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Antifungal Activities of Origanum Vulgare Subsp. Hirtum, Mentha Spicata, Lavandula Angustifolia, and Salvia Fruticosa Essential Oils Against Human Pathogenic Fungi

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Antifungal Activities of Origanum Vulgare Subsp. Hirtum, Mentha Spicata, Lavandula Angustifolia, and Salvia Fruticosa Essential Oils Against Human Pathogenic Fungi J. Agric. Food Chem. 1998, 46, 1739−1745 1739 Antifungal Activities of Origanum vulgare subsp. hirtum, Mentha spicata, Lavandula angustifolia, and Salvia fruticosa Essential Oils against Human Pathogenic Fungi Konstantia Adam,† Afroditi Sivropoulou,† Stella Kokkini,‡ Thomas Lanaras,‡ and Minas Arsenakis*,† Laboratory of General Microbiology, Section of Genetics, Development and Molecular Biology, School of Biology, and Laboratory of Systematic Botany and Phytogeography, Section of Botany, School of Biology, Aristotle University, Thessaloniki 54006, Greece The essential oils of Origanum vulgare subsp. hirtum, Mentha spicata, Lavandula angustifolia, and Salvia fruticosa exhibited antifungal properties against the human pathogens Malassezia furfur, Trichophyton rubrum, and Trichosporon beigelii. Of the four oils, O. vulgare subsp. hirtum oil showed the highest fungicidal activity and at a dilution of 1/50000 caused a 95% reduction in the number of metabolically active cells within6hofexposure. Among the main components of the four oils, carvacrol and thymol exhibited the highest levels of antifungal activity. The therapeutic efficacy of the O. vulgare subsp. hirtum essential oil was tested in rats experimentally infected with T. rubrum and yielded promising results. Furthermore, the above essential oils were tested with the Ames test and did not exhibit any mutagenic activity. Keywords: Essential oils; Origanum vulgare; Mentha spicata; Lavandula angustifolia; Salvia fruticosa; Malassezia furfur; Trichophyton rubrum; Trichosporon beigelii; Dermatophytosis; anti- fungal; mutagenic; in vivo studies INTRODUCTION MATERIALS AND METHODS Plant Material: GC and GC/MS Analyses of Essential Aromatic plants have been widely used to extend the Oils. Wild growing, fully flowered O. vulgare subsp. hirtum shelf life of foods and in folk medicine. It is known that plants were collected from Mt. Iti (central Greece). M. spicata most of their properties are due to the essential oils they and S. fruticosa were collected from Sithonia Peninsula contain as products of their secondary metabolism. (northern Greece), whereas L. angustifolia was of commercial origin, bought in the market of Thessaloniki. Voucher speci- Recently many studies on the antifungal activities of mens of the collected plants are kept in the Herbarium of the the essential oils have been reported (Garg and Siddiqui, Laboratory of Systematic Botany and Phytogeography, Aris- 1992; Daouk et al., 1995, Shimoni et al., 1993; Muller- totle University of Thessaloniki. Riedau et al., 1995; Thompson, 1989; Mishra and Dubey, The air-dried plant material (leaves only) was cut in small 1994; Kishore et al., 1993). Most of these have focused pieces, and the essential oils were isolated after hydrodistil- on the antifungal activities of essential oils against soil- lation for 2 h. The three essential oils were chromatographed borne pathogens (Shimoni et al., 1993; Muller-Riedau using a Shimadzu GC-14A gas chromatograph equipped with a Supelcowax 10 (Supelco, Bellefonte, PA) capillary column et al., 1995) and food storage fungi (Thompson, 1989; (60 m × 0.25 mm i.d.) and a flame ionization detector (FID). Mishra and Dubey, 1994; Kishore et al., 1993). Es- The carrier gas was helium, and the linear gas velocity was sential oils of some plants have proved their potential 20.4 cm s-1. The injection and FID temperature was initially for use as natural fumigants in controlling the fungal 70 °C, increased at a rate of 2 °C/min to 180 °C, then increased deterioration of some foods during storage (Dwivedi and at a rate of 4 °C/min to 200 °C, and finally isothermal for 10 Dubey, 1993; Mishra and Dubey, 1994). However, there min. GC/MS analyses were conducted using a Shimadzu GC/ MS QP2000 system equipped with a Supelcowax 10 capillary is only limited information in the literature on the column (60 m × 0.25 mm i.d.) under the same GC conditions. antifungal activity of essential oils toward human fungal For GC/MS detection an electron impact (EI) quadropolar pathogens. In the present study the antifungal activi- system was used with ionization energy of 70 eV. The ties of four essential oils [Origanum vulgare L. subsp. essential oil components were identified by comparing their hirtum (Link) Ietswaart, Mentha spicata L., Lavandula relative retention times and mass spectra with those of angustifolia Miller, and Salvia fruticosa Miller (syn.: S. authentic samples, the Wiley Registry of Mass Spectral Data (McLafferty, 1994), and literature citations (Cornu and Massot, triloba L.)] were examined against three widely spread 1979; Masada, 1976; Jennings and Shibamoto, 1980). It pathogenic fungal strains that cause superficial skin should be noted that all experiments in this study were carried infections in humans. out with the same lot of essential oil to ensure reproducibility due to the inherent variability observed from lot to lot. Fungal Strains and Media. The following reference * Author to whom correspondence should be addressed (fax strains of fungi, purchased from the National Collection of +30-31-99 8311; e-mail [email protected]). Pathogenic Fungi (Public Health Laboratory, Mycology Refer- † Laboratory of General Microbiology. ence Laboratory, Bristol), were used as test organisms in all ‡ Laboratory of Systematic Botany and Phytogeography. antifungal assays: Malassezia furfur (yeast, NCPF No. 3349), S0021-8561(97)00829-7 CCC: $15.00 © 1998 American Chemical Society Published on Web 04/11/1998 1740 J. Agric. Food Chem., Vol. 46, No. 5, 1998 Adam et al. Table 1. Qualitative and Quantitative Composition (Percent) of Essential Oils Obtained from O. vulgare subsp. hirtum, M. spicata, L. angustifolia, and S. fruticosa compound O. vulgare subsp. hirtum M. spicata L. angustifolia S. fruticosa 1 R-thujene 0.04 0.03 0.30 2 R-pinene 0.65 0.91 0.58 6.85 3 camphene 0.04 0.04 0.02 4 â-pinene 0.98 0.09 0.25 8.20 5 sabinene 0.11 1.15 0.08 4.81 6 δ-3-carene 0.04 0.03 7 myrcene 0.12 0.84 0.45 3.16 8 R-phellandrene 0.06 0.03 9 R-terpinene 1.63 0.45 0.06 10 limonene 1.21 5.07 0.25 1.50 11 1,8-cineole 0.21 5.42 13.10 43.10 12 â-phellandrene 0.07 13 (Z)-â-ocimene 0.16 0.14 3.11 14 γ-terpinene 5.54 0.04 0.07 0.09 15 (E)-â-ocimene 0.04 0.03 2.84 0.06 16 p-cymene 7.35 0.09 0.93 17 terpinolene 0.05 0.09 0.03 18 R-thujone 0.95 19 â-thujone 0.93 20 3-octanol 0.08 21 cis-linalool oxide (furanoid) 0.04 22 1-octen-3-ol 0.08 0.53 0.19 23 trans-linalool oxide (furanoid) 0.05 24 trans-sabinene hydrate 0.38 0.53 0.13 25 camphor 5.50 18.34 26 cis-sabinene hydrate 0.53 0.38 0.13 27 linalool 0.18 0.06 20.18 0.12 28 linalyl acetate 18.60 0.07 29 bornyl acetate 0.82 30 terpinen-4-ol 0.03 0.60 1.05 1.45 31 lavandulyl acetate 16.01 32 â-caryophyllene 0.97 0.90 2.15 1.53 33 lavandulol 3.09 34 trans-dihydrocarvone 0.12 35 cis-dihydrocarvone 4.90 36 isoborneol 0.06 1.52 37 R-humulene 0.20 0.25 0.16 38 R-terpineol + borneol 0.83 1.29 1.03 39 dihydrocarvyl acetate 0.19 40 germacrene D 1.76 0.80 41 neodihydrocarveol 0.18 42 neoisodihydrocarvyl acetate 0.90 43 carvone 59.12 44 dihydrocarveol 6.27 45 neoisodihydrocarveol 2.11 46 trans-carvyl acetate 0.24 47 trans-carveol 0.68 48 cis-carveol 3.90 49 neryl aceate 0.87 50 geranyl acetae 0.45 51 cis-jasmone 0.16 52 p-cymen-8-ol 0.50 53 caryophyllene oxide 0.15 1.34 54 spathulenol 0.13 55 thymol 45.22 0.03 56 carvacrol 33.05 Trichophyton rubrum (keratinophilic fungus, NCPF No. 192), Fungal disks, 7 mm in diameter, taken from a 7-day-old and Trichosporon beigelii (yeast, NCPF No. 3067). T. rubrum culture, were placed in the center of the Petri dish and and T. beigelii were grown and maintained in Sabouraud agar incubated at 27 (1 °C for 7 days. At the end of the incubation or in potato dextrose agar (PDA), while M. furfur was grown period the minimum inhibitory concentration (MIC) that in a medium containing 0.5% (w/v) glucose, 1.5% (w/v) bacte- caused complete inhibition of the mycelial growth was deter- riological agar, 0.01% (w/v) yeast extract, 0.4% (w/v) ox bile, mined. The fungistatic or fungicidal nature of the oils was 0.1% (v/v) glycerol, 2% (v/v) sterile olive oil, 0.05% (v/v) Tween determined by testing revival of growth following transfer of 60, and 1% (v/v) whole cow’s milk. All cultures were incubated the mycelial disk to an appropriate agar plate without oil. at 27 ((1) °C for 7 days. Finally, the lowest concentration of the oil that caused fungal Antifungal Assays. (a) Poisoned Food Technique. The death (minimum lethal concentration; MLC) was determined. toxicity of the essential oils against the three fungi was tested (b) Disk Diffusion Assay. Filter paper disks (Whatman No. by using the poisoned food technique described by Grover and 1, 5 mm in diameter) containing 5 µL of essential oil or isolated Moore (1962). The oils were diluted in 95% ethanol and were compound (authentic samples, Aldrich Chemical Co., Milwau- then mixed and homogenized by ultrasonication with the kee, WI) were applied to the surface of agar plates previously appropriate fungus growth medium to achieve final concentra- seeded with the test fungus. The fungal inoculum was taken tions of 4, 2, 1, 0.5, 0.25, or 0.125 µL/mL of medium.
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