Antifungal Activity, Phytochemical Characterization and Thermal Profile of Anadenanthera colubrina (Vell.) Brenan

Eveline Angélica Rocha, Ana Cláudia Dantas de Medeiros, Ricardo Dias de Castro, Pedro Luiz Rosalen, Karina Lidianne Alcântara Saraiva, Gustavo Pina Godoy, Larissa Rodrigues Apolinário da Silva, Cibelle Sousa Silva Aleixo, Priscilla Guimarães Silva, Edja Maria Melo de Brito Costa

Abstract


Objective: To investigate the antifungal potential of A. colubrina, and its phytochemical characteristics, thermal profile and toxicity. Material and Methods: To assess potential antifungal activity, the technique of microdilution was used with the determination of the Minimum Inhibitory Concentration and Minimum Fungicidal Concentration, using standard species of Candida and recent clinical isolates of Candida albicans. Analyses of action of the extract were performed on the wall and cell morphology of C. albicans, of the interactive effect between the plant extract and nystatin on C. albicans through the checkerboard method, and of growth kinetics. The phytochemical screening was determined by spectrophotometry. The thermal profile was traced with the determination of thermogravimetric curves (TG) and differential scanning calorimetry (DSC). The toxicity was evaluated by the method of hemolysis. Results: The extract of A. colubrina showed a fungistatic potential against all bacteria tested and it acted by modifying the cellular morphology of C. albicans. There was a synergism between nystatin and the plant extract (FIC=0.375), and 53.18% of total polyphenols were determined. The TG curve showed the occurrence of three steps of thermal decomposition. None of the tested concentrations became the effective cytotoxic concentration. Conclusion: Further studies should be conducted to understand the efficacy and the mechanisms of action involved in the antifungal activity of the plant extract of A. colubrina in order to produce a new drug for the treatment of oral candidiasis.

Keywords


Plants, Medicinal; Plant Extracts; Candida; Antifungal Agents.

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References


Li YY, Chen WY, Li X, Li HB, Li HQ, Li W, He L, Yang X, Wang X, Huang Y, Yao Y. Asymptomatic oral yeast carriage and antifungal susceptibility profile of HIV-infected patients in Kunming, Yunnan Province of China. BMC Infect Dis 2013; 13: 2-9. doi: 10.1186/1471-2334-13-46.

Williams D, Lewis M. Pathogenesis and treatment of oral candidosis. J Oral Microbiol 2011; 3(1):1-11. doi: 10.3402/jom.v3i0.5771.

Samaranayake LP, Leung K, Jin L. Oral mucosal fungal infection. Periodontol 2000 2009; 49(1):39-59. doi: 10.1111/j.1600-0757.2008.00291.x.

Lewis RE. Current concepts in antifungal pharmacology. Mayo Clin Proc 2011; 86(8):805-17. doi: 10.4065/mcp.2011.0247.

Patil S, Rao RS, Majumdar B, Anil S. Clinical appearance of oral candida infection and therapeutic strategies. Front Microbiol 2015: 6(1):1-10. doi: 10.3389/fmicb.2015.01391.

Shapiro RS, Robbins N, Cowen LE. Regulatory circuitry governing fungal development, drug resistance, and disease. Microbiol Mol Biol Rev 2011; 75(2):213-67. doi: 10.1128/MMBR.00045-10.

Lyu X, Zhao C, Yan Z, Hua H. Efficacy of nystatin for the treatment of oral candidiasis: a systematic review and meta-analysis. Drug Des Devel Ther 2016;10(1):1161-71. doi: 10.2147/DDDT.S100795.

Abad MJ, Ansuategui M, Bermejo P. Active antifungal substances from natural sources. J Organic Chem 2007; 2(1):116-45.

Albuquerque UP, Medeiros PM, Monteiro JM, Lins Neto EMFL, Gomes de Melo J, Santos JP. Medicinal plants of the caatinga (semi-arid) vegetation of NE Brazil: A quantitative approach. J Ethnopharmacol 2007; 114(3):325-54. doi: 10.1016/j.jep.2007.08.017.

Medeiros PM, Ladio AH, Albuquerque UP. Patterns of medicinal plant use by inhabitants of Brazilian urban and rural areas: A macroscale investigation based on available literature. J Ethnopharmacol 2013; 150(2): 729–46. doi: 10.1016/j.jep.2013.09.026.

Pedone-Bonfim MV, Lins MA, Coelho IR, Santana AS, Silva FS, Maia LC. Mycorrhizal technology and phosphorus in the production of primary and secondary metabolites in cebil (Anadenantheracolubrina (Vell.) Brenan) seedlings. J Sci Food Agric 2013; 93(6):1479-84. doi: 10.1002/jsfa.5919.

Damascena NP, Souza MT, Almeida AF, Cunha RS, Damascena NP, Curvello RL, et al. Antioxidant and orofacial anti-nociceptive activities of the stem bark aqueous extract of Anadenanthera colubrina (Velloso) Brenan (Fabaceae). Nat Prod Res 2014; 28(10):753-6.

Pessoa WS, Estevão LR, Simões RS, Barros ME, Mendonça FS, Baratella-Evência L, et al. Effects of angico extract (Anadenanthera colubrina var. cebil) in cutaneous wound healing in rats. Acta Cirur Bras 2012; 27(10):655-70. doi: 10.1590/S0102-86502012001000001.

Trentin DS, Silva DB, Amaral MW, Zimmer KR, Silva MV, Lipes NP, et al. Tannins possessing bacteriostatic effect impair pseudomonas aeruginosa adhesion and biofilm formation. PloS One 2013; 8(6):1-13. doi: 10.1371/journal.pone.0066257.

Silva CR, Oliveira LD, Leão MV, Jorge AO. Candida spp. adherence to oral epithelial cells and levels of IgA in children with orthodontic appliances. Braz Oral Res 2014; 28(1):28-32. doi: 10.1590/S1806-83242013005000031.

Lima RF, Alves EP, Rosalen PL, Ruiz ALCG, Duarte MCT, Góes VFF, et al. Antimicrobial and anti-proliferative potential of Anadenanthera Colubrina (Vell.) Brenan. Evidence-Based Complementary and Alternative Medicine, 2014, Article ID 802696. doi: 10.1155/2014/802696.

Clinical and Laboratory Standards Institute. M27-S3. Reference method for broth dilution antifungal susceptibility testing of yeasts: 3rd. informational supplement. CLSI, Wayne, PA, 2008.

Odds FC. Synergy, antagonism and what the chequerboard puts between them. J Antimicrob Chemother 2003; 52(1):1. doi: 10.1093/jac/dkg301.

Chandra S, De Mejia Gonzalez E. Polyphenolic compounds, antioxidant capacity, and quinone reductase activity of an aqueous extract of Ardisia compressa in comparison to mate (Ilex paraguariensis) and green (Camellia sinensis) teas. J Agric Food Chem 2004; 52(11):3583-9. doi: 10.1021/jf0352632.

Meda A, Lamien CE, Romito M, Millogo J, Nacoulma OG. Determination of the total phenolic, flavonoid and proline contents in Burkina Fasanhoney, as well as their radical scavenging activity. Food Chem 2005; 91(3):571-7. doi: 10.1016/j.foodchem.2004.10.006.

Makkar HPS, Blümmel M, Borowy NK, Becker K. Gravimetric determination of tannins and their correlations with chemical and protein precipitation methods. J Sci Agric 1993; 61(2):161-5. doi: 10.1002/jsfa.2740610205.

Pereira VSS, Oliveira CSC, Fumagalli F, Emery FS, Silva NB, Andrade-Neto VF. Cytotoxicity, hemolysis and in vivo acute toxicity of 2-hydroxy-3-anilino-1,4-naphthoquinone derivatives. Toxicology Reports 2016; 3(1):756-62. doi: 10.1016/j.toxrep.2016.09.007.

Aligiannis N, Kalpotzakis E, Mitaku S, Chinou IB. Composition and antimicrobial activity of the essential oils of two Origanum species. J Agr Food Chem 2001; 49(9):4168-70. doi: 10.1021/jf001494m.

Ríos JL, Recio MC. Medicinal plants and antimicrobial activity. J Ethnopharmacol 2005; 100(1-2):80-4. doi: 10.1016/j.jep.2005.04.025.

Moyes DL, Naglik JR. Mucosal Immunity and Candida albicans Infection. Clin Dev Immunology 2011; 2011(1):1-9. doi: doi: 10.1155/2011/346307.

Ibe C, Walker LA, Gow NAR, Munro CA. Unlocking the therapeutic potential of the fungal cell wall: Clinical implications and drug resistance. Candida albicans: Cellular and molecular biology. 2.nd. ed. Prasad R (Ed.). Springer International Publishing 2017. pp. 313-46.

Johnson MD, MacDougall C, Ostrosky-Zeichner L, Perfect JR, Rex JH. Combination antifungal therapy. J Antimicrob Chemother 2004; 48(3):693-715. doi: 10.1128/AAC.48.3.693-715.2004.

Castro RD, de Souza TM, Bezerra LM, Ferreira GL, Costa EM, Cavalcanti AL. Antifungal activity and mode of action of thymol and its synergism with nystatin against Candida species involved with infections in the oral cavity: an in vitro study. BMC Complement Altern Med 2015; 24(15):417. doi: doi: 10.1186/s12906-015-0947-2.

Estrella-cuenca M. Combinations of antifungal agents in therapy–what value are they? J Antimicrob Chemother 2004; 54(5):854-69. doi: 10.1093/jac/dkh434.

Rukayadi Y, Lee K, Lee M, Yong D, Hwang JK. Synergistic anticandidal activity of xanthorrhizol in combination with ketoconazole or amphotericin B. FEMS Yeast Res 2009; 9(8):1302-11. doi: 10.1111/j.1567-1364.2009.00548.x.

Andes D, Forrest A, Lepack A, Nett J, Marchillo K, Lincoln L. Impact of antimicrobial dosing regimen on evolution of drug resistance in vivo: fluconazole and Candida albicans. Antimicrob Agents Chemother 2006; 50(7):2374-83. doi: 10.1128/AAC.01053-05.

Gomes de Melo J, Sousa Araújo TA, Almeida TN, Castro V, Lyra de Vasconcelos CD, Desterro RM. Antiproliferative activity, antioxidant capacity and tannin content in plants of semi-arid northeastern Brazil. Molecules 2010; 15(12):8534-42. doi: 10.3390/molecules15128534.

Campos VAC, Perina FJ, Alves E, Sartorell J, Moura A, Oliveira DF. Anadenanthera colubrina (Vell.) Brenan produces steroidal substances that are active against Alternaria alternata (Fr.) Keissler and that may bind to oxysterol-binding proteins. Pest Manag Sci 2014; 70(12):1815-22. doi: 10.1002/ps.3722.

Evensen NA, Braun PC. The effects of tea polyphenols on Candida albicans: inhibition of biofilm formation and proteasome inactivation. Can J Microbiol 2009; 55(9):1033-9. doi: 10.1139/w09-058.

Redondo LM, Chacana PA, Dominguez JE, Fernandez Miyakawa ME. Perspectives in the use of tannins as alternative to antimicrobial growth promoter factors in poultry. FMICB 2014; 27(5):1-7. doi: 10.3389/fmicb.2014.00118.

Ullah N, Khan FA. An introduction to natural products and phytochemicals with special reference to its antimicrobial activity. Life Sci J 2016;13(10):103-119. doi: 10.7537/marslj.131016.14.

Samy RP, Gopalakrishnakone P. Therapeutic potential of plants as anti-microbials for drug discovery. Evid Based Complement Alternat Med 2010; 7(3):283-94. doi: 10.1093/ecam/nen036.

Orhan DD, Ozçelik B, Ozgen S, Ergun F. Antibacterial, antifungal, and antiviral activities of some flavonoids. Microbiol Res 2009; 165(6):496-504. doi: 10.1016/j.micres.2009.09.002.

Lourenço RMDC, Melo PS, Almeida ABA. Flavonoids as antifungal agents. In: Antifungal metabolites from plants. Razzaghi-Abyaneh M, Rai M. (Eds.). Springer-Verlag Berlin Heidelberg, 2013. pp. 283-300.

Okoth DA, Chenia HY, Koorbanally NA. Antibacterial and antioxidant activities of flavonoids from Lannea alata (Engl.) Engl. (Anacardiaceae). Phytochem Lett 2013; 6(3):476-81. doi: 10.1016/j.phytol.2013.06.003.

Costa RS, Negrão CAB, Camelo SRP, Ribeiro-Costa RM, Barbosa WLR, Costa CEF et al. Investigation of thermal behavior of Heliotropium indicum L. lyophilized extract by TG and DSC. J Thermal Anal Calorim 2013; 111(3):1959-64. doi: 10.1007/s10973-011-2088-2.

Fernandes FHA, Santana CP, Santos RL, Correira LP, Conceição MM, Macêdo RO et al. Thermal characterization of dried extract of medicinal plant by DSC and analytical techniques. J Thermal Anal Calorim. 2013; 113(2):443-7. doi: 10.1007/s10973-012-2807-3.

Tramer F, Da Ros T, Passamonti S. Screening of fullerene toxicity by hemolysis assay nanotoxicity. In: Reineke J (Ed.). Nanotoxicity: Methods and protocols method. 2012; pp. 203-17.

Protopopova M, Hanrahan C, Nikonenko B, Samala R, Chen P, Gearhart J, Einck L, Nacy CA. Identification of a new antitubercular drug candidate, SQ 109, from a combinatorial library of 1,2-ethylenediamines. J Antimicrob Chemother 2005; 56(5):968-74. doi: 10.1093/jac/dki319.




DOI: http://dx.doi.org/10.4034/PBOCI.2017.171.12

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