Vitis vinifera canes are waste material of grapevine pruning and thus represent cheap source of high-value polyphenols. In view of the fact that resistance of many pathogenic microorganisms to antibiotics is a growing problem, the antimicrobial activity of plant polyphenols is studied as one of the possible approaches. We have investigated the total phenolic content, composition, antioxidant activity, and antifungal activity against Candida biofilm of an extract from winter canes and a commercially available extract from blue grapes. Light microscopy and confocal microscopy imaging as well as crystal violet staining were used to quantify and visualize the biofilm. We found a decrease in cell adhesion to the surface depending on the concentration of resveratrol in the cane extract. The biofilm formation was observed as metabolic activity of Candida albicans, Candida parapsilosis and Candida krusei biofilm cells and the minimum biofilm inhibitory concentrations were determined. The highest inhibition of metabolic activity was observed in Candida albicans biofilm after treatment with the cane extract (30 mg/L) and blue grape extract (50 mg/L). The composition of cane extract was analyzed and found to be comparatively different from blue grape extract. In addition, the content of total phenolic groups in cane extract was three-times higher (12.75 gGA/L). The results showed that cane extract was more effective in preventing biofilm formation than blue grape extract and winter canes have proven to be a potential source of polyphenols for antimicrobial and antibiofilm treatment.

Department of Biochemistry and Microbiology University of Chemistry and Technology 166 28 Prague Czech Republic

Department of Biotechnology University of Chemistry and Technology 166 28 Prague Czech Republic

Institute of Microbiology Czech Academy of Sciences 14220 Prague Czech Republic

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Tsao R. Chemistry and Biochemistry of Dietary Polyphenols. Nutrients. 2010;2:1231–1246. doi: 10.3390/nu2121231. PubMed DOI PMC

Squillaci G., Giorio L.A., Cacciola N.A., La Cara F., Morana A. Effect of temperature and time on the phenolic extraction from grape canes. In: Vilarinho C., Castro F., Conçalves M., Fernando A.L., editors. Wastes-Solutions, Treatments and Opportunities III. CRC Press; Abingdon, UK: Taylor & Francis Group; Abingdon, UK: 2020. pp. 34–40.

De Filippis B., Ammazzalorso A., Amoroso R., Giampietro L. Stilbene derivatives as new perspective in antifungal medicinal chemistry. Drug Dev. Res. 2019;80:285–293. doi: 10.1002/ddr.21525. PubMed DOI

Daglia M. Polyphenols as antimicrobial agents. Curr. Opin. Biotechnol. 2012;23:174–181. doi: 10.1016/j.copbio.2011.08.007. PubMed DOI

Shukla Y., Singh R. Resveratrol and cellular mechanisms of cancer prevention. Ann. N. Y. Acad. Sci. 2011;1215:1–8. doi: 10.1111/j.1749-6632.2010.05870.x. PubMed DOI

Dixon R.A. Natural products and plant disease resistance. Nat. Cell Biol. 2001;411:843–847. doi: 10.1038/35081178. PubMed DOI

Kolouchova I., Melzoch K., Smidrkal J., Filip V. The content of resveratrol in vegetables and fruit. Chem. Listy. 2005;99:492–495.

Filip V., Plocková M., Šmidrkal J., Špičková Z., Melzoch K., Schmidt Š. Resveratrol and its antioxidant and antimicrobial effectiveness. Food Chem. 2003;83:585–593. doi: 10.1016/S0308-8146(03)00157-2. DOI

Wang W., Tang K., Yang H.-R., Wen P.-F., Zhang P., Wang H.-L., Huang W.-D. Distribution of resveratrol and stilbene synthase in young grape plants (Vitis vinifera L. cv. Cabernet Sauvignon) and the effect of UV-C on its accumulation. Plant Physiol. Biochem. 2010;48:142–152. doi: 10.1016/j.plaphy.2009.12.002. PubMed DOI

Gorena T., Sáez V., Mardones C., Vergara C., Winterhalter P., von Baer D. Influence of post-pruning storage on stilbenoid levels in Vitis vinifera L. canes. Food Chem. 2014;155:256–263. doi: 10.1016/j.foodchem.2014.01.073. PubMed DOI

Kang K., Fong W.-P., Tsang P.W.-K. Antifungal Activity of Baicalein against Candida krusei Does Not Involve Apoptosis. Mycopathologia. 2010;170:391–396. doi: 10.1007/s11046-010-9341-2. PubMed DOI

Silva S., Negri M., Henriques M., Oliveira R., Williams D., Azeredo J. Adherence and biofilm formation of non-Candida albicans Candida species. Trends Microbiol. 2011;19:241–247. doi: 10.1016/j.tim.2011.02.003. PubMed DOI

Serpa R., França E.J.G., Maia L., Andrade C.G.T.J., Diniz A., Furlaneto M.C. In vitro antifungal activity of the flavonoid baicalein against Candida species. J. Med. Microbiol. 2012;61:1704–1708. doi: 10.1099/jmm.0.047852-0. PubMed DOI

Mukherjee P.K., Chandra J., Kuhn D.M., Ghannoum M.A. Mechanism of Fluconazole Resistance in Candida albicans Biofilms: Phase-Specific Role of Efflux Pumps and Membrane Sterols. Infect. Immun. 2003;71:4333–4340. doi: 10.1128/IAI.71.8.4333-4340.2003. PubMed DOI PMC

Tobudic S., Kratzer C., Lassnigg A., Presterl E. Antifungal susceptibility of Candida albicans in biofilms. Mycoses. 2012;55:199–204. doi: 10.1111/j.1439-0507.2011.02076.x. PubMed DOI

Singh B.N., Upreti D.K., Pandey G., Verma S., Roy S., Naqvi A.H., Rawat A.K.S. Quercetin Sensitizes Fluconazole-Resistant Candida albicans To Induce Apoptotic Cell Death by Modulating Quorum Sensing. Antimicrob. Agents Chemother. 2015;59:2153–2168. doi: 10.1128/AAC.03599-14. PubMed DOI PMC

Gharwalova L., Hutar D., Masak J., Kolouchova I. Antioxidant activity and phenolic content of organic and conventional vine cane extracts. Czech J. Food Sci. 2018;36:289–295.

Anna Malinowska M., Billet K., Drouet S., Munsch T., Unlubayir M., Tungmunnithum D., Giglioli-Guivarc’H N., Hano C., LaNoue A. Grape Cane Extracts as Multifunctional Rejuvenating Cosmetic Ingredient: Evaluation of Sirtuin Activity, Tyrosinase Inhibition and Bioavailability Potential. Molecules. 2020;25:2203. doi: 10.3390/molecules25092203. PubMed DOI PMC

Zhang A., Fang Y., Wang H., Li H., Zhang Z. Free-Radical Scavenging Properties and Reducing Power of Grape Cane Extracts from 11 Selected Grape Cultivars Widely Grown in China. Molecules. 2011;16:10104–10122. doi: 10.3390/molecules161210104. PubMed DOI PMC

Denaro M., Smeriglio A., Trombetta D. Antioxidant and Anti-Inflammatory Activity of Citrus Flavanones Mix and its Stability after In Vitro Simulated Digestion. Antioxidants. 2021;10:140. doi: 10.3390/antiox10020140. PubMed DOI PMC

Mattos G.N., Tonon R., Furtado A., Cabral L.M. Grape by-product extracts against microbial proliferation and lipid oxidation: A review. J. Sci. Food Agric. 2017;97:1055–1064. doi: 10.1002/jsfa.8062. PubMed DOI

Oliveira D.A., Salvador A.A., Smânia A., Smânia E.F.A., Maraschin M., Ferreira S.R.S. Antimicrobial Activity and Composition Profile of Grape (Vitis vinifera) Pomace Extracts Obtained by Supercritical Fluids. J. Biotechnol. 2013;164:423–432. doi: 10.1016/j.jbiotec.2012.09.014. PubMed DOI

Moreira M.M., Barroso M.F., Vasconcellos Porto J., Ramalhosa M.J., Švarc-Gaji’c J., Estevinho L., Morais S., Delerue-Matos C. Potential of Portuguese vine shoot wastes as natural resources of bioactive compounds. Sci Total Environ. 2018;634:831–842. doi: 10.1016/j.scitotenv.2018.04.035. PubMed DOI

Jesus M.S., Ballesteros L.F., Pereira R.N., Genisheva Z., Carvalho A.C., Pereira-Wilson C., Teixeira J.A., Domingues L. Ohmic heating polyphenolic extracts from vine pruning residue with enhanced biological activity. Food Chem. 2020;316:126298. doi: 10.1016/j.foodchem.2020.126298. PubMed DOI

Augustine N., Goel A., Sivakumar K., Kumar R.A., Thomas S. Resveratrol—A potential inhibitor of biofilm formation in Vibrio cholerae. Phytomedicine. 2014;21:286–289. doi: 10.1016/j.phymed.2013.09.010. PubMed DOI

Lee J., Lee D.G. Novel Antifungal Mechanism of Resveratrol: Apoptosis Inducer in Candida albicans. Curr. Microbiol. 2014;70:383–389. doi: 10.1007/s00284-014-0734-1. PubMed DOI

Rollová M., Gharwalova L., Krmela A., Schulzová V., HajšLová J., Jaroš P., Kolouchová I., Maťátková O. Grapevine extracts and their effect on selected gut-associated microbiota: In vitro study. Czech J. Food Sci. 2020;38:137–143. doi: 10.17221/308/2019-CJFS. DOI

Paldrychová M., Kolouchová I., Vaňková E., Maťátková O., Šmidrkal J., Krmela A., Schulzová V., Hajšlová J., Masák J. Effect of resveratrol and Regrapex-R-forte on Trichosporon cutaneum biofilm. Folia Microbiol. 2019;64:73–81. doi: 10.1007/s12223-018-0633-0. PubMed DOI

Andrews J.M. Determination of minimum inhibitory concentrations. J. Antimicrob. Chemother. 2001;48:5–16. doi: 10.1093/jac/48.suppl_1.5. PubMed DOI

Riss T., Moravec R., Niles A., Benink H., Worzella T., Minor L. Assay Guidance Manual: Cell Viability Assays. Eli Lilly & Company and the National Center for Advancing Translational Sciences; Bethesda, MD, USA: 2004.

Sabaeifard P., Abdi-Ali A., Soudi M.R., Dinarvand R. Optimization of tetrazolium salt assay for Pseudomonas aeruginosa biofilm using microtiter plate method. J. Microbiol. Methods. 2014;105:134–140. doi: 10.1016/j.mimet.2014.07.024. PubMed DOI

Kvasnickova E., Matatkova O., Cejkova A., Masak J. Evaluation of baicalein, chitosan and usnic acid effect on Candida parapsilosis and Candida krusei biofilm using a Cellavista device. J. Microbiol. Methods. 2015;118:106–112. doi: 10.1016/j.mimet.2015.09.002. PubMed DOI

Fidler M., Kolářová L. Analýza antioxidantů v chmelu a pivu. Chem. Listy. 2009;103:232–235.

Alonso Á.M., Guillén D.A., Barroso C.G., Puertas B., García A. Determination of Antioxidant Activity of Wine Byproducts and Its Correlation with Polyphenolic Content. J. Agric. Food Chem. 2002;50:5832–5836. doi: 10.1021/jf025683b. PubMed DOI

Coenye T., Brackman G., Rigole P., De Witte E., Honraet K., Rossel B., Nelis H.J. Eradication of Propionibacterium acnes biofilms by plant extracts and putative identification of icariin, resveratrol and salidroside as active compounds. Phytomedicine. 2012;19:409–412. doi: 10.1016/j.phymed.2011.10.005. PubMed DOI

Lee J.-H., Cho H.S., Joo S.W., Regmi S.C., Kim J.-A., Ryu C.-M., Ryu S.Y., Cho M.H., Lee J. Diverse plant extracts and trans-resveratrol inhibit biofilm formation and swarming of Escherichia coli O157:H7. Biofouling. 2013;29:1189–1203. doi: 10.1080/08927014.2013.832223. PubMed DOI

Sheng J.-Y., Chen T.-T., Tan X.-J., Chen T., Jia A.-Q. The quorum-sensing inhibiting effects of stilbenoids and their potential structure–activity relationship. Bioorganic Med. Chem. Lett. 2015;25:5217–5220. doi: 10.1016/j.bmcl.2015.09.064. PubMed DOI

Seleem D., Pardi V., Murata R.M. Review of flavonoids: A diverse group of natural compounds with anti-Candida albicans activity in vitro. Arch. Oral Biol. 2017;76:76–83. doi: 10.1016/j.archoralbio.2016.08.030. PubMed DOI

Xu C., Yagiz Y., Hsu W.-Y., Simonne A., Lu J., Marshall M.R. Antioxidant, Antibacterial, and Antibiofilm Properties of Polyphenols from Muscadine Grape (Vitis rotundifolia Michx.) Pomace against Selected Foodborne Pathogens. J. Agric. Food Chem. 2014;62:6640–6649. doi: 10.1021/jf501073q. PubMed DOI

Yim N., Ha D.T., Trung T.N., Kim J.P., Lee S., Na M., Jung H., Kim H.S., Kim Y.H., Bae K. The antimicrobial activity of compounds from the leaf and stem of Vitis amurensis against two oral pathogens. Bioorganic Med. Chem. Lett. 2010;20:1165–1168. doi: 10.1016/j.bmcl.2009.12.020. PubMed DOI

Gunawardena Y.P., Sotheeswaran S., Sultanbawa M.S., Surendrakumar S., Bladon P. Another antibacterial polyphenol, copalliferol B, from Vateria copallifera (dipterocarpaceae) Phytochemistry. 1986;25:1498–1500. doi: 10.1016/S0031-9422(00)81323-0. DOI

Weber K., Schulz B., Ruhnke M. Resveratrol and its antifungal activity against Candida species. Mycoses. 2010;54:30–33. doi: 10.1111/j.1439-0507.2009.01763.x. PubMed DOI

Rhimi W., Ben Salem I., Immediato D., Saidi M., Boulila A., Cafarchia C. Chemical Composition, Antibacterial and Antifungal Activities of Crude Dittrichia viscosa (L.) Greuter Leaf Extracts. Molecules. 2017;22:942. doi: 10.3390/molecules22070942. PubMed DOI PMC

Alejo-Armijo A., Glibota N., Frías M.P., Altarejos J., Galvez A., Ortega-Morente E., Salido S. Antimicrobial and antibiofilm activities of procyanidins extracted from laurel wood against a selection of foodborne microorganisms. Int. J. Food Sci. Technol. 2017;52:679–686. doi: 10.1111/ijfs.13321. DOI

Rakib M., Ansari V.A., Arif M., Ahmad A. A review of phytochemical and biological studies on Cassia obtusifolia linn. In folklore medicine of Eastern Uttar Pradesh. World J. Pharm. Res. 2018;7:191–201.

El Darra N., Tannous J., Mouncef P.B., Palge J., Yaghi J., Vorobiev E., Louka N., Maroun R.G. A Comparative Study on Antiradical and Antimicrobial Properties of Red Grapes Extracts Obtained from Different Vitis vinifera Varieties. Food Nutr. Sci. 2012;3:1420–1432. doi: 10.4236/fns.2012.310186. DOI

Baydar N.G., Özkan G., Sagdic O. Total phenolic contents and antibacterial activities of grape (Vitis vinifera L.) extracts. Food Control. 2004;15:335–339. doi: 10.1016/S0956-7135(03)00083-5. DOI

Schnee S., Queiroz E.F., Voinesco F., Marcourt L., Dubuis P.-H., Wolfender J.-L., Gindro K. Vitis vinifera Canes, a New Source of Antifungal Compounds against Plasmopara viticola, Erysiphe necator, and Botrytis cinerea. J. Agric. Food Chem. 2013;61:5459–5467. doi: 10.1021/jf4010252. PubMed DOI

Katalinic V., Mozina S.S., Generalic I., Skroza D., Ljubenkov I., Klančnik A. Phenolic Profile, Antioxidant Capacity, and Antimicrobial Activity of Leaf Extracts from Six Vitis vinifera L. Varieties. Int. J. Food Prop. 2012;16:45–60. doi: 10.1080/10942912.2010.526274. DOI

Imbert C., Rodier M.-H., Daniault G., Jacquemin J.-L. Influence of sub-inhibitory concentrations of conventional antifungals on metabolism of Candida albicans and on its adherence to polystyrene and extracellular matrix proteins. Med. Mycol. J. 2002;40:123–129. doi: 10.1080/mmy.40.2.123.129. PubMed DOI

Abreu A.C., Tavares R.R., Borges A., Mergulhão F., Simões M. Current and emergent strategies for disinfection of hospital environments. J. Antimicrob. Chemother. 2013;68:2718–2732. doi: 10.1093/jac/dkt281. PubMed DOI PMC

Dal Mas C., Rossato L., Shimizu T., Oliveira E.B., da Silva Junior P.I., Meis J.F., Colombo A.L., Hayashi M.A.F. Effects of the Natural Peptide Crotamine from a South American Rattlesnake on Candida auris, an Emergent Multidrug Antifungal Resistant Human Pathogen. Biomolecules. 2019;9:205. doi: 10.3390/biom9060205. PubMed DOI PMC

Moreno L.S.S., Junior H.V.N., da Silva A.R., Nascimento F.B.S.A.D., da Silva C.R., Neto J.B.D.A., Cavalcanti B.C., de Moraes M.O., Pinazo A., Pérez L. Arginine-phenylalanine and arginine-tryptophan-based surfactants as new biocompatible antifungal agents and their synergistic effect with Amphotericin B against fluconazole-resistant Candida strains. Colloids Surf. B Biointerfaces. 2021;207:112017. doi: 10.1016/j.colsurfb.2021.112017. PubMed DOI

Vaňková E., Paldrychová M., Kašparová P., Lokočová K., Kodeš Z., Maťátková O., Kolouchová I., Masák J. Natural antioxidant pterostilbene as an effective antibiofilm agent, particularly for gram-positive cocci. World J. Microbiol. Biotechnol. 2020;36:101. doi: 10.1007/s11274-020-02876-5. PubMed DOI

Maksimov A.Y., Balandina S.Y., Topanov P.A., Mashevskaya I.V., Chaudhary S. Organic Antifungal Drugs and Targets of Their Action. Curr. Top. Med. Chem. 2021;21:705–736. doi: 10.2174/1568026621666210108122622. PubMed DOI

Karpiński T., Ożarowski M., Seremak-Mrozikiewicz A., Wolski H., Adamczak A. Plant Preparations and Compounds with Activities against Biofilms Formed by Candida spp. J. Fungi. 2021;7:360. doi: 10.3390/jof7050360. PubMed DOI PMC

Morais S.M., Lima K.S.B., Siqueira S.M.C., Cavalcanti E.S.B., Souza M.S.T., Menezes J.E.S.A., Trevisan M.T.S. Correlac¸ão entre as atividades antiradical, antiacetil- colinesterase e teor de fenóis totais de extratos de plantas medicinais de farmácias vivas. Rev. Bras. Plantas Med. Camp. 2013;15:575–582. doi: 10.1590/S1516-05722013000400014. DOI

Júnior J.T.C., Morais S.M., Vieira L.G., Alexandre J.B., Costa M.S., Morais-Braga M.F.B., Júnior J.E.G.L., Silva M.M.O., Barros L.M., Coutinho H.D.M. Phenolic composition and anticholinesterase, antioxidant, antifungal and antibiotic modulatory activities of Prockia crucis (Salicaceae) extracts collected in the Caatinga biome of Ceará State, Brazil. Eur. J. Integr. Med. 2015;7:547–555. doi: 10.1016/j.eujim.2015.04.006. DOI