Folia Microbiologica

, Volume 63, Issue 3, pp 261–272 | Cite as

Resveratrol, pterostilbene, and baicalein: plant-derived anti-biofilm agents

  • Irena Kolouchová
  • Olga Maťátková
  • Martina Paldrychová
  • Zdeněk Kodeš
  • Eva Kvasničková
  • Karel Sigler
  • Alena Čejková
  • Jan Šmidrkal
  • Kateřina Demnerová
  • Jan Masák
Original Article
  • 259 Downloads

Abstract

Microbial adhesion to surfaces and the subsequent biofilm formation may result in contamination in food industry and in healthcare-associated infections and may significantly affect postoperative care. Some plants produce substances with antioxidant and antimicrobial properties that are able to inhibit the growth of food-borne pathogens. The aim of our study was to evaluate antimicrobial and anti-biofilm effect of baicalein, resveratrol, and pterostilbene on Candida albicans, Staphylococcus epidermidis, Pseudomonas aeruginosa, and Escherichia coli. We determined the minimum inhibitory concentrations (MIC), the minimum adhesion inhibitory concentration (MAIC), and the minimum biofilm eradication concentration (MBEC) by crystal violet and XTT determination. Resveratrol and pterostilbene have been shown to inhibit the formation of biofilms as well as to disrupt preformed biofilms. Our results suggest that resveratrol and pterostilbene appear potentially very useful to control and inhibit biofilm contaminations by Candida albicans, Staphylococcus epidermidis, and Escherichia coli in the food industry.

Keywords

Baicalein Resveratrol Pterostilbene Adhesion Eradication Biofilm 

Notes

Acknowledgements

This work was supported by the Czech Science Foundation (GA CR) [grant number 17-15936S] and 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).

References

  1. Alakomi HL, Puupponen-Pimia R, Aura AM, Helander IM, Nohynek L, Oksman-Caldentey KM, Saarela M (2007) Weakening of Salmonella with selected microbial metabolites of berry-derived phenolic compounds and organic acids. J Agric Food Chem 55:3905–3912CrossRefPubMedGoogle Scholar
  2. Al-Shabib NA, Husain FM, Ahmad I, Khan MS, Khan RA, Khan JM (2017) Rutin inhibits mono and multi-species biofilm formation by foodborne drug resistant Escherichia coli and Staphylococcus aureus. Food Control 79:325–332CrossRefGoogle Scholar
  3. Andrews JM (2001) Determination of minimum inhibitory concentrations. J Antimicrob Chemother 48:5–16CrossRefPubMedGoogle Scholar
  4. Awolola VG (2014) Antibacterial and anti-biofilm activity of Ficus sansibarica Warb. subsp Sansibarica (Moraceae) extracts. Planta Med 80:779–779Google Scholar
  5. Bakkiyaraj D, Nandhini JR, Malathy B, Pandian SK (2013) The anti-biofilm potential of pomegranate (Punica granatum L.) extract against human bacterial and fungal pathogens. Biofouling 29:929–937CrossRefPubMedGoogle Scholar
  6. Balagopal A, Kothandapani S, Prathapkumar HS (2017) Study on E. coli and Salmonella biofilms from fresh fruits and vegetables. J Food Sci Technol 54:1091–1097CrossRefGoogle Scholar
  7. Barchiesi F, Di Francesco LF, Compagnucci P, Arzeni D, Giacometti A, Scalise G (1998) In-vitro interaction of terbinafine with amphotericin B, fluconazole and itraconazole against clinical isolates of Candida albicans. J Antimicrob Chemother 41:59–65CrossRefPubMedGoogle Scholar
  8. Bizerra FC, Nakamura CV, de Poersch C, Estivalet Svidzinski TI, Borsato Quesada RM, Goldenberg S, Krieger MA, Yamada-Ogatta SF (2008) Characteristics of biofilm formation by Candida tropicalis and antifungal resistance. FEMS Yeast Res 8:442–450CrossRefPubMedGoogle Scholar
  9. Bridier A, Sanchez-Vizuete P, Guilbaud M, Piard JC, Naitali M, Briandet R (2015) Biofilm-associated persistence of food-borne pathogens. Food Microbiol 45:167–178CrossRefPubMedGoogle Scholar
  10. Cao Y, Dai B, Wang Y, Huang S, Xu Y, Cao Y, Gao P, Zhu Z, Jiang Y (2008) In vitro activity of baicalein against Candida albicans biofilms. Int J Antimicrob Agents 32:73–77CrossRefPubMedGoogle Scholar
  11. Chan MM-Y (2002) Antimicrobial effect of resveratrol on dermatophytes and bacterial pathogens of the skin. Biochem Pharmacol 63:99–104CrossRefPubMedGoogle Scholar
  12. Chang P-C, Li H-Y, Tang H-J, Liu J-W, Wang J-J, Chuang Y-C (2007) In vitro synergy of baicalein and gentamicin against vancomycin-resistant Enterococcus. J Microbiol Immunol Infect 40:56–61PubMedGoogle Scholar
  13. Chen Y, Liu TJ, Wang K, Hou CC, Cai SQ, Huang YY, Hu ZY, Huang H, Kong JL, Chen YQ (2016) Baicalein inhibits Staphylococcus aureus biofilm formation and the quorum sensing system in vitro. PLoS One 11:e0153468CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chmielewski RAN, Frank JF (2003) Biofilm formation and control in food processing facilities. Compr Rev Food Sci Food Saf 2:22–32CrossRefGoogle Scholar
  15. Cho HS, Lee J-H, Ryu SY, Joo SW, Cho MH, Lee J (2013) Inhibition of Pseudomonas aeruginosa and Escherichia coli O157:H7 biofilm formation by plant metabolite ε-viniferin. J Agric Food Chem 61:7120–7126CrossRefPubMedGoogle Scholar
  16. Cho HS, Lee J-H, Cho MH, Lee J (2015) Red wines and flavonoids diminish Staphylococcus aureus virulence with anti-biofilm and anti-hemolytic activities. Biofouling 31:1–11CrossRefPubMedGoogle Scholar
  17. Coenye T, Nelis HJ (2010) In vitro and in vivo model systems to study microbial biofilm formation. J Microbiol Methods 83:89–105CrossRefPubMedGoogle Scholar
  18. Coenye T, Brackman G, Rigole P, De Witte E, Honrae 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 19:409–412CrossRefPubMedGoogle Scholar
  19. Collado-Gonzalez M, Guirao-Abad JP, Sanchez-Fresneda R, Belchi-Navarro S, Arguelles JC (2012) Resveratrol lacks antifungal activity against Candida albicans. World J Microbiol Biotechnol 28:2441–2446CrossRefPubMedGoogle Scholar
  20. Cottart CH, Nivet-Antoine V, Laguillier-Morizot C, Beaudeux JL (2010) Resveratrol bioavailability and toxicity in humans. Mol Nutr Food Res 54:7–16CrossRefPubMedGoogle Scholar
  21. Cui H, Zhou H, Lin L (2016) The specific antibacterial effect of the Salvia oil nanoliposomes against Staphylococcus aureus biofilms on milk container. Food Control 61:92–98CrossRefGoogle Scholar
  22. da Silva RA, Bernardo LP, Lopes JM, Moreno LVS, Porto VC (2017) Equisetum giganteum influences the ability of Candida albicans in forming biofilms over the denture acrylic resin surface. Pharm Biol 55:1698–1702CrossRefPubMedGoogle Scholar
  23. Dai B-D, Cao Y-Y, Huang S, Xu Y-G, Gao P-H, Wang Y, Jiang Y-Y (2009) Baicalein induces programmed cell death in Candida albicans. J Microbiol Biotechnol 19:803–809PubMedGoogle Scholar
  24. Das A, Das MC, Sandhu P, Das N, Tribedi P, De UC, Akhterb Y, Bhattacharjee S (2017) Antibiofilm activity of Parkia javanica against Pseudomonas aeruginosa: a study with fruit extract. RSC Adv 7:5497–5513CrossRefGoogle Scholar
  25. Delamare APL, Moschen-Pistorello IT, Artico L, Atti-Serafini L, Echeverrigaray S (2007) Antibacterial activity of the essential oils of Salvia officinalis L. and Salvia triloba L. cultivated in South Brazil. Food Chem 100:603–608CrossRefGoogle Scholar
  26. Dinda B, Dinda S, DasSharma S, Banik R, Chakraborty A, Dinda M (2017) Therapeutic potentials of baicalin and its aglycone, baicalein against inflammatory disorders. Eur J Med Chem 131:68–80CrossRefPubMedGoogle Scholar
  27. Donald G, Hertzer K, Eibl G (2012) Baicalein—an intriguing therapeutic phytochemical in pancreatic cancer. Curr Drug Targ 13:1772–1776CrossRefGoogle Scholar
  28. Donlan RM (2001) Biofilm formation: a clinically relevant microbiological process. Clin Infect Dis 33:1387–1392CrossRefPubMedGoogle Scholar
  29. Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193CrossRefPubMedPubMedCentralGoogle Scholar
  30. Douglas LJ (2002) Medical importance of biofilms in Candida infections. Rev Iberoam Micol 19:139–143PubMedGoogle Scholar
  31. Dynes JJ, Lawrence JR, Korber DR, Swerhone GD, Leppard GG, Hitchcock AP (2009) Morphological and biochemical changes in Pseudomonas fluorescens biofilms induced by sub-inhibitory exposure to antimicrobial agents. Can J Microbiol 55:163–178CrossRefPubMedGoogle Scholar
  32. El-Sharif AA, Hussain MHM (2011) Chitosan-EDTA new combination is a promising candidate for treatment of bacterial and fungal infections. Curr Microbiol 62:739–745CrossRefPubMedGoogle Scholar
  33. Franzetti L, Scarpellini M (2007) Characterisation of Pseudomonas spp. isolated from foods. Ann Microbiol 57:39–47CrossRefGoogle Scholar
  34. Gonzales-Siles L, Sjoling A (2016) The different ecological niches of enterotoxigenic Escherichia coli. Environ Microbiol 18:741–751CrossRefPubMedGoogle Scholar
  35. Gowrishankar S, Pandian SK (2017) Modulation of Staphylococcus epidermidis (RP62A) extracellular polymeric layer by marine cyclic dipeptide-cyclo(L-leucyl-L-prolyl) thwarts biofilm formation. Biochim Biophys Acta 1859:1254–1262CrossRefPubMedGoogle Scholar
  36. Gupta P, Sarkar A, Sandhu P, Daware A, Das MC, Akhter Y, Bhattacharjee S (2017) Potentiation of antibiotic against Pseudomonas aeruginosa biofilm: a study with plumbagin and gentamicin. J Appl Microbiol 123:246–261CrossRefGoogle Scholar
  37. Haussler S, Fuqua C (2013) Biofilms 2012: new discoveries and significant wrinkles in a dynamic field. J Bacteriol 195:2947–2958CrossRefPubMedPubMedCentralGoogle Scholar
  38. Hawser SP, Norris H, Jessup CJ, Ghannoum MA (1998) Comparison of a 2,3-bis(2-methoxy-4-nitro-5-sulfophenyl)-5-[(phenylamino) carbonyl]-2h-tetrazolium hydroxide (xtt) colorimetric method with the standardized national committee for clinical laboratory standards method of testing clinical yeast isolates for susceptibility to antifungal agents. J Clin Microbiol 36:1450–1452PubMedPubMedCentralGoogle Scholar
  39. Hirschfeld J, Akinoglu E, Wirtz DC, Hoerauf A, Bekeredjian-Ding I, Jepsen S, Haddouti EM, Limmer A, Giersig M (2017) Long-term release of antibiotics by carbon nanotube-coated titanium alloy surfaces diminish biofilm formation by Staphylococcus epidermidis. Nanomedicine 13:1587–1593CrossRefPubMedGoogle Scholar
  40. Hu DD, Zhang RL, Zou Y, Zhong H, Zhang ES, Luo X, Wang Y, Jiang YY (2017) The structure-activity relationship of pterostilbene against Candida albicans biofilms. Molecules 22:360CrossRefGoogle Scholar
  41. Huang KC (1999) Antibacterial, antiviral, and antifungal herbst, the pharmacology of chinese herbst. In C. Press (Ed.): FloridaGoogle Scholar
  42. Huang S, Cao YY, Di Dai B, Sun XR, Zhu ZY, Cao YB, Wang Y, Gao PH, Jiang YY (2008) In vitro synergism of fluconazole and baicalein against clinical isolates of Candida albicans resistant to fluconazole. Biol Pharm Bull 31:2234–2236CrossRefPubMedGoogle Scholar
  43. Jung HJ, Hwang IA, Sung WS, Kang H, Kang BS, Seu YB, Lee DG (2005) Fungicidal effect of resveratrol on human infectious fungi. Arch Pharm Res 28:557–560CrossRefPubMedGoogle Scholar
  44. Jung HJ, Seu YB, Lee DG (2007) Candicidal action of resveratrol isolated from grapes on human pathogenic yeast C. albicans. J Microbiol Biotechnol 17:1324–1329PubMedGoogle Scholar
  45. Kolouchova I, Melzoch K, Smidrkal J, Filip V (2005) The content of resveratrol in vegetables and fruit. Chem List 99:492–495Google Scholar
  46. Kosuru R, Rai U, Prakash S, Singh A, Singh S (2016) Promising therapeutic potential of pterostilbene and its mechanistic insight based on preclinical evidence. Eur J Pharmacol 789:229–243CrossRefPubMedGoogle Scholar
  47. Kuhn DM (2002) Comparison of biofilms formed by Candida albicans and Candida parapsilosis on bioprosthetic surfaces. Infect Immun 70:878–888CrossRefPubMedPubMedCentralGoogle Scholar
  48. Kuhn DM, Mukherjee PK, Clark TA, Pujol C, CHandra J, Hajjeh RA, Warnock D, Soll DR, Ghannoum MA (2004) Candida parapsilosis characterization in a outbreak setting. Emerg Infect Dis 10:1074–1081CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kvasničková E, Maťátková O, Čejková A, Masák J (2015) Evaluation of baicalein, chitosan and usnic acid effect on Candida parapsilosis and Candida krusei biofilm using a Cellavista device. J Microbiol Methods 118:106–112CrossRefPubMedGoogle Scholar
  50. Laverty G, McCloskey AP, Gorman SP, Gilmore BF (2015) Anti-biofilm activity of ultrashort cinnamic acid peptide derivatives against medical device-related pathogens. J Pept Sci 21:770–778CrossRefPubMedGoogle Scholar
  51. Lee JH, Cho HS, Joo SW, Regm SC, 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 29:1189–1203CrossRefPubMedGoogle Scholar
  52. Lee JH, Kim YG, Ryu SY, Cho MH, Lee J (2014a) Resveratrol oligomers inhibit biofilm formation of Escherichia coli O157:H7 and Pseudomonas aeruginosa. J Nat Prod 77:168–172CrossRefPubMedGoogle Scholar
  53. Lee K, Lee JH, Ryu SY, Cho MH, Lee J (2014b) Stilbenes reduce Staphylococcus aureus hemolysis, biofilm formation, and virulence. Foodborne Pathog Dis 11:710–717CrossRefPubMedGoogle Scholar
  54. Leid JG, Kerr M, Selgado C, Johnson C, Moreno G, Smith A, Shirtliff ME, O'Toole GA, Cope EK (2009) Flagellum-mediated biofilm defense mechanisms of Pseudomonas aeruginosa against host-derived lactoferrin. Infect Immun 77:4559–4566CrossRefPubMedPubMedCentralGoogle Scholar
  55. Li DD, Zhao LX, Mylonakis E, Hu GH, Zou Y, Huang TK, Yan L, Wang Y, Jiang YY (2014) In vitro and in vivo activities of pterostilbene against Candida albicans biofilms. Antimicrob Agents Chemother 58:2344–2355CrossRefPubMedPubMedCentralGoogle Scholar
  56. Luo J, Kong JL, Dong BY, Huang H, Wang K, Wu LH, Hou CC, Liang Y, Li B, Chen YQ (2016) Baicalein attenuates the quorum sensing-controlled virulence factors of Pseudomonas aeruginosa and relieves the inflammatory response in P. aeruginosa-infected macrophages by downregulating the MAPK and NFkappaB signal-transduction pathways. Drug Des Devel Ther 10:183–203CrossRefPubMedPubMedCentralGoogle Scholar
  57. Mah T-FC, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39CrossRefPubMedGoogle Scholar
  58. Marinas IC, Oprea E, Chifiriuc MC, Badea IA, Buleandra M, Lazara V (2015) Chemical composition and antipathogenic activity of Artemisia annua essential oil from romania. Chem Biodivers 12:1554–1564CrossRefPubMedGoogle Scholar
  59. Martin NH, Murphy SC, Ralyea RD, Wiedmann M, Boor KJ (2011) When cheese gets the blues: Pseudomonas fluorescens as the causative agent of cheese spoilage. J Dairy Sci 94:3176–3183CrossRefPubMedGoogle Scholar
  60. 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 49:253–262CrossRefPubMedGoogle Scholar
  61. Nguyen TH, Park MD, Otto M (2017) Host response to Staphylococcus Epidermidis colonization and infections. Front Cell Infect Microbiol 7: onlineGoogle Scholar
  62. Nimmy A, Goel AK, Sivakumar KC, Kumar RA, Sabu T (2014) Resveratrol—a potential inhibitor of biofilm formation in Vibrio cholerae. Phytomed 21:286–289CrossRefGoogle Scholar
  63. Nohynek LJ, Alakomi HL, Kahkonen MP, Heinonen M, Helander IM, Oksman-Caldentey KM, Puupponen-Pimia RH (2006) Berry phenolics: antimicrobial properties and mechanisms of action against severe human pathogens. Nutr Cancer 54:18–32CrossRefPubMedGoogle Scholar
  64. Nostro A, Guerrini A, Marino A, Tacchini M, Di Giulio M, Grandini A, Akin M, Cellini L, Bisignano G, Saraçoğlu HT (2016) In vitro activity of plant extracts against biofilm-producing food-related bacteria. Int J Food Microbiol 238:33–39CrossRefPubMedGoogle Scholar
  65. Okamoto-Shibayama K (2010) Resveratrol impaired the morphological transition of Candida albicans under various hyphae-inducing conditions. J Microbiol Biotechnol 20:942–945CrossRefPubMedGoogle Scholar
  66. O'Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Ann Rev Microbiol 54:49–79CrossRefGoogle Scholar
  67. Page MG, Heim J (2009) Prospects for the next anti-pseudomonas drug. Curr Opin Pharmacol 9:558–565CrossRefPubMedGoogle Scholar
  68. Pagedar A, Singh J (2015) Evaluation of antibiofilm effect of benzalkonium chloride, iodophore and sodium hypochlorite against biofilm of Pseudomonas aeruginosa of dairy origin. J Food Sci Technol 52:5317–5322CrossRefPubMedGoogle Scholar
  69. Palombo EA (2011) Traditional medicinal plant extracts and natural products with activity against oral bacteria: potential application in the prevention and treatment of oral diseases. Evid. Based Complement. Alternat Med 1–15Google Scholar
  70. Paulo L, Ferreira S, Gallardo E, Queiroz JA, Domingues F (2010) Antimicrobial activity and effects of resveratrol on human pathogenic bacteria. World J Microbiol Biotechnol 26:1533–1538CrossRefGoogle Scholar
  71. Pekmezovic M, Aleksic I, Barac A, Arsic-Arsenijevic V, Vasiljevic B, Nikodinovic-Runic J, Senerovic L (2016) Prevention of polymicrobial biofilms composed of Pseudomonas aeruginosa and pathogenic fungi by essential oils from selected citrus species. Pathog Dis 74:ftw102CrossRefPubMedGoogle Scholar
  72. Pompilio A, Crocetta V, Pomponio S, Fiscarelli E, Di Bonaventura G (2015) In vitro activity of colistin against biofilm by Pseudomonas aeruginosa is significantly improved under “cystic fibrosis-like” physicochemical conditions. Diagn Microbiol Infect Dis 82:318–325CrossRefPubMedGoogle Scholar
  73. Puligundla P, Mok C (2017) Potential applications of nonthermal plasmas against biofilm-associated micro-organisms in vitro. J Appl Microbiol 122:1134–1148CrossRefPubMedGoogle Scholar
  74. Rahman MRT, Lou Z, Yu F, Wang P, Wang H (2017) Anti-quorum sensing and anti-biofilm activity of Amomum tsaoko (Amommum tsao-ko Crevost et Lemarie) on foodborne pathogens. Saudi J Biol Sci 24:324–330CrossRefPubMedGoogle Scholar
  75. Rajasekharan SK, Ramesh S, Bakkiyaraj D (2014) Synergy of flavonoids with HDAC inhibitor: new approach to target Candida tropicalis biofilms. J Chemother 8:1–8Google Scholar
  76. Ramage G, Vande Walle K, Wickes BL, Lopez-Ribot JL (2001) Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother 45:2475–2479CrossRefPubMedPubMedCentralGoogle Scholar
  77. Ramage G, Saville SP, Thomas DP, Lopez-Ribot JL (2005) Candida biofilms: an update. Eukaryot Cell 4:633–638CrossRefPubMedPubMedCentralGoogle Scholar
  78. Ribic U, Klancnik A, Jersek B (2017) Characterization of Staphylococcus epidermidis strains isolated from industrial cleanrooms under regular routine disinfection. J Appl Microbiol 122:1186–1196CrossRefPubMedGoogle Scholar
  79. Ruzica T, Raspor P (2017) Influence of growth conditions on adhesion of yeast Candida spp. and Pichia spp. to stainless steel surfaces. Food Microbiol 65:179–184CrossRefGoogle Scholar
  80. Sardi JCO, Scorzoni L, Bernardi T, Fusco-Almeida AM, Mendes Giannini MJS (2013) Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options—review. J Med Microbiol 62:10–24CrossRefPubMedGoogle Scholar
  81. Selma MV, Larrosa M, Beltran D, Lucas R, Morales JC, Tomas-Barberan F, Espin JC (2012) Resveratrol and some glucosyl, glucosylacyl, and glucuronide derivatives reduce Escherichia coli O157:H7, Salmonella typhimurium, and Listeria monocytogenes Scott a adhesion to colonic epithelial cell lines. J Agric Food Chem 60:7367–7374CrossRefPubMedGoogle Scholar
  82. Serpa R, Franca EJ, Furlaneto-Maia L, Andrade CG, Diniz A, Furlaneto MC (2012) In vitro antifungal activity of the flavonoid baicalein against Candida species. J Med Microbiol 61:1704–1708CrossRefPubMedGoogle Scholar
  83. Sharma M, Manoharlal R, Negi AS, Prasad R (2010) Synergistic anticandidal activityof pure polyphenol curcuminI in combinationwith azoles and polyenes generates reactive oxygen species leading to apoptosis. FEMS Yeast Res 10:570–578PubMedGoogle Scholar
  84. Sievert DM, Ricks P, Edwards JR, Schneider A, Patel J, Srinivasan A, Kallen A, Limbago B, Fridkin S (2013) Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the national healthcare safety network at the centers for disease control and prevention, 2009-2010. Infect Cont Hosp Ep 34:1–14Google Scholar
  85. Singh B, Vuddanda PR, Vijayakumar MR, Kumar V, Saxena PS, Singh S (2014) Cefuroxime axetil loaded solid lipid nanoparticles for enhanced activity against S. aureus biofilm. Colloids Surf B 121:92–98CrossRefGoogle Scholar
  86. Szczuka E, Jabłonska L, Kaznowski A (2017) Effect of subinhibitory concentrations of tigecycline and ciprofloxacin on the expression of biofilm-associated genes and biofilm structure of Staphylococcus epidermidis. Microbiology-SGM 163:712–718CrossRefGoogle Scholar
  87. Tepe B, Daferera D, Sokmen A, Sokmen M, Polissio M (2005) Antimicrobial and antioxidant activities of the essential oil and various extracts of Salvia tomentosa Miller (Lamiaceae). Food Chem 90:333–340CrossRefGoogle Scholar
  88. Tote K, Horemans T, Vanden Berghe D, Mae L, Cos P (2010) Inhibitory effect of biocides on the viable masses and matrices of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 76:3135–3142CrossRefPubMedPubMedCentralGoogle Scholar
  89. Tsai HY, Ho CT, Chen YK (2017) Biological actions and molecular effects of resveratrol, pterostilbene, and 3′-hydroxypterostilbene. J Food Drug Anal 25:134–147CrossRefPubMedGoogle Scholar
  90. Van Houdt R, Michiels CW (2010) Biofilm formation and the food industry, a focus on the bacterial outer surface—review. J Appl Microbiol 109:1117–1131CrossRefPubMedGoogle Scholar
  91. Van Tassell JA, Martin NH, Murphy SC, Wiedmann M, Boor KJ, Ivy RA (2012) Evaluation of various selective media for the detection of Pseudomonas species in pasteurized milk. J Dairy Sci 95:1568–1574CrossRefPubMedGoogle Scholar
  92. Wahman S, Emara M, Shawky RM, El-Domany RA, Aboulwafa MM (2015) Inhibition of quorum sensing-mediated biofilm formation in Pseudomonas aeruginosa by a locally isolated Bacillus cereus. J Basic Microbiol 55:1406–1416CrossRefPubMedGoogle Scholar
  93. Wang K, Yan J, Dan W, Xie J, Yan B, Yan W, Sun M, Zhang B, Ma M, Zhao Y, Jia F, Zhu R, Chen W, Wang R (2014) Dual antifungal properties of cationic antimicrobial peptides polybia-MPI: membrane integrity disruption and inhibition of biofilm formation. Peptides 56:22–29CrossRefPubMedGoogle Scholar
  94. Weber K, Schulz B, Ruhnke M (2011) Resveratrol and its antifungal activity against Candida species. Mycoses 54:30–33CrossRefPubMedGoogle Scholar
  95. Wu J, Wen H (2009) Antifungal susceptibility analysis of berberine, baicalin, eugenol and curcumin on Candida albicans. J Med Coll PLA 24:142–147CrossRefGoogle Scholar
  96. Yun BY, Zhou L, Xie KP, Wang YJ, Xie MJ (2012) Antibacterial activity and mechanism of baicalein. Acta Pharm Sin 47:1587–1592Google Scholar
  97. Zeng Z, Qian L, Cao L, Tan H, Huang Y, Xue X, Shen Y, Zhou S (2008) Virtual screening for novel quorum sensing inhibitors to eradicate biofilm formation of Pseudomonas aeruginosa. Appl Microbiol Biotechnol 79:119–126CrossRefPubMedGoogle Scholar
  98. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333CrossRefPubMedGoogle Scholar
  99. Zhou Y, Wang G, Li Y, Liu Y, Song Y, Zheng W, Zhang N, Hu X, Yan S, Jia J (2012) In vitro interactions between aspirin and amphotericinB against planktonic cells and biofilm cells of Candida albicans and C. parapsilosis. Antimicrob Agents Chemother 56:3250–3260CrossRefPubMedPubMedCentralGoogle Scholar
  100. Zida A, Bamba S, Yacouba A, Ouedraogo-Traore R, Guiguemdé RT (2017) Anti-Candida albicans natural products, sources of new antifungal drugs: a review. J Mycol Med 27:1–19CrossRefPubMedGoogle Scholar

Copyright information

© Institute of Microbiology, Academy of Sciences of the Czech Republic, v.v.i. 2017

Authors and Affiliations

  • Irena Kolouchová
    • 1
  • Olga Maťátková
    • 1
  • Martina Paldrychová
    • 1
  • Zdeněk Kodeš
    • 1
  • Eva Kvasničková
    • 1
  • Karel Sigler
    • 2
  • Alena Čejková
    • 1
  • Jan Šmidrkal
    • 3
  • Kateřina Demnerová
    • 4
  • Jan Masák
    • 1
  1. 1.Department of BiotechnologyUniversity of Chemistry and TechnologyPragueCzech Republic
  2. 2.Institute of Microbiology, CASPragueCzech Republic
  3. 3.Department of Diary, Fat and Cosmetic ScienceUniversity of Chemistry and TechnologyPragueCzech Republic
  4. 4.Department of Biochemistry and MicrobiologyUniversity of Chemistry and TechnologyPragueCzech Republic

Personalised recommendations