Folia Microbiologica

, Volume 64, Issue 1, pp 73–81 | Cite as

Effect of resveratrol and Regrapex-R-forte on Trichosporon cutaneum biofilm

  • Martina Paldrychová
  • Irena Kolouchová
  • Eva Vaňková
  • Olga MaťátkováEmail author
  • Jan Šmidrkal
  • Aleš Krmela
  • Věra Schulzová
  • Jana Hajšlová
  • Jan Masák
Original Article


Microorganisms that cause chronic infections exist predominantly as surface-attached stable communities known as biofilms. Microbial cells in biofilms are highly resistant to conventional antibiotics and other forms of antimicrobial treatment; therefore, modern medicine tries to develop new drugs that exhibit anti-biofilm activity. We investigated the influence of a plant polyphenolic compound resveratrol (representative of the stilbene family) on the opportunistic pathogen Trichosporon cutaneum. Besides the influence on the planktonic cells of T. cutaneum, the ability to inhibit biofilm formation and to eradicate mature biofilm was studied. We have tested resveratrol as pure compound, as well as resveratrol in complex plant extract—the commercially available dietary supplement Regrapex-R-forte, which contains the extract of Vitis vinifera grape and extract of Polygonum cuspidatum root. Regrapex-R-forte is rich in stilbenes and other biologically active substances. Light microscopy imaging, confocal microscopy, and crystal violet staining were used to quantify and visualize the biofilm. The metabolic activity of biofilm-forming cells was studied by the tetrazolium salt assay. Amphotericin B had higher activity against planktonic cells; however, resveratrol and Regrapex-R-forte showed anti-biofilm effects, both in inhibition of biofilm formation and in the eradication of mature biofilm. The minimum biofilm eradicating concentration (MBEC80) for Regrapex-R-forte was found to be 2222 mg/L (in which resveratrol concentration is 200 mg/L). These methods demonstrated that Regrapex-R-forte can be employed as an anti-biofilm agent, as it has similar effect as amphotericin B (MBEC80 = 700 mg/L), which is routinely used in clinical practice.


Anti-biofilm activity Trichosporon Stilbene Plant extract 


Funding information

This work was supported by the Czech Science Foundation (GACR) [17-15936S] and by the “Operational Programme Prague – Competitiveness” (CZ.2.16/3.1.00/24503) and the “National Program of Sustainability I” - NPU I (LO1601 - No.: MSMT-43760/2015).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.


  1. Andrews JM (2001) Determination of minimum inhibitory concentrations. J Antimicrob Chemother 48:5–16CrossRefGoogle Scholar
  2. Augustine N, Goel AK, Sivakumar KC, Ajay Kumar R, Thomas S (2014) Resveratrol – a potential inhibitor of biofilm formation in Vibrio cholerae. Phytomedicine 21:286–289CrossRefGoogle Scholar
  3. Coenye T, Brackman G, Rigole P, De Witte E, Honraet K, Rossel B, Nelis HJ (2012) Eradication of Propionibacterium acnes biofilms by plant extracts and putative identification of icariin, resveratrol and salidroside as active compounds. Phytomedicine 19:409–412CrossRefGoogle Scholar
  4. Colombo AL, Padovan ACB, Chaves GM (2011) Current knowledge of Trichosporon spp. and Trichosporonosis. Clin Microbiol Rev 24:682–700CrossRefGoogle Scholar
  5. Daglia M (2012) Polyphenols as antimicrobial agents. Curr Opin Biotechnol 23:174–181CrossRefGoogle Scholar
  6. de la Fuente-Núñez C, Reffuveille F, Fernández L, Hancock RE (2013) Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies. Curr Opin Microbiol 16:580–589CrossRefGoogle Scholar
  7. Di Bonaventura G, Pompilio A, Picciani C, Iezzi M, D'Antonio D, Piccolomini R (2006) Biofilm formation by the emerging fungal pathogen Trichosporon asahii: development, architecture, and antifungal resistance. Antimicrob Agents Chemother 50(10):3269–3276CrossRefGoogle Scholar
  8. Fridkin SK, Jarvis WR (1996) Epidemiology of nosocomial fungal infections. Clin Microbiol Rev 9:499–511CrossRefGoogle Scholar
  9. Gyawali R, Ibrahim SA (2014) Natural products as antimicrobial agents. Food Control 46:412–429CrossRefGoogle Scholar
  10. Herrera CL, Alvear M, Barrientos L, Montenegro G, Salazar LA (2010) The antifungal effect of six commercial extracts of Chilean propolis on Candida spp. Cienc Invest Agrar 37(1):75–84Google Scholar
  11. Houille B, Papon N, Boudesocque L, Bourdeaud E, Besseau S, Courdavault V, Enguehard-Gueiffier C, Delanoue G, Guerin L, Bouchara JP, Clastre M, Giglioli-Guivarch N, Guillard J, Lanoue A (2014) Antifungal activity of resveratrol derivatives against Candida species. J Nat Prod 77(7):1658–1662CrossRefGoogle Scholar
  12. Iturrieta-Gonzalez IA, Padovan ACB, Bizerra FC, Hahn RC, Colombo AL (2014) Multiple species of Trichosporon produce biofilms highly resistant to triazoles and amphotericin B. PLoS One 9(10):e109553CrossRefGoogle Scholar
  13. Jun JH, Seu YB, Lee DG (2007) Candicidal action of resveratrol isolated from grapes on human pathogenic yeast C. albicans. J Microbiol Biotechnol 17(8):1324–1329Google Scholar
  14. Karimzadeh I, Khalili H, Farsaei S, Dashti-Khavidaki S, Sagheb MM (2013) Role of diuretics and lipid formulations in the prevention of amphotericin B-induced nephrotoxicity. Eur J Clin Pharmacol 69:1351–1368CrossRefGoogle Scholar
  15. Kvasnickova E, Matatkova O, Cejkova A, Masak J (2015) Evaluation of baicalein, chitosan and usnic acid effect on Candida parapsilosis and Candida krusei biofilm using a Cellavista device. J Microbiol Methods 118:106–112CrossRefGoogle Scholar
  16. Lee J, Lee DG (2015) Novel antifungal mechanism of resveratrol: apoptosis inducer in Candida albicans. Curr Microbiol 70(3):383–389CrossRefGoogle Scholar
  17. Lee JH, Cho HS, Joo SW, Chandra Regmi S, Kim JA, Ryu CM, Ryu SY, Cho MH, Lee J (2013) Diverse plant extracts and trans-resveratrol inhibit biofilm formation and swarming of Escherichia coli O157: H7. Biofouling 29:1189–1203CrossRefGoogle Scholar
  18. Lee S, Lee H, Min H, Park K, Lee K, AhnY CY, Pyee J (2005) Antibacterial and antifungal activity of pinosylvin, a constituent of pine. Fitoterapia 76:258–260CrossRefGoogle Scholar
  19. Long J, Gao H, Sun L, Liu J, Zhao-Wilson X (2009) Grape extract protects mitochondria from oxidative damage and improves locomotor dysfunction and extends lifespan in a Drosophila Parkinson’s disease model. Rejuvenation Res 12(5):321–331CrossRefGoogle Scholar
  20. López-Nicolás JM, Núñez-Delicado E, Pérez-López AJ, Barrachina ÁC, Cuadra-Crespo P (2006) Determination of stoichiometric coefficients and apparent formation constants for β-cyclodextrin complexes of trans-resveratrol using reversed-phase liquid chromatography. J Chromatogr A 1135(2):158–165CrossRefGoogle Scholar
  21. Mah TFC, O'Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39CrossRefGoogle Scholar
  22. Melo AS, Bizerra FC, Freymuller E, Arthington-Skaggs BA, Colombo AL (2011) Biofilm production and evaluation of antifungal susceptibility amongst clinical Candida spp. isolates, including strains of the Candida parapsilosis complex. Med Mycol 49(3):253–262CrossRefGoogle Scholar
  23. Mesa-Arango AC, Scorzoni L, Zaragoza O (2012) It only takes one to do many jobs: amphotericin B as antifungal and immunomodulatory drug. Front Microbiol 3(286).
  24. Morinaga N, Yahiro K, Noda M (2010) Resveratrol, a natural polyphenolic compound, inhibits cholera toxin-induced cyclic AMP accumulation in Vero cells. Toxicon 56:29–35CrossRefGoogle Scholar
  25. Peeters E, Nelis HJ, Coenye T (2008) Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J Microbiol Methods 72:157–165CrossRefGoogle Scholar
  26. Prokop J, Abrman P, Seligson AL, Sovak M (2006) Resveratrol and its glycon piceid are stable polyphenols. J Med Food 9(1):11–14CrossRefGoogle Scholar
  27. Riihinen KR, Ou ZM, Gödecke T, Lankin DC, Pauli GF, Wu CD (2014) The antibiofilm activity of lingonberry flavonoids against oral pathogens is a case connected to residual complexity. Fitoterapia 97:78–86CrossRefGoogle Scholar
  28. Sabaeifard P, Abdi-Ali A, Soudi MR, Dinarvand R (2014) Optimization of tetrazolium salt assay for Pseudomonas aeruginosa biofilm using microtiter plate method. J Microbiol Methods 105:134–140CrossRefGoogle Scholar
  29. Seleem D, Pardi V, Murata RM (2017) Review of flavonoids: a diverse group of natural compounds with anti-Candida albicans activity in vitro. Arch Oral Biol 76:76–83CrossRefGoogle Scholar
  30. Silva WJD, Seneviratne J, Parahitiyawa N, Rosa EAR, Samaranayake LP, Cury AADB (2008) Improvement of XTT assay performance for studies involving Candida albicans biofilms. Braz Dent J 19:364–369CrossRefGoogle Scholar
  31. Thimothe J, Bonsi IA, Padilla-Zakour OI, Koo H (2007) Chemical characterization of red wine grape (Vitis vinifera and Vitis interspecific hybrids) and pomace phenolic extracts and their biological activity against Streptococcus mutans. J Agric Food Chem 55:10200–10207CrossRefGoogle Scholar
  32. Weber K, Schulz B, Ruhnke M (2011) Resveratrol and its antifungal activity against Candida species. Mycoses 54(1):30–33CrossRefGoogle Scholar
  33. Xu C, Yagiz Y, Hs WY, Simonne A, Lu J, Marshall MR (2014) Antioxidant, antibacterial, and antibiofilm properties of polyphenols from muscadine grape (Vitis rotundifolia Michx.) pomace against selected foodborne pathogens. J Agric Food Chem 62(28):6640–6649CrossRefGoogle Scholar
  34. Yousefbeyk F, Gohari AR, Hashemighahderijani Z, Ostad SN, Sourmaghi MHS, Amini M, Golfakhrabadi F, Jamalifar H, Amin G (2014) Bioactive terpenoids and flavonoids from Daucus littoralis Smith subsp. hyrcanicus Rech. f, an endemic species of Iran. Daru J Pharm Sci 22(1):12CrossRefGoogle Scholar

Copyright information

© Institute of Microbiology, Academy of Sciences of the Czech Republic, v.v.i. 2018

Authors and Affiliations

  1. 1.Department of BiotechnologyUniversity of Chemistry and Technology, PraguePragueCzech Republic
  2. 2.Department of Dairy, Fat and CosmeticsUniversity of Chemistry and Technology, PraguePragueCzech Republic
  3. 3.Department of Food Analysis and NutritionUniversity of Chemistry and Technology, PraguePragueCzech Republic

Personalised recommendations