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Antifungal Activity of Essential Oils Against Candida Species Isolated from Clinical Samples

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Abstract

We evaluated the in vitro antifungal activity of essential oils obtained from the aromatic plants Laurus nobilis, Thymus vulgaris, Mentha piperita, Cymbopogon citratus and Lippia junelliana against the following Candida species isolated from clinical samples: C. krusei (n = 10); C. albicans (n = 50); C. glabrata (n = 70) and C. parapsilosis (n = 80). The minimal inhibitory concentration (MIC) was determined according to EDef 7.3.1 document from EUCAST. Amphotericin B and fluconazole were the antifungal drugs used as inhibition control. The concentration ranges evaluated were 0.4–800 and 0.03–128 mg l−1 for essential oils and antifungal drugs, respectively. MIC50 and MIC90, mode and ranges were calculated. All the Candida spp. evaluated were susceptible to amphotericin B (MIC ≤ 1 mg l−1), while fluconazole was inactive for C. krusei (MIC ≥ 32 mg l−1) and intermediate for C. glabrata (MIC≤ 32 mg l−1). The essential oils showed antifungal activity on Candida spp. tested with MIC90 values ranging from 0.8 to 800 mg l−1. In general, the most active essential oils were L. nobilis and T. vulgaris (MIC90 0.8–0.16 mg l−1), and the least active was C. officinalis (MIC90 400–800 mg l−1). C. krusei was inhibited by 5/6 of the essential oils evaluated, and C. glabrata was the least susceptible one. This in vitro study confirms the antifungal activity of these six essential oils assayed which could be a potential source of new molecules useful to control fungal infections caused by some Candida species, including those resistant to antifungal drugs.

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References

  1. Barchiesi F, Orsetti E, Mazzanti S, Trave F, Salvi A, Nitti C, et al. Candidemia in the elderly: what does it change? PLoS One. 2017;12(5):e0176576. https://doi.org/10.1371/journal.pone.0176576.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Cleveland AA, Farley MM, Harrison LH, Stein B, Hollick R, Lockhart SR, et al. Changes in incidence and antifungal drug resistance in candidemia: results from population-based laboratory surveillance in Atlanta and Baltimore, 2008–2011. Clin Infect Dis. 2012;55(10):1352–61. https://doi.org/10.1093/cid/cis697.

    Article  CAS  PubMed  Google Scholar 

  3. Nucci M, Queiroz-Telles F, Alvarado-Matute T, Tiraboschi IN, Cortes J, Zurita J, et al. Epidemiology of candidemia in Latin America: a laboratory-based survey. PLoS One. 2013;8:e59373. https://doi.org/10.1371/journal.pone.0059373.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Tsai MH, Hsu JF, Chu SM, Chang PJ, Lai MY, Wu IH, et al. Clinical and microbiological characteristics and impact of therapeutic strategies on the outcomes of children with candidemia. Sci Rep. 2017;7(1):1083. https://doi.org/10.1038/s41598-017-01123-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Córdoba S, Vivot W, Bosco-Borgeat ME, Taverna C, Szusz W, Murisengo O, et al. Species distribution and susceptibility profile of yeasts isolated from blood culture: results of a multicenter active laboratory-based surveillance study in Argentina. Rev Arg Microbiol. 2011;43:176–185. ISSN 0325-7541.

  6. Lockhart SR, Iqbal N, Cleveland AA, Farley MM, Harrison LH, Bolden CB, et al. Species identification and antifungal susceptibility testing of Candida bloodstream isolates from population-based surveillance studies in two U.S. cities from 2008 to 2011. J Clin Microbiol. 2012;50(11):3435–42. https://doi.org/10.1128/jcm.01283-12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Pappas PG, Kauffman CA, Andes DR, Clancy CJ, Marr KA, Ostrosky-Zeichner L, et al. Clinical practice guideline for the management of candidiasis: 2016 update by the infectious diseases society of America. Clin Infect Dis. 2016;62(4):e1–50. https://doi.org/10.1093/cid/civ933.

    Article  PubMed  Google Scholar 

  8. Egunsola O, Adefurin A, Fakis A, Jacqz-Aigrain E, Choonara I, Sammons H. Safety of fluconazole in paediatrics: a systematic review. Eur J Clin Pharmacol. 2013;69:1211–21. https://doi.org/10.1007/s00228-012-1468-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Perlin DS, Rautemaa-Richardson R, Alastruey-Izquierdo A. The global problem of antifungal resistance: prevalence, mechanisms, and management. Lancet Infect Dis. 2017;17(12):e383–92. https://doi.org/10.1016/S1473-3099(17)30316-X.

    Article  PubMed  Google Scholar 

  10. Kontoyiannis DP. Antifungal resistance: an emerging reality and a global challenge. J Infect Dis. 2017;216(suppl_3):S431–5. https://doi.org/10.1093/infdis/jix179.

    Article  CAS  PubMed  Google Scholar 

  11. Sakkas H, Papadopoulou C. Antimicrobial activity of basil, oregano, and thyme essential oils. J Microbiol Biotechnol. 2017;27(3):429–38. https://doi.org/10.4014/jmb.1608.08024.

    Article  CAS  PubMed  Google Scholar 

  12. Swamy MK, Akhtar MS, Sinniah UR. Antimicrobial properties of plant essential oils against human pathogens and their mode of action: an updated review. Evid Based Complement Alternat Med. 2016;2016:3012462. https://doi.org/10.1155/2016/3012462.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Veeresham C. Natural products derived from plants as a source of drugs. J Adv Pharm Technol Res. 2012;3(4):200–1. https://doi.org/10.4103/2231-4040.104709.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Soković MD, Vukojevic J, Marin PD, Brkić DD, Vajs V, Van Griensven LJLD. Chemical composition of essential oils of Thymus and Mentha species and their antifungal activities. Molecules. 2009;14(1):238–49. https://doi.org/10.3390/molecules14010238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Borugă O, Jianu C, Mişcă C, Goleţ I, Gruia AT, Horhat FG. Thymus vulgaris essential oil: chemical composition and antimicrobial activity. J Med Life. 2014;3:56–60.

    Google Scholar 

  16. Delucchi G, Farina E, Torres Robles S. Laurus nobilis (Lauraceae) especie naturalizada en la República Argentina. Bol Soc Argent Bot. 2007;42(3–4):309–12.

    Google Scholar 

  17. Zuloaga FO, Belgrano MJ. The catalogue of vascular plants of the southern cone and the flora of Argentina: their contribution to the World Flora. Rodriguésia. 2015;66(4):989–1024. https://doi.org/10.1590/2175-7860201566405.

    Article  Google Scholar 

  18. Boukhatem MN, Ferhat MA, Kameli A, Saidi F, Kebir HT. Lemon grass (Cymbopogon citratus) essential oil as a potent anti-inflammatory and antifungal drugs. Libyan J Med. 2014;9:10. https://doi.org/10.3402/ljm.v9.25431.

    Article  PubMed Central  Google Scholar 

  19. Casamassima D, Chiosi F, Vizzarri F, Palazzo M, Costagliola C. The effect of Laurus nobilis on the blood and lenses antioxidant activity in rabbit under fat- 2 enriched diet. Physiol Res Physiol Res. 2017;66:325–33.

    CAS  PubMed  Google Scholar 

  20. Chmit M, Kanaan H, Habib J, Abbass M, Mcheik A, Chokr A. Antibacterial and antibiofilm activities of polysaccharides, essential oil, and fatty oil extracted from Laurus nobilis growing in Lebanon. Asian Pac J Trop Med. 2014;7S1:S546–52. https://doi.org/10.1016/s1995-7645(14)60288-1.

    Article  PubMed  Google Scholar 

  21. da Silva Ramos R, Rodrigues AB, Farias AL, Simões RC, Pinheiro MT, Ferreira RM, et al. Chemical composition and in vitro antioxidant, cytotoxic, antimicrobial, and larvicidal activities of the essential oil of Mentha piperita L. (Lamiaceae). Sci World J. 2017;2017:4927214. https://doi.org/10.1155/2017/4927214.

    Article  CAS  Google Scholar 

  22. Grigore A, Paraschiv I, Colceru-Mihul S, Bubueanu C, Draghici E, Ichim M. Chemical composition and antioxidant activity of Thymus vulgaris L. volatile oil obtained by two different methods. Rom Biotech Lett. 2010;15(4):5436–43.

    CAS  Google Scholar 

  23. Kilic A, Hafizoglu H, Kollmannsberger H, Nitz S. Volatile constituents and key odorants in leaves, buds, flowers, and fruits of Laurus nobilis L. J Agric Food Chem. 2004;52:1601–6.

    Article  CAS  PubMed  Google Scholar 

  24. Rachitha P, Krupashree K, Jayashree GV, Gopalan N, Khanum F. Growth inhibition and morphological alteration of fusarium sporotrichioides by mentha piperita essential oil. Pharmacognosy Res. 2017;9(1):74–9. https://doi.org/10.4103/0974-8490.199771.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Tyagi AK, Malik A. Liquid and vapour-phase antifungal activities of selected essential oils against candida albicans: microscopic observations and chemical characterization of cymbopogon citratus. BMC Complement Altern Med. 2010;10:65.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Monforte MT, Tzakou O, Nostro A, Zimbalatti V, Galati EM. Chemical composition and biological activities of Calamintha officinalis Moench essential oil. J Med Food. 2011;14(3):297–303. https://doi.org/10.1089/jmf.2009.0191.

    Article  CAS  PubMed  Google Scholar 

  27. Nazzaro F, Fratianni F, Coppola R, Feo V. Essential oils and antifungal activity. Pharmaceuticals (Basel). 2017;2;10(4). pii: E86. https://doi.org/10.3390/ph10040086.

  28. Morales-López SE, Taverna CG, Bosco-Borgeat ME, Maldonado I, Vivot W, Szusz W, et al. Candida glabrata complex species prevalence and antifungal susceptibility testing in an Argentinean culture collection: first description of Candida nivariensis in Argentina. Mycopathologia. 2016;181(11–12):871–8. https://doi.org/10.1007/s11046-016-0052-1.

    Article  CAS  PubMed  Google Scholar 

  29. European Committee for Antimicrobial Susceptibility Testing (EUCAST) Method for the determination of broth dilution minimum inhibitory concentrations of antifungal agents for yeasts, EUCAST Definitive Document E.Def 7.3.1 2017. www.eucast.org.

  30. NIST 2011-Standard Reference Database 1A. NIST/EPA/NIH Mass Spectral Database (NIST 11) and NIST Mass Spectral Search Program (Version 2.0g). www.nist.gov/sites/default/files/documents/srd/NIST1a11Ver2-0Man.pdf.

  31. Adams RP. Identification of essential oils components by gas chromatography/mass spectroscopy. 2007. 4th ed. Allured Pub. Corp., Carol Stream, Illinois, USA.

  32. Kovats E. Gas chromatographic characterization of organic substances in the retention index system. Adv Chromatogr. 1965;1:229–47.

    CAS  Google Scholar 

  33. Larrán S, Ringuelet JA, Carranza MR, Henning CP, Ré MS, Cerimele EL, et al. In vitro fungistatic effect of essential oils against Ascosphaera apis. J Essential Oil Res. 2001;13(2):122–4. https://doi.org/10.1080/10412905.2001.9699633.

    Article  Google Scholar 

  34. INIBIOLP. Instituto de Investigaciones Bioquímicas de La Plata “Profesor Doctor Rodolfo R. Brenner”. http://www.inibiolp.org.ar/.

  35. Alippi AM, Ringuelet JA, Cerimele EL, Re MS, Henning CP. Antimicrobial activity of some essential oils against Paenibacillus larvae, the causal agent of American foulbrood disease. J Herbs Spices Med Plants. 1996;4(2):9–16.

    Article  Google Scholar 

  36. European Committee on Antimicrobial Susceptibility Testing (EUCAST). Antifungal Agents. Breakpoint tables for interpretation of MICs Version 9.0 valid from 2018-02-12;1–5. www.eucast.org.

  37. 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.

    Article  CAS  PubMed  Google Scholar 

  38. Rajput SB, Karuppayil SM. Small molecules inhibit growth, viability and ergosterol biosynthesis in Candida albicans. Springerplus. 2013;2(1):26. https://doi.org/10.1186/2193-1801-2-26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Satyal P, Murray BL, McFeeters RL, Setzer WN. Essential oil characterization of thymus vulgaris from various geographical locations. Foods. 2016;5:70. https://doi.org/10.3390/foods5040070.

    Article  CAS  PubMed Central  Google Scholar 

  40. De Toledo LG, Dos Santos Ramos MA, Spósito L, Castilho EM, Pavan FR, De Oliveira Lopes É, et al. Essential Oil of Cymbopogon nardus (L.) Rendle: a strategy to combat fungal infections caused by Candida Species. Int J Mol Sci. 2016;17:1252. https://doi.org/10.3390/ijms17081252.

    Article  CAS  PubMed Central  Google Scholar 

  41. Zygadlo JA, Grosso NR. Comparative study of the antifungal activity of essential oils from aromatic plants growing wild in the central region of Argentina. Flavour Fragr J. 1995;10:113–8.

    Article  CAS  Google Scholar 

  42. Nostro A, Cannatelli MA, Morelli I, Musolino AD, Scuderi F, Pizzimenti F, et al. Efficiency of Calamintha officinalis essential oil as preservative in two topical product types. J Appl Microbiol. 2004;97:395–401. https://doi.org/10.1111/j.1365-2672.2004.02319.x.

    Article  CAS  PubMed  Google Scholar 

  43. Galindo LA, Pultrini Ade M, Costa M. Biological effects of Ocimum gratissimum L. are due to synergic action among multiple compounds present in essential oil. J Nat Med. 2010;64(4):436–41. https://doi.org/10.1007/s11418-010-0429-2.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Sonia Vigna and Miguel Juárez for providing the essential oils used in the present study.

Funding

This study was partially funded by the Universidad Nacional de La Plata, Tetraanual Research Incentive Project No. 11A 283.

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SC designed the study and prepared the manuscript; WV and WS performed the in vitro test; GNA analyzed the data.

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Correspondence to S. Córdoba.

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Córdoba, S., Vivot, W., Szusz, W. et al. Antifungal Activity of Essential Oils Against Candida Species Isolated from Clinical Samples. Mycopathologia 184, 615–623 (2019). https://doi.org/10.1007/s11046-019-00364-5

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