Antifungal effects of the flavonoids kaempferol and quercetin: a possible alternative for the control of fungal biofilms

References

• Abi-Chacra ÉA, Souza LO, Cruz LP, Braga-Silva LA, Gonçalves DS, Sodré CL, Ribeiro MD, Seabra SH, Figueiredo-Carvalho MH, Barbedo LS, et al. 2013. Phenotypical properties associated with virulence from clinical isolates belonging to the Candida parapsilosis complex. FEMS Yeast Res. 13: 831–848. doi: 10.1111/1567-1364.12092
   PubMed Web of Science ®Google Scholar
• Anwar F, Latif S, Ashraf M, Gilani AH. 2007. Moringa oleifera: a food plant with multiple medicinal uses. Phytother Res. 21: 17–25. doi: 10.1002/ptr.2023
   PubMed Web of Science ®Google Scholar
• Brilhante RS, de Alencar LP, Cordeiro RA, Castelo-Branco DS, Teixeira CE, Macedo RB, Lima DT, Paiva-Neto MA, Monteiro AJ, Alves ND, et al. 2013. Detection of Candida species resistant to azoles in the microbiota of rheas (Rhea americana): possible implications for human and animal health. J Med Microbiol. 62: 889–895. doi: 10.1099/jmm.0.055566-0
   PubMed Web of Science ®Google Scholar
• Brilhante RS, Rodrigues TJ, Castelo-Branco DS, Teixeira CE, Macedo RB, Bandeira SP, de Alencar LP, Monteiro AJ, Cordeiro RA, Bandeira TJ, et al. 2014. Antifungal susceptibility and virulence attributes of animal-derived isolates of Candida parapsilosis complex. J Med Microbiol. 63: 1568–1572. doi: 10.1099/jmm.0.076216-0
   PubMed Web of Science ®Google Scholar
• Brilhante RS, Sales JA, Sampaio CM, Barbosa FG, Paiva-Neto MA, Guedes GM, De Alencar LP, de Pontes YB, Bandeira TJ, Moreira JL, et al. 2015. Vibrio spp. from Macrobrachium amazonicum prawn farming are inhibited by Moringa oleifera extracts. Asian Pac J Trop Med. 8: 919–922. doi: 10.1016/j.apjtm.2015.10.012
   PubMed Web of Science ®Google Scholar
• Brilhante RS, Sales JA, Pereira VS, Castelo-Branco DS, Cordeiro RA, Sampaio CM, Paiva-Neto MA, Santos JB, Sidrim JJ, Rocha MF. 2017. Research advances on the multiple uses of Moringa oleifera: a sustainable alternative for socially neglected population. Asian Pac J Trop Med. 10: 621–630. doi: 10.1016/j.apjtm.2017.07.002
   PubMed Web of Science ®Google Scholar
• Brilhante RS, Sales JA, Silva ML, Oliveira JS, Pereira LA, Pereira-Neto WA, Cordeiro RA, Sidrim JJ, Castelo-Branco DS, Rocha MF. 2018. Antifungal susceptibility and virulence of Candida parapsilosis species complex: an overview of their pathogenic potential. J Med Microbiol. 67: 903–914. doi: 10.1099/jmm.0.000756
   PubMed Web of Science ®Google Scholar
• Cavalheiro M., Teixeira MC. 2018. Candida biofilms: threats, challenges, and promising strategies. Front Med. (Lausanne).
   Google Scholar
• Chao P, Shi GS, Boost M. 2015. Inhibitory effects of 2,2'-Dipyridyl and 1,2,3,4,6-Penta-O-Galloyl-b-D-Glucopyranose on biofilm formation in contact lens cases. Invest Ophthalmol Vis Sci. 56: 7053–7057. doi: 10.1167/iovs.15-17723
   PubMed Web of Science ®Google Scholar
• CLSI, 2008. Reference method for broth dilution antifungal susceptibility testing of yeasts: approved Standard. CLSI Document M27-A3. Clinical and Laboratory Standards Institute, Wayne, PA.
   Google Scholar
• CLSI, 2012. Reference method for broth dilution antifungal susceptibility testing of yeasts—fourth informational supplement. CLSI Document M27-S4. Clinical and Laboratory Standards Institute, Wayne, PA.
   Google Scholar
• Cordeiro RA, Sales JA, Castelo-Branco DSCM, Brilhante RSN, Ponte YB, Araújo GS, Mendes PBL, Pereira VS, de Alencar LP, Pinheiro AQ, et al. 2017a. Candida parapsilosis complex in veterinary practice: a historical overview, biology, virulence attributes and antifungal susceptibility traits. Vet Microbiol. 212: 22–30. doi: 10.1016/j.vetmic.2017.07.031
   PubMed Web of Science ®Google Scholar
• Cordeiro RA., Sales JA., de Ponte YB., Mendes PB., Serpa R., Evangelista AJ., de Alencar LP., Pereira-Neto WA., Brilhante RS., Sidrim JJ., et al. 2018. Phenotype-driven strategies for screening Candida parapsilosis complex for molecular identification. Braz J Microbiol. 49: 193–198. doi: 10.1016/j.bjm.2017.11.004
   PubMed Web of Science ®Google Scholar
• Cordeiro RA, Serpa R, Mendes PB, Evangelista AJ, Andrade AR, Franco JD, Pereira VD, Alencar LP, Oliveira JS, Camargo ZP, et al. 2017b. The HIV aspartyl protease inhibitor ritonavir impairs planktonic growth, biofilm formation and proteolytic activity in Trichosporon spp. Biofouling. 33: 640–650. doi: 10.1080/08927014.2017.1350947
   PubMed Web of Science ®Google Scholar
• Cushnie TP, Lamb AJ. 2005. Antimicrobial activity of flavonoids. Int J Antimicrob Agents. 26: 343–356. doi: 10.1016/j.ijantimicag.2005.09.002
   PubMed Web of Science ®Google Scholar
• Dhayalan A, Gracilia DE, Dela Peña RA, Malison MT, Pangilinan CR. 2018. Phytochemical constituents and antimicrobial activity of the ethanol and chloroform crude leaf extracts of Spathiphyllum cannifolium (Dryand. Ex Sims) Schott. J. Pharm. Bioallied Sci. 10: 15–20.
   PubMed Web of Science ®Google Scholar
• Gao M, Wang H, Zhu L. 2016. Quercetin assists fluconazole to inhibit biofilm formation of fluconazole-resistant Candida albicans in in vitro and in vivo antifungal managements of vulvovaginal candidiasis. Cell Physiol Biochem. 40: 727–742. doi: 10.1159/000453134
   PubMed Web of Science ®Google Scholar
• Garzilo C, Bagattini M, Bogdanović L, Di Popolo A, Lula DV, Catania MR, Raimondi F, Triassi M, Zarrilli R. 2017. Risk factors for Candida parapsilosis bloodstream infection in a neonatal intensive care unit: a case-control study. Ital J Pedriatr. 43: 10. doi: 10.1186/s13052-017-0332-5
   PubMed Web of Science ®Google Scholar
• Latiff A, Mukherjee P, Chandra J, Swindell K, Lockhart S, Diekema D, Pfaller M, Ghannoum M. 2010. Characterization of biofilms formed by Candida parapsilosis, C. metapsilosis, and C. orthopsilosis. Int J Med Microbiol. 300: 265–270. doi: 10.1016/j.ijmm.2009.09.001
   PubMed Web of Science ®Google Scholar
• Leone A, Spada A, Battezzati A, Schiraldi A, Aristil J, Bertoli S. 2016. Moringa oleifera seeds and oil: characteristics and uses for human health. Int J Mol Sci. 17: 2141–2152. doi: 10.3390/ijms17122141
   PubMed Web of Science ®Google Scholar
• Lin S, Chen R, Zhu S, Wang H, Wang L, Zou J, Yan J, Zhang X, Farmakiotis D, Tan X, et al. 2018. Candidemia in adults at a tertiary hospital in China: clinical characteristics, species distribution, resistance, and outcomes. Mycopathologia. 183: 679–689. doi: 10.1007/s11046-018-0258-5
   PubMed Web of Science ®Google Scholar
• Lo HJ, Tsai SH, Chu WL, Chen YZ, Zhou ZL, Chen HF, Lee CF, Yang YL. 2017. Fruits as the vehicle of drug resistant pathogenic yeasts. J Infect. 75: 254–262. doi: 10.1016/j.jinf.2017.06.005
   PubMed Web of Science ®Google Scholar
• Ming D, Wang D, Cao F, Xiang H, Mu D, Cao J, Li B, Zhong L, Dong X, Zhong X, et al. 2017. Kaempferol inhibits the primary attachment phase of biofilm formation in Staphylococcus aureus. Front Microbiol. 15: 2263.
   Web of Science ®Google Scholar
• Muhammad AA., Pauzi NA., Arulselvan P., Abas F., Fakurazi S. 2013. In vitro wound healing potential and identification of bioactive compounds from Moringa oleifera. Biomed Res Int.
   Web of Science ®Google Scholar
• Neji S, Hadrich I, Trabelsi H, Abbes S, Cheikhrouhou F, Sellami H, Makni F, Ayadi A. 2017. Virulence factors, antifungal susceptibility and molecular mechanisms of azole resistance among Candida parapsilosis complex isolates recovered from clinical specimens. J Biomed Sci. 24: 67–83. doi: 10.1186/s12929-017-0376-2
   PubMed Web of Science ®Google Scholar
• Oliveira VM, Carraro E, Auler ME, Khalil NM. 2016. Quercetin and rutin as potential agents antifungal against Cryptococcus spp. Braz J Biol. 76: 1029–1034. doi: 10.1590/1519-6984.07415
   PubMed Web of Science ®Google Scholar
• Robl D, Thimoteo SS, de Souza GC, Beux MR, Dalzoto PR, Pinheiro RL, Pimentel IC. 2014. Occurrence of Candida orthopsilosis in Brazilian tomato fruits (Lycopersicum esculentum Mill.). Braz J Microbiol. 45: 105–109. doi: 10.1590/S1517-83822014000100015
   PubMed Web of Science ®Google Scholar
• Rocha MF, Alencar LP, Brilhante RS, Sales JA, Ponte YB, Rodrigues PH, Sampaio CM, Cordeiro RA, Castelo-Branco DS, de Oliveira FC, et al. 2014. Moringa oleifera inhibits growth of Candida spp. and Hortaea werneckii isolated from Macrobrachium amazonicum prawn farming with a wide margin of safety. Cienc Rural 44: 2197–2203. doi: 10.1590/0103-8478cr20140266
   Web of Science ®Google Scholar
• Rocha MF, de Aguiar FL, Brilhante RS, Cordeiro RA, Teixeira CE, Castelo-Branco DS, Paiva-Neto MA, Zeferino JP, Mafezoli J, Sampaio CM, et al. 2011. Extratos de Moringa oleifera e Vernonia sp. sobre Candida albicans e Microsporum canis isolados de cães e gatos e análise da toxicidade em Artemia sp. [Moringa oleifera and Vernonia sp. extracts against Candida albicans and Microsporum canis isolates from dogs and cats and analysis of toxicity to Artemia sp]. Cienc Rural. 41: 1807–1812. doi: 10.1590/S0103-84782011001000022
   Web of Science ®Google Scholar
• Rocha MF, Alencar LP, Paiva-Neto MA, Melo LM, Bandeira SP, Ponte YB, Sales JA, Guedes GM, Castelo-Branco DS, Bandeira TJ, et al. 2016. Cross-resistance to fluconazole induced by exposure to the agricultural azole tetraconazole: an environmental resistance school? Mycoses 59: 281–290. doi: 10.1111/myc.12457
   PubMed Web of Science ®Google Scholar
• Shao J, Zhang M, Wang T, Li Y, Wang C. 2016. The roles of CDR1, CDR2, and MDR1, in kaempferol-induced suppression with fluconazole-resistant Candida albicans. Pharm Biol. 54: 984–992. doi: 10.3109/13880209.2015.1091483
   PubMed Web of Science ®Google Scholar
• Silva CR, Andrade-Neto JB, Campos RS, Figueiredo NS, Sampaio LS, Magalhães HI, Cavalcanti BC, Gaspar DM, Andrade GM, Lima IS, et al. 2014. Synergistic effect of the flavonoid catechin, quercetin, or epigallocatechin gallate with fluconazole induces apoptosis in Candida tropicalis resistant to fluconazole. Antimicrob Agents Chemother. 58: 1468–1478. doi: 10.1128/AAC.00651-13
   PubMed Web of Science ®Google Scholar
• Silva BV, Silva LB, Oliveira DB, Silva PR, Ferreira-Paim K, Andrade-Silva LE, Silva-Vergara ML, Andrade AA. 2015. Species distribution, virulence factors, and antifungal susceptibility among Candida parapsilosis complex isolates recovered from clinical specimens. Mycopathologia. 180: 333–343. doi: 10.1007/s11046-015-9916-z
   PubMed Web of Science ®Google Scholar
• Tavanti A, Davidson AD, Gow NA, Maiden MC, Odds FC. 2005. Candida orthopsilosis and Candida metapsilosis spp. nov. to replace Candida parapsilosis groups II and III. J Clin Microbiol. 43: 284–292. doi: 10.1128/JCM.43.1.284-292.2005
   PubMed Web of Science ®Google Scholar