SpringerLink
Log in

The Antimicrobial, Anti-Quorum Sensing, and Anti-Biofilm Activities of Ethanolic Propolis Extracts Used as Food Supplements

  • BIOCHEMISTRY
  • Published:
Biology Bulletin Aims and scope Submit manuscript

Abstract

Propolis extracts are the natural bee product most widely used as food supplements. The high antioxidant and antimicrobial properties of propolis derive from its polyphenol compositions. This study investigated the relationship between the phenolic composition and antimicrobial activities of four different prepared ethanolic propolis extracts. The composition of the samples was tested in terms of total phenolic content and total flavonoid content, and their phenolic compositions were analyzed using high performance liquid chromatography-photometric diode array detection. Ferric reducing/antioxidant capacity (FRAP) and 2,2-Diphenyl-1-picrylhydrazyl (DPPH) radical scavenging tests were used as antioxidant assays. The antimicrobial effects of the extracts were tested using bacteriostatic, bactericide, anti-quorum sensing (QS), and anti-biofilm tests. Staphylococcus aureus, Chromobacterium violaceum, Mycobacterium smegmatis, Bacillus cereus, Candida albicans and Candida parapsilosis were used in the agar well diffusion assay. Anti-QS and anti-biofilm activities were tested against Chromobacterium violaceum ATCC31532, Chromobacterium violaceum ATCC 12472, and Pseudomonas aeruginosa PAO1. The phenolic compositions and the antioxidant properties of the extracts varied. All propolis specimens exhibited antimicrobial activity against the strains studied, although that activity varied according to the propolis extract. The findings showed that the high phenolic content of the propolis extracts resulted in high antioxidant and high antimicrobial activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.

REFERENCES

  1. Alavian, S.M., Dolatimehr, F., Sharafi, H., Safi-Abadi, M., Rezaee-Zavareh, M.S., Bayatpour, M.E., … and Mohazzab-Torabi, S., Treatment of HCV infection with direct-acting antiviral agents in patients with HIV/HCV co-infection: a systematic review, Hepatitis Mon., 2018, vol. 18, no. 12, p. 10. https://doi.org/10.5812/hepatmon.82971

    Article  CAS  Google Scholar 

  2. Andrade, M., Benfeito, S., Soares, P., e Silva, D.M., Loureiro, J., Borges, A., … and Simoes, M., Fine-tuning of the hydrophobicity of caffeic acid: studies on the antimicrobial activity against Staphylococcus aureus and Escherichia coli, RSC Adv., 2015, vol. 5, no. 66, pp. 53915–53925. https://doi.org/10.1016/j.foodres.2017.08.066

    Article  CAS  Google Scholar 

  3. Andrade, J.K.S., Denadai, M., de Oliveira, C.S., Nunes, M.L., and Narain, N., Evaluation of bioactive compounds potential and antioxidant activity of brown, green and red propolis from Brazilian northeast region, Food Res. Int., 2017, vol. 101, pp. 129–138. https://doi.org/10.1039/c5ra05840f

    Article  CAS  PubMed  Google Scholar 

  4. Asfour, H.Z., Anti-quorum sensing natural compounds, J. Microsc. Ultrastruct., 2018, vol. 6, no. 1, p. 1. https://doi.org/10.4103/JMAU.JMAU_10_18

    Article  PubMed  PubMed Central  Google Scholar 

  5. Bankova, V., Recent trends and important developments in propolis research, J. Evidence-Based Complementary Altern. Med., 2005, vol. 2, no. 1, pp. 29–32. https://doi.org/10.1093/ecam/neh059

    Article  Google Scholar 

  6. Benzie, I.F. and Strain, J.J., The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay, Anal. Biochem., 1996, vol. 239, no. 1, pp. 70–76. https://doi.org/10.1006/abio.1996.0292

    Article  CAS  PubMed  Google Scholar 

  7. Can, Z., Yildiz, O., Sahin, H., Turumtay, E.A., Silici, S., and Kolayli, S., An investigation of Turkish honeys: their physico-chemical properties, antioxidant capacities and phenolic profiles, Food Chem., 2015, vol. 180, pp. 133–141. https://doi.org/10.1016/j.foodchem.2015.02.024

    Article  CAS  PubMed  Google Scholar 

  8. Drago, L., De Vecchi, E., Nicola, L., and Gismondo, M.R., In vitro evaluation of antibiotics’ combinations for empirical therapy of suspected methicillin resistant Staphylococcus aureus severe respiratory infections, BMC Infect. Dis., 2007, vol. 7, no. 1, pp. 1–7. https://doi.org/10.1186/1471-2334-7-111

    Article  CAS  Google Scholar 

  9. Frost, I., Van Boeckel, T.P., Pires, J., Craig, J., and Laxminarayan, R., Global geographic trends in antimicrobial resistance: the role of international travel, J. Travel Med., 2019, vol. 26, no. 8, p. taz036.

    Article  PubMed  Google Scholar 

  10. Fukumoto, L.R. and Mazza, G., Assessing antioxidant and prooxidant activities of phenolic compounds, J. Agric. Food Chem., 2000, vol. 48, no. 8, pp. 3597–3604. https://doi.org/10.1021/jf000220w

    Article  CAS  PubMed  Google Scholar 

  11. Gemiarto, A.T., Ninyio, N.N., Lee, S.W., Logis, J., Fatima, A., Chan, E.W.C., and Lim, C.S.Y., Isoprenyl caffeate, a major compound in manuka propolis, is a quorum-sensing inhibitor in Chromobacterium violaceum, Antonie Van Leeuwenhoek, 2015, vol. 108, no. 2, pp. 491–504. https://doi.org/10.1007/s10482-015-0503-6

    Article  CAS  PubMed  Google Scholar 

  12. Guler, H.I., Tatar, G., Yildiz, O., Belduz, A.O., and Kolayli, S., Investigation of potential inhibitor properties of ethanolic propolis extracts against ACE-II receptors for COVID-19 treatment by molecular docking study, Arch. Microbiol., 2021, vol. 203, no. 6, pp. 3557–3564. https://doi.org/10.1007/s00203-021-02351-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Guo, C., Yang, J., Wei, J., Li, Y., Xu, J., and Jiang, Y., Antioxidant activities of peel, pulp and seed fractions of common fruits as determined by FRAP assay, Nutr. Res., 2003, vol. 23, no. 12, pp. 1719–1726. https://doi.org/10.1016/j.nutres.2003.08.005

    Article  CAS  Google Scholar 

  14. Kahlmeter, G., Brown, D.F.J., Goldstein, F.W., MacGowan, A.P., Mouton, J.W., Odenholt, I., … and Stetsiouk, O., European Committee on Antimicrobial Susceptibility Testing (EUCAST) technical notes on antimicrobial susceptibility testing, Clin. Microbiol. Infect., 2006, vol. 12, no. 6, pp. 501–503. https://doi.org/10.1111/j.1469-0691.2006.01454.x

    Article  CAS  PubMed  Google Scholar 

  15. Kara, Y., Can, Z., and Kolaylı, S., What should be the ideal solvent percentage and solvent-propolis ratio in the preparation of ethanolic propolis extract?, Food Anal. Methods, 2022a, vol. 15, no. 6, pp. 1707–1719. https://doi.org/10.1007/s12161-022-02244-z

    Article  Google Scholar 

  16. Kara, Y., Can, Z., and Kolaylı, S., Applicability of phenolic profile analysis method developed with RP-HPLC-PDA to some bee product, Braz. Arch. Biol. Technol., 2022b, vol. 65. https://doi.org/10.1590/1678-4324-2022210384

  17. Khan, F., Bamunuarachchi, N.I., Tabassum, N., and Kim, Y.M., Caffeic acid and its derivatives: antimicrobial drugs toward microbial pathogens, J. Agric. Food Chem., 2021, vol. 69, no. 10, pp. 2979–3004. https://doi.org/10.1021/acs.jafc.0c07579

    Article  CAS  PubMed  Google Scholar 

  18. Kurek-Górecka, A., Keskin, Ş., Bobis, O., Felitti, R., Górecki, M., Otręba, M., … and Rzepecka-Stojko, A., Comparison of the antioxidant activity of propolis samples from different geographical regions, Plants, 2022, vol. 11, no. 9, p. 1203. https://doi.org/10.3390/plants11091203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Lima, V.N., Oliveira-Tintino, C.D., Santos, E.S., Morais, L.P., Tintino, S.R., Freitas, T.S., … and Coutinho, H.D., Antimicrobial and enhancement of the antibiotic activity by phenolic compounds: gallic acid, caffeic acid and pyrogallol, Microb. Pathog., 2016, vol. 99, pp. 56–61. https://doi.org/10.1016/j.micpath.2016.08.004

    Article  CAS  PubMed  Google Scholar 

  20. McLean, R.J., Pierson L.S. III, and Fuqua, C., A simple screening protocol for the identification of quorum signal antagonists, J. Microbiol. Methods, 2004, vol. 58, no. 3, pp. 351–360. https://doi.org/10.1016/j.mimet.2004.04.016

    Article  CAS  PubMed  Google Scholar 

  21. Menezes da Silveira, C.C., Luz, D.A., da Silva, C.C., Prediger, R.D., Martins, M.D., Martins, M.A., … and Maia, C.S., Propolis: a useful agent on psychiatric and neurological disorders? A focus on CAPE and pinocembrin components, Med. Res. Rev., 2021, vol. 41, no. 2, pp. 1195–1215. https://doi.org/10.1002/med.21757

    Article  PubMed  Google Scholar 

  22. Meyuhas, S., Assali, M., Huleihil, M., and Huleihel, M., Antimicrobial activities of caffeic acid phenethyl ester, J. Mol. Biochem., 2015, vol. 4, no. 2.

  23. Molyneux, P., The use of the stable free radical diphenylpicrylhydrazyl (DPPH) for estimating antioxidant activity, Songklanakarin J. Sci. Technol., 2004, vol. 26, no. 2, pp. 211–219.

    CAS  Google Scholar 

  24. Mulani, M.S., Kamble, E.E., Kumkar, S.N., Tawre, M.S., and Pardesi, K.R., Emerging strategies to combat ESKAPE pathogens in the era of antimicrobial resistance: a review, Front. Microbiol., 2019, vol. 10, p. 539. https://doi.org/10.3389/fmicb.2019.00539

    Article  PubMed  PubMed Central  Google Scholar 

  25. Panche, A.N., Diwan, A.D., and Chandra, S.R., Flavonoids: an overview, J. Nutr. Sci., 2016, vol. 5. https://doi.org/10.1017/jns.2016.41

  26. Pleeging, C.C., Coenye, T., Mossialos, D., De Rooster, H., Chrysostomou, D., Wagener, F.A., and Cremers, N.A., Synergistic antimicrobial activity of supplemented medical-grade honey against Pseudomonas aeruginosa biofilm formation and eradication, Antibiotics, 2020, vol. 9, no. 12, p. 866. https://doi.org/10.3390/antibiotics9120866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Pobiega, K., Kraśniewska, K., and Gniewosz, M., Application of propolis in antimicrobial and antioxidative protection of food quality—a review, Trends Food Sci. Technol., 2019, vol. 83, pp. 53–62. https://doi.org/10.1016/j.tifs.2018.11.007

    Article  CAS  Google Scholar 

  28. Romero-Calle, D., Guimarães Benevides, R., Góes-Neto, A., and Billington, C., Bacteriophages as alternatives to antibiotics in clinical care, Antibiotics, 2019, vol. 8, no. 3, p. 138. https://doi.org/10.3390/antibiotics8030138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Savka, M.A., Dailey, L., Popova, M., Mihaylova, R., Merritt, B., Masek, M., … and Bankova, V., Chemical composition and disruption of quorum sensing signaling in geographically diverse United States propolis, Evidence-Based Complementary Altern. Med., 2015. https://doi.org/10.1155/2015/472593

  30. Scazzocchio, F., D’auria, F.D., Alessandrini, D., and Pantanella, F., Multifactorial aspects of antimicrobial activity of propolis, Microbiol. Res., 2006, vol. 161, no. 4, pp. 327–333. https://doi.org/10.1016/j.micres.2005.12.003

    Article  CAS  PubMed  Google Scholar 

  31. Slinkard, K. and Singleton, V.L., Total phenol analysis: automation and comparison with manual methods, Am. J. Enol. Viticult., 1977, vol. 28, no. 1, pp. 49–55.

    Article  CAS  Google Scholar 

  32. Snoussi, M., Noumi, E., Punchappady-Devasya, R., Trabelsi, N., Kanekar, S., Nazzaro, F., … and Al-Sieni, A., Antioxidant properties and anti-quorum sensing potential of Carum copticum essential oil and phenolics against Chromobacterium violaceum, J. Food Sci. Technol., 2018, vol. 55, no. 8, pp. 2824–2832. https://doi.org/10.1007/s13197-018-3219-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Stojković, D., Petrović, J., Soković, M., Glamočlija, J., Kukić-Marković, J., and Petrović, S. In situ antioxidant and antimicrobial activities of naturally occurring caffeic acid, p-coumaric acid and rutin, using food systems, J. Sci. Food Agric., 2013, vol. 93, no. 13, pp. 3205–3208. https://doi.org/10.1002/jsfa.6156

    Article  CAS  PubMed  Google Scholar 

  34. Tamfu, A.N., Ceylan, O., Cârâc, G., Talla, E., and Dinica, R.M., Antibiofilm and anti-quorum sensing potential of cycloartane-type triterpene acids from cameroonian grassland propolis: phenolic profile and antioxidant activity of crude extract, Molecules, 2022, vol. 27, no. 15, p. 4872. https://doi.org/10.3390/molecules27154872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Tosi, E.A., Ciappini, M.C., Cazzolli, A.F., and Tapiz, L.M., Physicochemical characteristics of propolis collected in Santa Fe (Argentine), APIACTA, 2006, vol. 41, pp. 110–120.

    Google Scholar 

  36. Truchado, P., Gil-Izquierdo, A., Tomas-Barberan, F., and Allende, A., Inhibition by chestnut honey of N-Acyl-L-homoserine lactones and biofilm formation in Erwinia carotovora, Yersinia enterocolitica, and Aeromonas hydrophila, J. Agric. Food Chem., 2009, vol. 57, no. 23, pp. 11186–11193. https://doi.org/10.1021/jf9029139

    Article  CAS  PubMed  Google Scholar 

  37. Turnidge, J.D., Jorgensen, J.H., Murray, P.R., and Baron, E.J., Antimicrobial susceptibility testing: general considerations, in Manual of Clinical Microbiology, Washington, DC: ASM Press, 1999, 7th ed., pp. 1469–1473.

    Google Scholar 

  38. Ureyen Esertaş, Ü.Z., Kara, Y., Kiliç, A.O., and Kolayli, S., A comparative study of antimicrobial, anti-quorum sensing, anti-biofilm, anti-swarming, and antioxidant activities in flower extracts of pecan (Carya illinoinensis) and chestnut (Castanea sativa), Arch. Microbiol., 2022, vol. 204, no. 9, pp. 1–7. https://doi.org/10.1007/s00203-022-03172-6

    Article  CAS  Google Scholar 

  39. Vasavi, H.S., Arun, A.B., and Rekha, P.D., Anti-quorum sensing activity of Psidium guajava L. flavonoids against Chromobacterium violaceum and Pseudomonas aeruginosa PAO1, Microbiol. Immunol., 2014, vol. 58, no. 5, pp. 286–293.https://doi.org/10.1111/1348-0421.12150

    Article  CAS  PubMed  Google Scholar 

  40. Woods, G.L., Grace Lin, S.Y., and Desmond, E.P., Susceptibility test methods: mycobacteria, nocardia, and other actinomycetes, in Manual of Clinical Microbiology, 2011, pp. 1215–1238. https://doi.org/10.1128/9781555816728.ch73

Download references

ACKNOWLEDGMENTS

We are most grateful to SBS Bilimsel Bio Çözümler San. ve Tic. A.Ş. (Bee&You, Bee’O Propolis) for providing all the propolis samples used in the study.

Author information

Authors and Affiliations

  1. Department of Chemistry, Faculty of Science, Karadeniz Technical University, Trabzon, Türkiye

    Sevgi Kolaylı & Yakup Kara

  2. Department of Microbiology, Faculty of Medicine, Karadeniz Technical University, Trabzon, Türkiye

    Ulku Zeynep Ureyen Esertas

Authors
  1. Sevgi Kolaylı
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ulku Zeynep Ureyen Esertas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yakup Kara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sevgi Kolaylı.

Ethics declarations

The authors declare that they have no conflicts of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sevgi Kolaylı, Ureyen Esertas, U.Z. & Kara, Y. The Antimicrobial, Anti-Quorum Sensing, and Anti-Biofilm Activities of Ethanolic Propolis Extracts Used as Food Supplements. Biol Bull Russ Acad Sci 49 (Suppl 3), S21–S30 (2022). https://doi.org/10.1134/S1062359022150134

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062359022150134

Keywords:

Search

Navigation