Abstract
Candida spp. can form biofilms on mucosal surfaces and epithelial cells as well as on devices implanted in the body such as catheters and dentures, which are thought to underlie the most recalcitrant infections. It was aimed to show antifungal and antibiofilm activities of oregano oil (Origanum onites). The antifungal activities of some essential oils were investigated against C. spp. and among them, oregano oil was found to be the most effective oil and further biofilm studies were conducted with it. Oregano oil inhibited biofilm adhesion and formation of C. spp. and mature biofilms and also displayed the ability to reduce biofilm formation when they were allowed to form on surfaces previously coated with oil (up to 50% inhibition rates). In addition, oregano oil was found to be effective against dual biofilms of Candida albicans + Staphyloccocus aureus at different concentrations. This study suggests that O. onites essential oil has useful antibiofilm effects against C. spp. The inhibitory effects of O. onites essential oil, against C. spp., were demonstrated for the first time. It also had antifungal effect on biofilm formation and established biofilm even at MIC level.
Acknowledgement
The authors are grateful to MSc. Merve ATAMAN, for providing essential oils.
-
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
-
Research funding: This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
-
Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
1. Lohse, MB, Gulati, M, Craik, CS, Johnson, AD, Nobile, CJ. Combination of antifungal drugs and protease inhibitors prevent Candida albicans biofilm formation and disrupt mature biofilms. Front Microbiol 2020;11:1027.10.3389/fmicb.2020.01027Search in Google Scholar
2. Palmeira-de-Oliveira, A, Gaspar, C, Palmeira-de-Oliveira, R, Silva-Dias, A, Salgueiro, L, Cavaleiro, C, et al.. The anti-Candida activity of Thymbra capitata essential oil: effect upon pre-formed biofilm. J Ethnopharmacol 2012;140:379–83. https://doi.org/10.1016/j.jep.2012.01.029.Search in Google Scholar
3. Mah, TF, O’Toole, GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 2001;9:34–9. https://doi.org/10.1016/s0966-842x(00)01913-2.Search in Google Scholar
4. Stewart, PS, Costerton, JW. Antibiotic resistance of bacteria in biofilms. Lancet 2001;358:135–8. https://doi.org/10.1016/s0140-6736(01)05321-1.Search in Google Scholar
5. Dongari-Bagtzoglou, A, Kashleva, H, Dwivedi, P, Diaz, P, Vasilakos, J. Characterization of mucosal Candida albicans biofilms. PloS One 2009;4:e7967. https://doi.org/10.1371/journal.pone.0007967.Search in Google Scholar PubMed PubMed Central
6. Harriott, MM, Lilly, EA, Rodriguez, TE, Fidel, PL, Noverr, MC. Candida albicans forms biofilms on the vaginal mucosa. Microbiology (Read) 2010;156:3635–44. https://doi.org/10.1099/mic.0.039354-0.Search in Google Scholar PubMed PubMed Central
7. Hirota, K, Yumoto, H, Sapaar, B, Matsuo, T, Ichikawa, T, Miyake, Y. Pathogenic factors in Candida biofilm-related infectious diseases. J Appl Microbiol 2017;122:321–30. https://doi.org/10.1111/jam.13330.Search in Google Scholar PubMed
8. Newman, DJ, Cragg, GM. Natural products as sources of new drugs over the 30 years from 1981 to 2010. J Nat Prod 2012;75:311–35. https://doi.org/10.1021/np200906s.Search in Google Scholar PubMed PubMed Central
9. Kavanaugh, NL, Ribbeck, K. Selected antimicrobial essential oils eradicate Pseudomonas spp. and Staphylococcus aureus biofilms. Appl Environ Microbiol 2012;78:4057–61. https://doi.org/10.1128/AEM.07499-11.Search in Google Scholar PubMed PubMed Central
10. Kang, J, Jin, W, Wang, J, Sun, Y, Wu, X, Liu, L. Antibacterial and anti-biofilm activities of peppermint essential oil against Staphylococcus aureus. Lebensm Wiss Technol 2019;101:639–45.10.1016/j.lwt.2018.11.093Search in Google Scholar
11. Lou, Z, Chen, J, Yu, F, Wang, H, Kou, X, Ma, C, et al.. The antioxidant, antibacterial, antibiofilm activity of essential oil from Citrus medica L. var. sarcodactylis and its nanoemulsion. Lebensm Wiss Technol 2017;80:371–7.10.1016/j.lwt.2017.02.037Search in Google Scholar
12. Peixoto, LR, Rosalen, PL, Ferreira, GL, Freires, IA, de Carvalho, FG, Castellano, LR, et al.. Antifungal activity, mode of action and anti-biofilm effects of Laurus nobilis Linnaeus essential oil against Candida spp. Arch Oral Biol 2017;73:179–85. https://doi.org/10.1016/j.archoralbio.2016.10.013.Search in Google Scholar PubMed
13. dos-Santos-Rodrigues, JB, de-Carvalho, RJ, de-Souza, NT, de-Sousa-Oliveira, K, Franco, OL, Schaffner, D, et al.. Effects of oregano essential oil and carvacrol on biofilms of Staphylococcus aureus from food-contact surfaces. Food Contr 2017;73:1237–46.10.1016/j.foodcont.2016.10.043Search in Google Scholar
14. Rodriguez-Garcia, I, Silva-Espinoza, BA, Ortega-Ramirez, LA, Leyva, JM, Siddiqui, MW, Cruz-Valenzuela, MR, et al.. Oregano essential oil as an antimicrobial and antioxidant additive in food products. Crit Rev Food Sci Nutr 2016;56:1717–27. https://doi.org/10.1080/10408398.2013.800832.Search in Google Scholar PubMed
15. Spyridopoulou, K, Fitsiou, E, Bouloukosta, E, Tiptiri-Kourpeti, A, Vamvakias, M, Oreopoulou, A, et al.. Extraction, chemical composition, and anticancer potential of Origanum onites L. essential oil. Molecules 2019;24:2612. https://doi.org/10.3390/molecules24142612.Search in Google Scholar PubMed PubMed Central
16. Ortega-Ramirez, LA, Rodriguez-Garcia, I, Silva-Espinoza, BA, Ayala-Zavala, JF. Oregano (Origanum spp.) oils. In: Preedy, VR, editor. Essential oils in food preservation, flavor and safety. San Diego, USA: Academic Press; 2016.10.1016/B978-0-12-416641-7.00071-7Search in Google Scholar
17. Clinical and Laboratory Standards Institute (CLSI). Method for antifungal disk diffusion susceptibility testing of yeasts; approved guideline—second edition M44-A2. Wayne, PA: CLSI; 2009.Search in Google Scholar
18. Clinical and Laboratory Standards Institute (CLSI). Reference method for broth dilution antifungal susceptibility testing of yeasts. Approved standard-third edition. Document M27-A3. Wayne, PA: CLSI; 2008.Search in Google Scholar
19. Ramage, G, Vande Walle, K, Wickes, BL, López-Ribot, JL. Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother 2001;45:2475–9. https://doi.org/10.1128/aac.45.9.2475-2479.2001.Search in Google Scholar PubMed PubMed Central
20. Hacioglu, M, Haciosmanoglu, E, Birteksoz-Tan, AS, Bozkurt-Guzel, C, Savage, PB. Effects of ceragenins and conventional antimicrobials on Candida albicans and Staphylococcus aureus mono and multispecies biofilms. Diagn Microbiol Infect Dis 2019;95:114863. https://doi.org/10.1016/j.diagmicrobio.2019.06.014.Search in Google Scholar PubMed
21. Bozkurt-Guzel, C, Hacioglu, M, Savage, PB. Investigation of the in vitro antifungal and antibiofilm activities of ceragenins CSA-8, CSA-13, CSA-44, CSA-131, and CSA-138 against Candida species. Diagn Microbiol Infect Dis 2018;91:324–30. https://doi.org/10.1016/j.diagmicrobio.2018.03.014.Search in Google Scholar PubMed
22. Hacioglu, M, Oyardi, O, Bozkurt-Guzel, C, Savage, PB. Antibiofilm activities of ceragenins and antimicrobial peptides against fungal-bacterial mono and multispecies biofilms. J Antibiot 2020;73:455–62. https://doi.org/10.1038/s41429-020-0299-0.Search in Google Scholar PubMed
23. Peters, BM, Ward, RM, Rane, HS, Lee, SA, Noverr, MC. Efficacy of ethanol against Candida albicans and Staphylococcus aureus polymicrobial biofilms. Antimicrob Agents Chemother 2013;57:74–82. https://doi.org/10.1128/AAC.01599-12.Search in Google Scholar PubMed PubMed Central
24. Bakkali, F, Averbeck, S, Averbeck, D, Idaomar, M. Biological effects of essential oils--a review. Food Chem Toxicol 2008;46:446–75. https://doi.org/10.1016/j.fct.2007.09.106.Search in Google Scholar PubMed
25. Bona, E, Cantamessa, S, Pavan, M, Novello, G, Massa, N, Rocchetti, A, et al.. Sensitivity of Candida albicans to essential oils: are they an alternative to antifungal agents? J Appl Microbiol 2016;121:1530–45. https://doi.org/10.1111/jam.13282.Search in Google Scholar PubMed
26. Ebani, VV, Nardoni, S, Bertelloni, F, Pistelli, L, Mancianti, F. Antimicrobial activity of five essential oils against bacteria and fungi responsible for urinary tract infections. Molecules 2018;23:1668. https://doi.org/10.3390/molecules23071668.Search in Google Scholar PubMed PubMed Central
27. Hammer, KA, Carson, CF, Riley, TV. In-vitro activity of essential oils, in particular Melaleuca alternifolia (tea tree) oil and tea tree oil products, against Candida spp. J Antimicrob Chemother 1998;42:591–5. https://doi.org/10.1093/jac/42.5.591.Search in Google Scholar PubMed
28. Tepe, B, Cakir, A, Sihoglu Tepe, A. Medicinal uses, phytochemistry, and pharmacology of Origanum onites (L.): a review. Chem Biodivers 2016;13:504–20. https://doi.org/10.1002/cbdv.201500069.Search in Google Scholar PubMed
29. Massa, N, Cantamessa, S, Novello, G, Ranzato, E, Martinotti, S, Pavan, M, et al.. Antifungal activity of essential oils against azole-resistant and azole-susceptible vaginal Candida glabrata strains. Can J Microbiol 2018;64:647–63. https://doi.org/10.1139/cjm-2018-0082.Search in Google Scholar PubMed
30. Cleff, MB, Meinerz, AR, Xavier, M, Schuch, LF, Schuch, LF, Araújo Meireles, MC, et al.. In vitro activity of Origanum vulgare essential oil against Candida species. Braz J Microbiol 2010;41:116–23. https://doi.org/10.1590/S1517-838220100001000018.Search in Google Scholar PubMed PubMed Central
31. Pozzatti, P, Loreto, ÉS, Nunes-Mario, DA, Rossato, L, Santurio, JM, Alves, SH. Activities of essential oils in the inhibition of Candida albicans and Candida dubliniensis germ tube formation. J Mycol Med 2010;20:185–9.10.1016/j.mycmed.2010.06.003Search in Google Scholar
32. Ozdikmenli, S, Demirel Zorba, NN. Evaluation of usage of essential oils instead of spices in meat ball formulation for controlling Salmonella spp. Food Sci Technol Int 2016;22:93–101. https://doi.org/10.1177/1082013215571118.Search in Google Scholar PubMed
33. Kaskatepe, B, Yildiz, SS, Kiymaci, ME, Yazgan, AN, Cesur, S, Erdem, SA. Chemical composition and antimicrobial activity of the commercial Origanum onites L. oil against nosocomial carbapenem resistant extended spectrum beta lactamase producer Escherichia coli isolates. Acta Biol Hung 2017;68:466–76. https://doi.org/10.1556/018.68.2017.4.11.Search in Google Scholar
34. Altintas, A, Tabanca, N, Tyihák, E, Ott, PG, Móricz, AM, Mincsovics, E, et al.. Characterization of volatile constituents from Origanum onites and their antifungal and antibacterial activity. J AOAC Int 2013;96:1200–8. https://doi.org/10.5740/jaoacint.sgealtintas.Search in Google Scholar
35. Soković, M, Tzakou, O, Pitarokili, D, Couladis, M. Antifungal activities of selected aromatic plants growing wild in Greece. Nahrung 2002;46:317–20.10.1002/1521-3803(20020901)46:5<317::AID-FOOD317>3.0.CO;2-BSearch in Google Scholar
36. Lebeaux, D, Ghigo, JM, Beloin, C. Biofilm-related infections: bridging the gap between clinical management and fundamental aspects of recalcitrance toward antibiotics. Microbiol Mol Biol Rev 2014;78:510–43. https://doi.org/10.1128/MMBR.00013-14.Search in Google Scholar
37. Mutlu Sariguzel, F, Berk, E, Koc, AN, Sav, H, Demir, G. Investigation of the relationship between virulence factors and genotype of Candida spp. isolated from blood cultures. J Infect Dev Ctries 2015;9:857–64. https://doi.org/10.3855/jidc.5359.Search in Google Scholar
38. Ramage, G, Rajendran, R, Sherry, L, Williams, C. Fungal biofilm resistance. Int J Med Microbiol 2012;2012:528521. https://doi.org/10.1155/2012/528521.Search in Google Scholar
39. Tellapragada, C, Eshwara, VK, Johar, R, Shaw, T, Malik, N, Bhat, PV, et al.. Antifungal susceptibility patterns, in vitro production of virulence factors, and evaluation of diagnostic modalities for the speciation of pathogenic Candida from blood stream infections and vulvovaginal candidiasis. J Pathog 2014;2014:142864. https://doi.org/10.1155/2014/142864.Search in Google Scholar
40. Nostro, A, Roccaro, AS, Bisignano, G, Marino, A, Cannatelli, MA, Pizzimenti, FC, et al.. Effects of oregano, carvacrol and thymol on Staphylococcus aureus and Staphylococcus epidermidis biofilms. J Med Microbiol 2007;56:519–23. https://doi.org/10.1099/jmm.0.46804-0.Search in Google Scholar
41. Oral, N, Vatansever, L, Aydin, B, Guven, A, Gulmez, M. Effect of oregano essential oil on biofilms formed by Staphylococci and Escherichia coli. Kafkas Univ Vet Fak Derg 2010;16:23–9.Search in Google Scholar
42. Lu, M, Dai, T, Murray, CK, Wu, MX. Bactericidal property of Oregano oil against multidrug-resistant clinical isolates. Front Microbiol 2018;9:2329. https://doi.org/10.3389/fmicb.2018.02329.Search in Google Scholar
43. Harriott, MM, Noverr, MC. Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother 2009;53:3914–22. https://doi.org/10.1128/AAC.00657-09.Search in Google Scholar
44. Harriott, MM, Shoyinka, AT, Ponniah, MP, Doyon-Reale, N, Vager, D, Vazquez, JA. In vitro antifungal-antibacterial combinations are effective against MRSA in Candida albicans-Staphylococcus aureus polymicrobial biofilms. J Microbiol Exp 2016;3:00090.10.15406/jmen.2016.03.00090Search in Google Scholar
45. Zago, CE, Silva, S, Sanitá, PV, Barbugli, PA, Dias, CM, Lordello, VB, et al.. Dynamics of biofilm formation and the interaction between Candida albicans and methicillin-susceptible (MSSA) and -resistant Staphylococcus aureus (MRSA). PloS One 2015;10:e0123206. https://doi.org/10.1371/journal.pone.0123206.Search in Google Scholar PubMed PubMed Central
46. Knowles, JR, Roller, S, Murray, DB, Naidu, AS. Antimicrobial action of carvacrol at different stages of dual-species biofilm development by Staphylococcus aureus and Salmonella enterica serovar Typhimurium. Appl Environ Microbiol 2005;71:797–803. https://doi.org/10.1128/AEM.71.2.797-803.2005.Search in Google Scholar PubMed PubMed Central
Supplementary material
The online version of this article offers supplementary material (https://doi.org/10.1515/znc-2021-0002).
© 2021 Walter de Gruyter GmbH, Berlin/Boston