Activity of Selected Essential Oils against Candida spp. strains. Evaluation of New Aspects of their Specific Pharmacological Properties, with Special Reference to Lemon Balm


The aim was to investigate the antifungal effectiveness and some of pharmacological properties of essential oils (EOs), which had not yet been thoroughly studied in the planned scope. We first evaluated MIC/MFC of sixteen EOs against C. albicans ATCC 10231. Then, five most active EOs were tested, using 50 clinical Candida spp. strains and additional reference C. albicans ATCC 90028 strain. The time-kill curve, carryover, post-antifungal effects (PAFE), mutant prevention concentrations, the susceptibility of reference strains to the cell wall disrupting agents and tolerance to oxidative stress, were evaluated. For these detailed studies, we chose the following four essential oils. Clove oil, Geranium oil, Lemon balm and Citronella oil, with MICs of 0.097% (v/v), resulted concentration- and time-dependent killing and may be therapeutically safe, because they do not generate resistance. The best one was Lemon balm, which caused most extended PAFE, significantly reduced tolerance to oxidative stress and increased susceptibility to Calcofluor White, Congo Red and SDS. Phytochemical analysis of these four EOs has been performed and compared; looking for the reason that Lemon balm was the best.

Share and Cite:

A. Budzyńska, B. Sadowska, G. Lipowczan, A. Maciąg, D. Kalemba and B. Różalska, "Activity of Selected Essential Oils against Candida spp. strains. Evaluation of New Aspects of their Specific Pharmacological Properties, with Special Reference to Lemon Balm," Advances in Microbiology, Vol. 3 No. 4, 2013, pp. 317-325. doi: 10.4236/aim.2013.34045.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] S. A. Messer, R. N. Jones and T. R. Fritsche, “International Surveillance of Candida spp. and Aspergillus spp. Report from the SENTRY Antimicrobial Surveillance Program,” Journal of Clinical Microbiology, Vol. 44, No. 5, 2006, 2003, pp. 1782-1787. doi:10.1128/JCM.44.5.1782-1787.2006
[2] E. Mlinaric-Missoni, S. Kalenic, M. Vukelic, D. De Syo, M. Belicza and V. Vazic-Babic, “Candida Infections of Diabetic Foot Ulcers,” Diabetologia Croatica, Vol. 34, No 1, 2005, pp. 29-35.
[3] R. Rajeshkumar and M. Sundararaman, “Emergence of Candida spp. and Exploration of Natural Bioactive Molecules for AntiCandidal Therapy—Status Quo,” Mycoses, Vol. 55, No. 3, 2012, pp. e60-e73. doi:10.1111/j.1439-0507.2011.02156.x
[4] F. Silva, S. Ferreira, A. Duarte, D. I. Mendonca and F. C. Domingues, “Antifungal Activity of Coriandrum sativum Essential Oil, Its Mode of Action against Candida Species and Potential Synergism with Amphotericin B,” Phytomedicine, Vol. 19, No. 1, 2011, pp. 42-47. doi:10.1016/j.phymed.2011.06.033
[5] F. Solórzano-Santos and M. G. Miranda-Novales, “Essential Oils from Aromatic Herbs as Antimicrobial Agents,” Current Opinion in Biotechnology, Vol. 23, No. 2, 2012, pp. 136-141. doi:10.1016/j.copbio.2011.08.005
[6] Mikolajewska, S. Schwartz and M. Ruhnke, “Antifungal Treatment Strategies in Patients with Haematological Diseases and Cancer: From Prophylaxis to Empirical, Pre-Emptive and Targeted Therapy,” Mycoses, Vol. 55, No. 1, 2012, pp. 2-16. doi:10.1111/j.1439-0507.2010.01961.x
[7] P. Pozzatti, E. S. Loreto, P. G. M. Lopes, M. L. Athayde, J. M. Santurio and S. H. Alves, “Comparison of the Susceptibilities of Clinical Isolates of Candida albicans and Candida dubliniensis to Essential Oils,” Mycoses, Vol. 53, No. 1, 2010, pp. 12-15. doi:10.1111/j.1439-0507.2008.01643.x
[8] J. Reichling, P. Schnitzler, U. Suschke and R. Saller, “Essential Oils of Aromatic Plants with Antibacterial, Antifungal, Antiviral, and Cytotoxic Properties—An Overview,” Forschende Komplementarmedizin, Vol. 16, No. 2, 2009, pp. 79-90. doi:10.1159/000207196
[9] A. Rosato, C. Vitali, D. Gallo, L. Balenzano, R. Mallamaci, “The Inhibition of Candida Species by Selected Essential Oils and Their Synergism with Amphotericin B,” Phytomedicine, Vol. 15, No. 8, 2008, pp. 635-638. doi:10.1016/j.phymed.2008.05.001
[10] A. Budzyńska, M. Wieckowska-Szakiel, D. Kalemba, B. Sadowska and B. Rózalska, “The Optimization of Methods Utilized for Testing the Antibacterial Activity of Essential Oils,” Medycyna Doswiadczalna i Mikrobiologia, Vol. 61, No. 3, 2009, pp. 281-287 (in polish).
[11] A. Budzyńska, M. Wieckowska-Szakiel, B. Sadowska, D. Kalemba and B. Rózalska, “Antibiofilm Activity of Selected Plant Essential Oils and Their Major Components,” Polish Journal of Microbiology, Vol. 60, No. 1, 2011, pp. 35-41.
[12] M. J. Abad, M. Ansuategui and P. Bermejo, “Active Antifungal Substances from Natural Sources,” Arkivoc: Archive for Organic Chemistry, Vol. vii, No. 7, 2007, pp. 116-145.
[13] F. Bakkali, S. Averbeck, D. Averbeck and M. Idaomarb, “Biological Effects of Essential Oils—A Review,” Food and Chemical Toxicology, Vol. 46, No. 2, 2008, pp. 446-475. doi:10.1016/j.fct.2007.09.106
[14] A. N. Devkatte, G. B. Zore and S. M. Karuppayil, “Potential of Plant Oils as Inhibitors of Candida albicans Growth,” FEMS Yeast Research, Vol. 5, No. 9, 2005, pp. 867-873. doi:10.1016/j.femsyr.2005.02.003
[15] R. Khosravi, H. Shokri, S. Kermani, M. Dakhili, M. Madani and S. Parsa, “Antifungal Properties of Artemisia sieberi and Origanum vulgare Essential Oils against Candida glabrata Isolates Obtained from Patients with Vulvovaginal Candidiasis,” Journal of Medical Mycology, Vol. 21, No. 2, 2011, pp. 93-99. doi:10.1016/j.mycmed.2011.01.006
[16] K. Credito, K. Kosowska-Shick and P. C. Appelbaum, “Mutant Prevention Concentration (MPC) of Four Carbapenems against Gram-Negative Rods,” Antimicrobial Agents and Chemotherapy, Vol. 54, No. 6, 2010, pp. 2692-2695. doi:10.1128/AAC.00033-10
[17] K. Drlica and M. Malik, “Fluoroquinolones: Action and Resistance,” Current Topics in Medicinal Chemistry, Vol. 3, No. 3, 2002, pp. 249-282. doi:10.2174/1568026033452537
[18] M. E. Klepser, E. J. Ernst, R. E. Lewis, M. E. Ernst and M. A. Pfaller, “Influence of Test Conditions on Antifungal Time-Kill Curve Results: Proposal for Standardized Methods,” Antimicrobial Agents and Chemotherapy, Vol. 42, No. 5, 1998, pp. 1207-1212.
[19] M. Hancianu, A. C. Aprotosoaie, E. Gille, A. Poiata, C. Tuchilus, A. Spac and U. Stanescu, “Chemical Composition and in Vitro Antimicrobial Activity of Essential Oil of Melissa officinalis L. from Romania,” Revista medicochirurgicala a Societatti de Medici si Naturalisti din Iasi, Vol. 112, No. 3, 2008, pp. 843-847.
[20] N. Mimica-Dukic, B. Bozin, M. Sokovic and N. Simin, “Antimicrobial and Antioxidant Activities of Melissa officinalis L. (Lamiaceae) Essential Oil,” Journal of Agricultural and Food Chemistry, Vol. 52, No. 9, 2004, pp. 2485-2489. doi:10.1021/jf030698a
[21] A. K. Tyagi and A. Malik, “Liquid and Vapour-Phase Antifungal Activities of Selected Essential Oils against Candida albicans: Microscopic Observations and Chemical Characterization of Cymbopogon citratus,” BMC Complementary and Alternative Medicine, Vol. 10, 2010, p. 65. doi:10.1155/2012/692625
[22] A. E. Edris, “Pharmaceutical and Therapeutic Potentials of Essential Oils and their Individual Volatile Constituents: A Review,” Phytotherapy Research, Vol. 21, No. 4, 2007, pp. 308-323. doi:10.1002/ptr.2072
[23] D. Kalemba and A. Kunicka, “ Antibacterial and Antifungal Properties of Essential Oils,” Current Medicinal Chemistry, Vol. 10, No. 10, 2003, pp. 813-829. doi:10.2174/0929867033457719
[24] J. Kim, M.R Marschal, C. Wei, “Antibacterial Activity of Some Essential Oil Components against Five Foodborne Pathogens,” Journal of Agricultural Chemistry, Vol. 43, No. 11, 1995, pp. 2839-2845. doi:10.1021/jf00059a013
[25] R. Hashash, S. Younes, W. Bahnan, J. El Koussa, K. Maalouf, H. I. Dimassi and R. A. Khalaf, “Characterisation of Pga1, a Putative Candida albicans Cell Wall Protein Necessary for Proper Adhesion and Biofilm Formation,” Mycoses, Vol. 54, No. 6, 2011, pp. 491-500. doi:10.1111/j.1439-0507.2010.01883.x
[26] R. K. Shields, M. H. Nguyen, E. Press and C. J. Clancy, “Five-Minute Exposure to Caspofungin Results in Prolonged Post-Antifungal Effects and Eliminates the Paradoxical Growth of Candida albicans,” Antimicrobial Agents and Chemotherapy, Vol. 55, No.7, 2011, pp. 3598-3602. doi:10.1128/AAC.00095-11
[27] T. Missall, J. K. Lodge and J. E. McEwen, “Mechanisms of Resistance to Oxidative and Nitrosative Stress. Implications for Fungal Survival in Mammalian Hosts,” Eukaryotic Cell, Vol. 3, No. 4, 2004, pp. 835-846. doi:10.1128/EC.3.4.835-846.2004
[28] A. Bink, D. Vandenbosch, T. Coenye, H. Nelis, B. P. A. Cammue and K. Thevissen, “Superoxide Dismutases Are Involved in Candida albicans Biofilm Persistence against Miconazole,” Antimicrobial Agents and Chemotherapy, Vol. 55, No. 9, 2011, pp. 4033-4037. doi:10.1128/AAC.00280-11
[29] A. Enjalbert, D. M. MacCallum, F. C. Odds and A. J. P. Brown, “Niche-Specific Activation of the Oxidative Stress Response by the Pathogenic Fungus Candida albicans,” Infection and Immunity, Vol. 75, No. 5, 2007, pp. 2143-2151. doi:10.1128/IAI.01680-06
[30] P. H. Warnke, E. Sherry, P. A. J. Russo, Y. Acil, J. Wiltfang, S. Sivananthan, J. C. Roldàn, S. Schubert, J. P. Bredee and I. N. Springer, “Antibacterial Essential Oils in Malodorous Cancer Patients: Clinical Observations in 30 Patients,” Phytomedicine, Vol. 13, No. 7, 2006, pp. 463-467. doi:10.1016/j.phymed.2005.09.012
[31] S. Hampton, “Malodorous Fungating Wounds: How Dressings Alleviate Symptoms,” British Journal of Community Nursing, Vol. 13, No. 6, 2008, pp. S34-S36.
[32] D. Mercier and A. Knevitt, “Using Topical Aromatherapy for the Management of Fungating Wounds in a Palliative Care Unit,” Journal of Wound Care, Vol. 14, No. 10, 2005, pp. 497-498.
[33] E. Sherry, H. Boeck and P. H. Warnke, “Topical Application of a New Formulation of Eucalyptus Oil Phytochemical Clears Methicillin-Resistant Staphylococcus aureus Infection,” American Journal of Infection Control, Vol. 29, No. 5, 2001, pp. 346. doi:10.1067/mic.2001.117403

Copyright © 2024 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.