In vitro evaluation of the acquisition of resistance, antifungal activity and synergism of Brazilian red propolis with antifungal drugs on Candida spp.

Journal of Applied Microbiology

Volumn 118, Issue 4, 2015, Pages 839-850

  Pippi, B ^a   Lana, A J D ^a   Moraes, R C ^a   Guez C M ^b   Machado, M ^b   de Oliveira, L F S ^b   Lino von Poser, G ^a   Fuentefria, A M ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b UNIVERSIDADE FEDERAL DO PAMPA   (Brazil)

Author keywords

Antifungal agent; Brazilian red propolis; Candida; Fluconazole; Resistance; Synergism

Indexed keywords

ANTIFUNGAL AGENTS; YEAST;

ANIDULAFUNGIN; ANTIFUNGAL ACTIVITIES; ANTIFUNGAL AGENT; ANTIFUNGALS; BRAZILIAN RED PROPOLIS; CANDIDA SP; FLUCONAZOLE; IN-VITRO EVALUATION; RESISTANCE; SYNERGISM;

CANDIDA;

ANIDULAFUNGIN; BRAZILIAN RED PROPOLIS; FLUCONAZOLE; ITRACONAZOLE; KETOCONAZOLE; MICONAZOLE; PROPOLIS; UNCLASSIFIED DRUG; ANTIFUNGAL AGENT; PLANT EXTRACT;

ANTIMICROBIAL ACTIVITY; CONCENTRATION (COMPOSITION); DISEASE RESISTANCE; DISEASE TREATMENT; DRUG; EMERGENCE; FRACTIONATION; INHIBITOR; ORGANIC COMPOUND; PHENOTYPE; YEAST;

ANTIFUNGAL ACTIVITY; ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; CANDIDA; CANDIDA GLABRATA; CANDIDA PARAPSILOSIS; CANDIDA TROPICALIS; CONTROLLED STUDY; CROSS RESISTANCE; DRUG POTENTIATION; EVALUATION STUDY; FUNGAL CELL WALL; FUNGAL STRAIN; IN VITRO STUDY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PICHIA KUDRIAVZEVII; BRAZIL; CHEMISTRY; CLASSIFICATION; DRUG EFFECTS; GENETICS; METABOLISM; MICROBIAL SENSITIVITY TEST;

BRAZIL;

CANDIDA; CANDIDA GLABRATA; CANDIDA PARAPSILOSIS;

ANTIFUNGAL AGENTS; BRAZIL; CANDIDA; DRUG RESISTANCE, FUNGAL; DRUG SYNERGISM; FLUCONAZOLE; MICROBIAL SENSITIVITY TESTS; PLANT EXTRACTS; PROPOLIS;

EID: 84924914555     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12746     Document Type: Article

References (50)

1. Alves, I.A., Bandeira, L.A., Mario, D.A.N., Denardi, L.B., Neves, L.V., Santurio, J.M. and Alves, S.H. (2012) Effects of antifungal agents alone and in combination against Candida glabrata strains susceptible or resistant to fluconazole. Mycopathologia 174, 215-221.
2. Al-Waili, N., Al-Ghamdi, A., Ansari, M.J., Al-attal, Y. and Salom, K. (2012) Synergistic effects of honey and propolis toward drug multi- resistant Staphylococcus aureus, Escherichia coli and Candida albicans isolates in single and polymicrobial cultures. Int J Med Sci 9, 793-800.
3. Barchiesi, F., Calabrese, D., Sanglard, D., di Francesco, L.F., Caselli, F., Giannini, D., Giacometti, A., Gavaudan, S. et al. (2000) Experimental induction of fluconazole resistance in Candida tropicalis ATCC 750. Antimicrob Agents Chemother 44, 1578-1584.
4. Borst, A., Raimer, M.T., Warnock, D.W., Morrison, C.J. and Arthington-Skaggs, B.A. (2005) Rapid acquisition of stable azole resistance by Candida glabrata isolates obtained before the clinical introduction of fluconazole. Antimicrob Agents Chemother 49, 783-787.
5. Bremenkampa, R.M., Carisa, A.R., Jorgea, A.O.C., Back-Britoa, G.N., Motaa, A.J., Balduccib, I., Brighentia, F.L. and Koga-Itoa, C.Y. (2011) Prevalence and antifungal resistance profile of Candida spp. oral isolates from patients with type 1 and 2 diabetes mellitus. Arch Oral Biol 56, 549-555.
6. Cabral, I.S.R., Oldoni, T.L.C., Prado, A., Bezerra, R.M.N. and Alencar, S.M. (2009) Composição fenólica, atividade antibacteriana e antioxidante da própolis vermelha brasileira. Quim Nova 32, 1523-1527.
7. Chiou, C.C., Mavrogiorgos, N., Tillem, E., Hector, R. and Walsh, T.J. (2001) Synergy, pharmacodynamics, and time-sequenced ultrastructural changes of the interaction between nikkomycin Z and the echinocandin FK463 against Aspergillus fumigatus. Antimicrob Agents Chemother 45, 3310-3321.
8. CLSI M27 - A3 (2008) Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts: Third Informational Supplement. Wayne, PA, USA: Clinical and Laboratory Standards Institute.
9. CLSI M27-S4 (2012) Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts: Fourth Informational Supplement. Wayne, PA, USA: Clinical and Laboratory Standards Institute.
10. Dalben-Dota, K., Faria, M., Bruschi, M., Pelloso, S., Lopes-Consolaro, M. and Svidzinski, T. (2010) Antifungal activity of propolis extract against yeasts isolated from vaginal exudates. J Altern Complement Med 16, 285-290.
11. Escalante, A., Gattuso, M., Perez, P. and Zacchino, S. (2008) Evidence for the mechanism of action of the antifungal phytolaccoside B Isolated from Phytolacca tetramera Hauman. J Nat Prod 71, 1720-1725.
12. Fekete-Forgacs, K., Gyure, L. and Lenkey, B. (2000) Changes of virulence factors accompanying the phenomenon of induced fluconazole resistance in Candida albicans. Mycoses 43, 273-279.
13. Fianco, A.L.B. (2014) Estudo sobre a atividade antifúngica e antioxidante de extratos de própolis obtidos com CO2 supercrítico. Dissertation in Engenharia e Tecnologia de Materiais, Pontífica Universidade Católica, Brazil.
14. Flevari, A., Theodorakopoulou, M., Velegraki, A., Armaganidis, A. and Dimopoulos, G. (2013) Treatment of invasive candidiasis in the elderly: a review. Clin Interv Aging 8, 1199-1208.
15. Ghannoum, M.A., Herbert, J. and Isham, N. (2011) Repeated exposure of Candida spp. to miconazole demonstrates no development of resistance. Mycoses 54, E175-E177.
16. Güez, C.M., Waczuk, E.P., Pereira, K.B., Querol, M.V.M., Da Rocha, J.B.T. and De Oliveira, L.F.S. (2012) In vivo and in vitro genotoxicity studies of aqueous extract of Xanthium spinosum. Braz J Pharm Sci 48, 461-467.
17. Henry, K., Nickels, J. and Edlind, T. (2000) Upregulation of ERG genes in Candida species by azoles and other sterol biosynthesis inhibitors. Antimicrob Agents Chemother 44, 2693-2700.
18. Holderna, E. and Kedzia, B. (1987) Investigations upon the combined action of propolis and antimycotic drugs on Candida albicans. Herba Pol 33, 145-151.
19. Huang, M. and Kao, K.C. (2012) Population dynamics and the evolution of antifungal drug resistance in Candida albicans. FEMS Microbiol Lett 333, 85-93.
20. Isham, N. and Ghannoum, M.A. (2010) Antifungal activity of miconazole against recent Candida strains. Mycoses 53, 434-437.
21. Johnson, M., Macdougall, C., Ostrosky-Zeichner, L., Perfect, J. and Rex, J. (2004) Combination antifungal therapy. Antimicrob Agents Chemother 48, 693-715.
22. López, B.G., Schmidt, E.M., Eberlin, M.N. and Sawaya, A.C.H.F. (2014) Phytochemical markers of different types of red propolis. Food Chem 146, 174-180.
23. Marr, K.A., Lyons, C.N., Rustad, T.R., Bowden, R.A. and White, T.C. (1998) Rapid, transient fluconazole resistance in Candida albicans is associated with increased mRNA levels of CDR. Antimicrob Agents Chemother 42, 2584-2589.
24. Marr, K.A., Lyons, C.N., Ha, K., Rustad, T.R. and White, T.C. (2001) Inducible azole resistance associated with a heterogeneous phenotype in Candida albicans. Antimicrob Agents Chemother 45, 52-59.
25. Mirzoeva, O., Grishanin, R. and Calder, P. (1997) Antimicrobial action of propolis and some of its components: the effects on growth, membrane potential and motility of bacteria. Microbiol Res 152, 239-246.
26. Nucci, M., Queiroz-Telles, F., Tobon, A., Restrepo, A. and Colombo, A. (2010) Epidemiology of opportunistic fungal infections in Latin America. Clin Infect Dis 51, 561-570.
27. Odds, F.C. (2003) Synergy, antagonism, and what the chequerboard puts between them. J Antimicrob Chemother 52, 1.
28. Orsi, R., Sforcin, J., Funari, S., Fernandes, A. and Bankova, V. (2006) Synergistic effect of propolis and antibiotics on the Salmonella typhi. Braz J Microbiol 37, 108-112.
29. Orsi, R., Fernandes, A., Bankova, V. and Sforcin, J. (2012) The effects of Brazilian and Bulgarian propolis in vitro against Salmonella typhi and their synergism with antibiotics acting on the ribosome. Nat Prod Res 26, 430-437.
30. Peman, J., Canton, E. and Espinel-Ingroff, A. (2009) Antifungal drug resistance mechanisms. Expert Rev Anti Infect Ther 7, 453-460.
31. Pfaller, M. (2012) Antifungal drug resistance: mechanisms, epidemiology, and consequences for treatment. Am J Med 125, S3-S13.
32. Piccinelli, A.L., Lotti, C., Campone, L., Cuesta-Rubio, O., Fernandez, M.C. and Rastrelli, L. (2011) Cuban and Brazilian Red Propolis: botanical origin and comparative analysis by high-performance liquid chromatography - photodiode array detection/electrospray ionization tandem mass spectrometry. J Agric Food Chem 59, 6484-6491.
33. Pinto e Silva, A.T., Costa-de-Oliveira, S., Silva-Dias, A., Pina-Vaz, C. and Rodrigues, A.G. (2009) Dynamics of in vitro acquisition of resistance by Candida parapsilosis to different azoles. FEMS Yeast Res 9, 626-633.
34. Raghukumar, R., Vali, L., Watson, D., Fearnley, J. and Seidel, V. (2010) Antimethicillin-resistant Staphylococcus aureus (MRSA) activity of 'pacific propolis' and isolated prenylflavanones. Phytother Res 24, 1181-1187.
35. Redding, S.W., Kirkpatrick, W.R., Saville, S., Coco, B.J., White, W., Fothergill, A., Rinaldi, M., Eng, T. et al. (2003) Multiple patterns of resistance to fluconazole in Candida glabrata isolates from a patient with oropharyngeal candidiasis receiving head and neck radiation. J Clin Microbiol 41, 619-622.
36. Salatino, A., Fernandes-Silva, C.C., Righi, A.A. and Salatino, M.L. (2011) Propolis research and the chemistry of plant products. Nat Prod Rep 28, 925-936.
37. Sanglard, D. and Odds, F. (2002) Resistance of Candida species to antifungal agents: molecular mechanisms and clinical consequences. Lancet Infect Dis 2, 73-85.
38. Sforcin, J. and Bankova, V. (2011) Propolis: is there a potential for the development of new drugs? J Ethnopharmacol 133, 253-260.
39. Shokri, H., Khosravi, A. and Yalfani, R. (2011) Antifungal efficacy of propolis against fluconazole-resistant Candida glabrata isolates obtained from women with recurrent vulvovaginal candidiasis. Int J Gynecol Obstet 114, 158-159.
40. Siqueira, A.B.S., Gomes, B.S., Cambuim, I., Maia, R., Abreu, S., Souza-Motta, C.M., Queiroz, L.A. and Porto, A.L.F. (2009) Trichophyton species susceptibility to green and red propolis from Brazil. Lett Appl Microbiol 48, 90-96.
41. Stepanovic, S., Antic, N., Dakic, L. and Svabic-Vlahovic, M. (2003) In vitro antimicrobial activity of propolis and synergism between propolis and antimicrobial drugs. Microbiol Res 158, 353-357.
42. Takaisi-Kikuni, N.B. and Schilcher, H. (1994) Electron microscopic and microcalorimetric investigations of the possible mechanism of the antibacterial action of a defined propolis provenance. Planta Med 60, 222-227.
43. Thein, Z.M., Seneviratne, C.J., Samaranayake, Y.H. and Samaranayake, L.P. (2009) Community lifestyle of Candida in mixed biofilms: a mini review. Mycoses 52, 467-475.
44. Tortorano, A., Kibbler, C., Peman, J., Bernhardt, H., Klingspor, L. and Grillot, R. (2006) Candidaemia in Europe: epidemiology and resistance. Int J Antimicrob Agents 27, 359-366.
45. Trofa, D., Gacser, A. and Nosanchuk, J. (2008) Candida parapsilosis, an emerging fungal pathogen. Clin Microbiol Rev 21, 606-625.
46. Trusheva, B., Popova, M., Bankova, V., Simova, S., Marcucci, M.C., Miorin, P.L., Pasin, F.R. and Tsvetkova, I. (2006) Bioactive constituents of Brazilian red propolis. Evid Based Complement Alternat Med 3, 249-254.
47. Ugur, A., Barlas, M., Ceyhan, N. and Turkmen, V. (2000) Antimicrobial effects of propolis extracts on Escherichia coli and Staphylococcus aureus strains resistant to various antibiotics and some microorganisms. J Med Food 3, 173-180.
48. Vargas, K., Messer, S.A., Pfaller, M., Lockhart, S.R., Stapleton, J.T., Hellstein, J. and Soll, D.R. (2000) Elevated phenotypic switching and drug resistance of Candida albicans from human immunodeficiency virus-positive individuals prior to first thrush episode. J Clin Microbiol 38, 3595-3607.
49. White, T.C. (1997) Increased mRNA levels of ERG16, CDR, and MDR1 correlate with increases in azole resistance in Candida albicans isolates from a patient infected with human immunodeficiency virus. Antimicrob Agents Chemother 41, 1482-1487.
50. Yarfani, R., Khosravi, A.R. and Shokri, H. (2010) The antifungal activity of Iranian propolis samples against fluconazole-resistant Candida albicans strains isolated from HIV+ patients with oropharyngeal candidiasis. J ApiProd ApiMed Sci 2, 161-166.