Planta Med 2012; 78(15): 1633-1635
DOI: 10.1055/s-0032-1315153
Biological and Pharmacological Activity
Georg Thieme Verlag KG Stuttgart · New York

Positive Interaction of Thyme (Red) Essential Oil with Human Polymorphonuclear Granulocytes in Eradicating Intracellular Candida albicans

Vivian Tullio
1   Department of Public Health and Microbiology, University of Turin, Turin, Italy
Narcisa Mandras
1   Department of Public Health and Microbiology, University of Turin, Turin, Italy
Valeria Allizond
1   Department of Public Health and Microbiology, University of Turin, Turin, Italy
Antonia Nostro
2   Pharmaco-Biological Department, University of Messina, Messina, Italy
Janira Roana
1   Department of Public Health and Microbiology, University of Turin, Turin, Italy
Chiara Merlino
1   Department of Public Health and Microbiology, University of Turin, Turin, Italy
Giuliana Banche
1   Department of Public Health and Microbiology, University of Turin, Turin, Italy
Daniela Scalas
1   Department of Public Health and Microbiology, University of Turin, Turin, Italy
Anna Maria Cuffini
1   Department of Public Health and Microbiology, University of Turin, Turin, Italy
› Author Affiliations
Further Information

Publication History

received 09 May 2012
revised 04 July 2012

accepted 12 July 2012

Publication Date:
07 August 2012 (online)


The essential oils have started to be recognized for their potential antimicrobial role only in recent years. Clinical experience showed that the efficacy of antimicrobial agents depends not only on their direct effect on a given microorganism but also on the functional activity of the host immune system. Since data on the effects of essential oils on the innate immune system are scanty and fragmentary, the aim of this study was to evaluate the influence of thyme (red) essential oil (EO), at subinhibitory/inhibitory concentrations, on intracellular killing activity by human polymorphonuclear granulocytes (PMNs) against Candida albicans. In order to provide a frame of reference for the activity of this EO, its in vitro killing activity in the absence of PMNs was also evaluated.

Results showed that EO at subminimal inhibitory (subMIC)/minimal inhibitory (MIC) concentrations significantly enhanced intracellular killing of C. albicans in comparison with EO-free controls and was comparable to the positive control (fluconazole). In in vitro killing assays without PMNs, we observed progressive growth of the yeast cells in the presence of EO subMIC/MIC concentrations. A positive antifungal interaction with phagocytes could explain why this EO, which appeared to be only fungistatic in time-kill assays, had efficacy in killing yeast cells once incubated with PMNs.

  • References

  • 1 Pina-Vaz C, Gonçalves Rodrigues A, Pinto E, Costa-de-Oliveira S, Tavares C, Salgueiro L, Cavaleiro C, Gonçalves MJ, Martinez-de-Oliveira J. Antifungal activity of Thymus oils and their major compounds. J Eur Acad Dermatol Venereol 2004; 18: 73-78
  • 2 Kalemba D, Kunicka A. Antibacterial and antifungal properties of essential oils. Curr Med Chem 2003; 10: 813-829
  • 3 Tullio V, Nostro A, Mandras N, Dugo P, Banche G, Cannatelli MA, Cuffini AM, Alonzo V, Carlone NA. Antifungal activity of essential oils against filamentous fungi determined by broth microdilution and vapour contact methods. J Appl Microbiol 2007; 102: 1544-1550
  • 4 Vale-Silva LA, Gonçalves MJ, Cavaleiro C, Salgueiro L, Pinto E. Antifungal activity of the essential oil of Thymus x viciosoi against Candida, Cryptococcus, Aspergillus and dermatophyte species. Planta Med 2010; 76: 882-888
  • 5 Abe S, Maruyama N, Hayama K, Ishibashi H, Inoue S, Oshima H, Yamaguchi H. Suppression of tumour necrosis factor-alpha-induced neutrophil adherence responses by essential oils. Mediators Inflamm 2003; 12: 323-328
  • 6 Chao LK, Hua KF, Hsu HY, Cheng SS, Lin IF, Chen CJ, Chen ST, Chang ST. Cinnamaldehyde inhibits pro-inflammatory cytokines secretion from monocytes/macrophages through suppression of intracellular killing. Food Chem Toxicology 2008; 46: 220-231
  • 7 Conrad A, Hansmann C, Engels I, Daschner FD, Frank U. Extract of Pelargonium sidoides (EPs®7630) improves phagocytosis, oxidative burst, and intracellular killing of human peripheral blood phagocytes in vitro . Phytomedicine 2007; 14: 46-51
  • 8 Salem ML. Immunomodulatory and therapeutic properties of the Nigella sativa L. seed. Int Immunopharmacol 2005; 5: 1749-1770
  • 9 Amirghofran Z, Hashemzadeh R, Javidnia K, Golmoghaddam H, Esmaeilbeig AJ. In vitro immunomodulatory effects of extracts from three plants of the Labiatae family and isolation of the active compound(s). J Immunotoxicol 2011; 8: 265-273
  • 10 Tullio V, Cuffini AM, Giacchino F, Mandras N, Roana J, Comune L, Merlino C, Carlone NA. Combined action of fluconazole and PMNs from uremic patients in clearing intracellular Candida albicans . J Chemother 2003; 15: 301-303
  • 11 Tullio V, Cuffini AM, Banche G, Mandras N, Allizond V, Roana J, Giacchino F, Bonello F, Ungheri D, Carlone NA. Role of fosfomycin tromethamine in modulating non-specific defence mechanisms in chronic uremic patients towards ESBL-producing Escherichia coli . Int J Immunopathol Pharmacol 2008; 21: 153-160
  • 12 Rustaiyan A, Masoudi S, Monfared A, Kamalinejad M, Lajevardi T, Sedaghat S, Yari M. Volatile constituents of three Thymus species grown wild in Iran. Planta Med 2000; 66: 197-198
  • 13 Marino M, Bersani C, Comi G. Antimicrobial activity of the essential oils of Thymus vulgaris L. measured using a bioimpedometric method. J Food Prot 1999; 62: 1017-1023
  • 14 Palmeira-de-Oliveira A, Salgueiro L, Palmeira-de-Oliveira R, Martinez-de-Oliveira J, Pina-Vaz C, Queiroz JA, Rodrigues AG. Anti-Candida activity of essential oils. Mini Rev Med Chem 2009; 9: 1292-1305
  • 15 Soković MD, Vukojević J, Marin PD, Brkić DD, Vajs V, van Griensven LJ. Chemical composition of essential oils of Thymus and Mentha species and their antifungal activities. Molecules 2009; 14: 238-249
  • 16 Grosso C, Figueiredo AC, Burillo J, Mainar AM, Urieta JS, Barroso JG, Coelho JA, Palavra AM. Composition and antioxidant activity of Thymus vulgaris volatiles: comparison between supercritical fluid extraction and hydrodistillation. J Sep Sci 2010; 33: 2211-2218
  • 17 El-Nekeety AA, Mohamed SR, Hathout AS, Hassan NS, Aly SE, Abdel-Wahhab MA. Antioxidant properties of Thymus vulgaris oil against aflatoxin-induce oxidative stress in male rats. Toxicon 2011; 57: 984-991
  • 18 Cuffini AM, Tullio V, Mandras N, Roana J, Banche G, Carlone NA. The leading role of antimicrobial agents in modulating the binomial host-microorganism. Curr Med Chem Anti Infect Agents 2004; 3: 1-13
  • 19 Tullio V, Mandras N, Scalas D, Allizond V, Banche G, Roana J, Greco D, Castagno F, Cuffini AM, Carlone NA. Synergy of caspofungin with human polymorphonuclear granulocytes for killing Candida albicans . Antimicrob Agents Chemother 2010; 54: 3964-3966
  • 20 Ahmad A, Khan A, Akhtar F, Yousuf S, Xess I, Khan LA, Manzoor N. Fungicidal activity of thymol and carvacrol by disrupting ergosterol biosynthesis and membrane integrity against Candida. Eur J Clin Microbiol Infect Dis 2011; 30: 41-50
  • 21 Bakkali F, Averbeck S, Averbeck D, Idaomar M. Biological effects of essential oils – a review. Food Chem Toxicol 2008; 46: 446-475
  • 22 Mickiené R, Bakutis B, Baliukoniene V. Antimicrobial activity of two essential oils. Ann Agric Environ Med 2011; 18: 139-144
  • 23 Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of yeasts, third edition. Approved standard M27-A3. Wayne: Clinical and Laboratory Standards Institute; 2008