. trachypus foram eficazes contra todas as cepas de T. rubrum com CIM que variaram de 0,31 a 0,62 mg/mL e o CFM de 0,62 a 1,25 mg/mL, para ambos os extratos (Tabela 4). A presença de compostos fitoquímicos tem sido associada às atividades antimicrobianas da maioria dos materiais vegetais. Algumas classes de metabólitos foram identificadas nesse estudo e podem ser associadas à atividade antimicrobiana (Santos et al. 2018Santos, T.C.D., Gomes, T.M., Pinto, B.A.S., Camara, A.L. & Paes, A.M.D.A. 2018. Naturally occurring acetylcholinesterase inhibitors and their potential use for Alzheimer's disease therapy. Frontiers in Pharmacology 9: 1192., Odeja et al. 2015Odeja, O., Obi, G., Ogwuche, C.E., Elemike, E.E. & Oderinlo, Y. 2015. Phytochemical Screening, Antioxidant and Antimicrobial activities of Senna occidentalis (L.) leaves Extract. Clinical Phytoscience 1: 1-6.).

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      Figura 1.
      Correlação entre o teor de fenóis totais e CE50 de espécies de Senna Mill. (Fabaceae). Símbolos cheios: folhas. Símbolos vazados: caule.
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      Figura 2.
      Correlação entre o teor de fenóis totais e CI50 de espécies de Senna Mill. (Fabaceae). Símbolos cheios: folhas. Símbolos vazados: caule.
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      Tabela 1.
      Identificação das espécies de Senna Mill. (Fabaceae) coletadas em diferentes locais da região noroeste do Estado do Ceará. *Exótica, **Endêmica do Brasil. Fonte: Herbário Francisco José de Abreu Matos (HUVA).
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      Tablela 2
      Triagem fitoquímica do EEF e do EEC de espécies de Senna Mill. (Fabaceae). Presente: + Ausente: - EEF: Extrato etanólico da folha. EEC: Extrato etanólico do caule.
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      Table 3.
      Teor de fenóis totais, atividade antioxidante e inibição da enzima acetilcolinesterase de espécies de Senna Mill. (Fabaceae).
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      -Figure 1. Correlation between total phenol content and EC50 of Senna Mill species. (Fabaceae). Symbols filled: leaves. Hollow symbols: stem. +Figure 1. Correlation between total phenol content and EC50 of Senna Mill species. (Fabaceae). Symbols filled: leaves. Hollow symbols: stem.

      -Figure 2. Correlation between total phenol content and IC50 of Senna Mill species. (Fabaceae). Symbols filled: leaves. Hollow symbols: stem. +Figure 2. Correlation between total phenol content and IC50 of Senna Mill species. (Fabaceae). Symbols filled: leaves. Hollow symbols: stem.

      -Figure 3. Correlation between IC50 and EC50 of Senna Mill species. (Fabaceae). Symbols filled: leaves. Hollow symbols: stem. +Figure 3. Correlation between IC50 and EC50 of Senna Mill species. (Fabaceae). Symbols filled: leaves. Hollow symbols: stem.

      -Sobre os autores +Sobre os autores
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        Figuras | Fórmulas