Abstract
The use of Essential Oil (EO) as an antimicrobial agent has been widely used since antiquity, and interest has grown due to the resistance of microorganisms to drugs. This study aims to evaluate the chemical composition of Algerian Citrus limon peel EO and its antifungal activity against dermatophyte strains, according to the harvest period. EO from C. limon peel harvested during four different periods (Winter, Spring, Summer, and Autumn) was extracted by hydrodistillation Clevenger type and analyzed by GC/MS. Antifungal activity was evaluated against four dermatophyte strains (Trichophyton rubrum, Microsporum canis, Trichophyton mentagrophytes, and Microsporum gypseum) using the disc diffusion and agar dilution methods. The yield of EO from C. limon peel varied from 1.54 to 2.43% (w/w), the highest yield was obtained in Autumn and the lowest in Summer, the EOs were mainly composed of limonene (43.45–58.75%) followed by β-pinene (4.73–13.23%) and γ-terpinene (8.06–11.04%). The assessment of the antifungal activity showed that C. limon peel EO has a strong antifungal activity against the tested strains, with inhibition zones ranging from 16.63 ± 0,38 to 90.00 ± 00 mm, and Minimal Inhibitory Concentration (MIC) from 0.6 to 5 mg/mL and Minimal Fungicidal Concentration (MFC) from 1.25 to 10 mg/mL. Spring harvest EO was relatively more effective in terms of MIC (0.6–2.5 mg/mL) and MFC (1.25–2.5 mg/mL). The EO of C. limon peel showed a seasonal change in the chemical composition and the antifungal activity, also revealed a high antifungal potential, and can be used for the treatment of fungal infections caused by dermatophytes.
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References
Adams RP (2007) Identification of Essential Oil Components by Gas Chromatograpy/Mass Spectrometry, 4th Edition. Illinois USA Allured Publ Corp Carol Stream 804–806
Alma MH, Nitz S, Kollmannsberger H et al (2004) Chemical composition and antimicrobial activity of the essential oils from the gum of Turkish Pistachio (Pistacia vera L.). J Agric Food Chem 52:3911–3914. https://doi.org/10.1021/jf040014e
Alsohaili S (2018) Seasonal variation in the chemical composition and antimicrobial activity of essential oil extracted from achillea fragrantissima grown in northern - eastern jordanian desert. J Essent Oil-Bearing Plants 21:139–145. https://doi.org/10.1080/0972060X.2018.1446848
Alzahraa F, Ali HA, Al-janabi JKA, Alhattab MK (2017) Prevalence of dermatophyte fungal infection in Hillah, Iraq. Int J ChemTech Res 10:827–837
Amorim JL, Simas DLR, Pinheiro MMG et al (2016) Anti-inflammatory properties and chemical characterization of the essential oils of four Citrus species. PLoS ONE 11:1–18. https://doi.org/10.1371/journal.pone.0153643
Arrache D, Sebai K, Talzazet L et al (2015) Profil épidémiologique des teignes du cuir chevelu (2009–2014). J Mycol Med 25:243–244. https://doi.org/10.1016/J.MYCMED.2015.06.064
Belletti N, Kamdem SS, Patrignani F et al (2007) Antimicrobial activity of aroma compounds against Saccharomyces cerevisiae and improvement of microbiological stability of soft drinks as assessed by logistic regression. Appl Environ Microbiol 73:5580–5586. https://doi.org/10.1128/AEM.00351-07
Bourgou S, Rahali FZ, Ourghemmi I, Tounsi MS (2012) Changes of peel essential oil composition of four tunisian citrus during fruit maturation. Sci World J. https://doi.org/10.1100/2012/528593
Bouzenna H, Dhibi S, Samout N et al (2016) The protective effect of Citrus limon essential oil on hepatotoxicity and nephrotoxicity induced by aspirin in rats. Biomed Pharmacother 83:1327–1334. https://doi.org/10.1016/j.biopha.2016.08.037
Caccioni DRL, Guizzardi M, Biondi DM et al (1998) Relationship between volatile components of citrus fruit essential oils and antimicrobial action on Penicillium digitatum and Penicillium italicum. Int J Food Microbiol 43:73–79. https://doi.org/10.1016/S0168-1605(98)00099-3
Caputo L, Cornara L, Bazzicalupo M et al (2020) Chemical composition and biological activities of essential oils from peels of three Citrus species. Molecules 25:1–17. https://doi.org/10.3390/molecules25081890
Chabasse D, Contet-Audonneau N (2011) Dermatophytes et dermatophytoses. EMC - Mal Infect 8:1–15. https://doi.org/10.1016/s1166-8598(11)56491-9
Chadeganipour M, Nilipour S, Havaei A (2004) In vitro evaluation of griseofulvin against clinical isolates of dermatophytes from Isfahan. Mycoses 47:503–507. https://doi.org/10.1111/j.1439-0507.2004.01050.x
Daouda T, Prevost K, Gustave B et al (2014) Terpenes, antibacterial and modulatory antibiotic activity of essential oils from croton hirtus L’ Hér. (Euphorbiaceae) from ivory coast. J Essent Oil-Bearing Plants 17:607–616. https://doi.org/10.1080/0972060X.2014.958550
Ennaghra N, Meddour A, Soumati B, Kabouchi-Bouzidi L (2016) Epidemiological survey on the dermatophyte flora in the Area of Annaba East of Algeria. J Appl Environ Biol Sci 6:8–15
Favre B, Ghannoum MA, Ryder NS (2004) Biochemical characterization of terbinafine-resistant Trichophyton rubrum isolates. Med Mycol 42:525–529. https://doi.org/10.1080/13693780410001661482
Ferhat MA, Boukhatem MN, Hazzit M, Chemat F (2018) Rapid extraction of volatile compounds from Citrus fruits using a microwave dry distillation. J Fundam Appl Sci 8:753. https://doi.org/10.4314/jfas.v8i3.6
Fratini F, Giusti M, Mancini S et al (2021) Evaluation of the in vitro antibacterial activity of some essential oils and their blends against Staphylococcus spp. isolated from episodes of sheep mastitis. Rend Fis Acc Lincei 32:407–416. https://doi.org/10.1007/s12210-021-00991-5
Friedman M, Henika PR, Mandrell RE (2002) Bactericidal activities of plant essential oils and some of their isolated constituents against Campylobacter jejuni, Escherichia coli, Listeria monocytogenes, and Salmonella enterica. J Food Prot 65:1545–1560. https://doi.org/10.4315/0362-028X-65.10.1545
Gayoso CW, Lima EO, Oliveira VT et al (2005) Sensitivity of fungi isolated from onychomycosis to Eugenia cariophyllata essential oil and eugenol. Fitoterapia 76:247–249. https://doi.org/10.1016/j.fitote.2004.12.005
Golmakani MT, Moayyedi M (2015) Comparison of heat and mass transfer of different microwave-assisted extraction methods of essential oil from Citrus limon (Lisbon variety) peel. Food Sci Nutr 3:506–518. https://doi.org/10.1002/fsn3.240
Gondim CNFL, Carneiro JNP, Leite CP et al (2021) GC-MS-FID characterization and antibacterial activity of the essential oil from Achyrocline satureioides (Lam) DC. J Plant Biochem Biotechnol 31:394–398. https://doi.org/10.1007/s13562-021-00691-z
Hamroune Z, Mazouz A, Benelmouffok AB, Kellou D (2016) Evolution of tinea capitis observed in mycology laboratory of institute Pasteur of Algeria from1995 to 2015. J Mycol Med 26:337–344. https://doi.org/10.1016/j.mycmed.2016.06.005
Havlickova B, Czaika VA, Friedrich M (2009) Epidemiological trends in skin mycoses worldwide. Mycoses 52:95. https://doi.org/10.1111/j.1439-0507.2008.01668.x
Hussain AI, Anwar F, Hussain Sherazi ST, Przybylski R (2008) Chemical composition, antioxidant and antimicrobial activities of basil (Ocimum basilicum) essential oils depends on seasonal variations. Food Chem 108:986–995. https://doi.org/10.1016/j.foodchem.2007.12.010
Ismaili R, Lamiri A, Moustaid K (2014) Study of the antifungal activity of essential oils of three moroccan aromatic plants. Int J Innov Sci Res 12:2351–8014
Jain N, Sharma M (2017) Evaluation of Citrus lemon essential oil for its chemical and biological properties against fungi causing dermatophytic infection in human beings. Anal Chem Lett 7:402–409. https://doi.org/10.1080/22297928.2017.1349620
Jain N, Sharma M (2020) Inhibitory effect of some selected essential oil terpenes on fungi causing superficial infection in human beings. J Essent Oil-Bearing Plants 23:862–869. https://doi.org/10.1080/0972060X.2020.1824686
Jazet Dongmoa PM, Kuate J, Fekam Boyomc F et al (2002) Composition chimique et activité antifongique in vitro des huiles essentielles de Citrus sur la croissance mycélienne de Phaeoramularia angolensis. Fruits 57:95–104. https://doi.org/10.1051/fruits:2002009
Jing L, Lei Z, Li L et al (2014) Antifungal activity of citrus essential oils. J Agric Food Chem 62:3011–3033. https://doi.org/10.1021/jf5006148
Kheffache H, Seklaoui N, Bouchara JP et al (2020) Tinea capitis at the University Hospital of Tizi-Ouzou, Algeria, and first isolation of Trichophyton tonsurans. J Mycol Med 30:101040. https://doi.org/10.1016/j.mycmed.2020.101040
Lota ML, De Rocca SD, Tomi F et al (2002) Volatile components of peel and leaf oils of lemon and lime species. J Agric Food Chem 50:796–805. https://doi.org/10.1021/jf010924l
Luro F, Neves CG, Costantino G et al (2020) Effect of Environmental conditions on the yield of peel and composition of essential oils from citrus cultivated in Bahia (Brazil) and Corsica (France). Agronomy. https://doi.org/10.3390/agronomy10091256
Majdoub S, Chaabane-Banaoues R, El MR et al (2022) Seasonal variation in the chemical profile, Antifungal and insecticidal activities of essential oils from daucus reboudii. Waste Biomass Valorization 13:1859–1871. https://doi.org/10.1007/s12649-021-01594-9
Maness LR, Zubov T (2019) The Inhibitory effect of essential oils on rhizopus stolonifer, trichophyton mentagrophytes, and microsporum gypseum. Lab Med 50:E18–E22. https://doi.org/10.1093/labmed/lmy080
Mukherjee PK, Leidich SD, Isham N et al (2003) Clinical Trichophyton rubrum strain exhibiting primary resistance to terbinafine. Antimicrob Agents Chemother 47:82–86. https://doi.org/10.1128/AAC.47.1.82-86.2003
Murbach Teles Andrade BF, Nunes Barbosa L, Da Silva PI, Fernandes Júnior A (2014) Antimicrobial activity of essential oils. J Essent Oil Res 26:34–40. https://doi.org/10.1080/10412905.2013.860409
Nardoni S, Giovanelli S, Pistelli L et al (2015) In vitro activity of twenty commercially available, plant-derived essential oils against selected dermatophyte species. Nat Prod Commun 10:1473–1478. https://doi.org/10.1177/1934578x1501000840
Nasir M, Tafess K, Abate D (2015) Antimicrobial potential of the Ethiopian Thymus schimperi essential oil in comparison with others against certain fungal and bacterial species. BMC Complement Altern Med 15:1–5. https://doi.org/10.1186/s12906-015-0784-3
Nikolić MM, Jovanović KK, Marković TL et al (2017) Antimicrobial synergism and cytotoxic properties of Citrus limon L., Piper nigrum L. and Melaleuca alternifolia (Maiden and Betche) Cheel essential oils. J Pharm Pharmacol 69:1606–1614. https://doi.org/10.1111/jphp.12792
Ouraïni D, Agoumi A, Alaoui MI et al (2005) Approche thérapeutique des dermatophyties par les huiles essentielles de plantes aromatiques marocaines. Phytotherapie 3:3–12. https://doi.org/10.1007/s10298-005-0058-1
Pinto E, Pina-Vaz C, Salgueiro L et al (2006) Antifungal activity of the essential oil of Thymus pulegioides on Candida, Aspergillus and dermatophyte species. J Med Microbiol 55:1367–1373. https://doi.org/10.1099/jmm.0.46443-0
Pinto E, Hrimpeng K, Lopes G et al (2013) Antifungal activity of Ferulago capillaris essential oil against Candida, Cryptococcus, Aspergillus and dermatophyte species. Eur J Clin Microbiol Infect Dis 32:1311–1320. https://doi.org/10.1007/s10096-013-1881-1
Raspo MA, Vignola MB, Andreatta AE, Juliani HR (2020) Antioxidant and antimicrobial activities of citrus essential oils from Argentina and the United States. Food Biosci 36:100651. https://doi.org/10.1016/j.fbio.2020.100651
Remmal A, Bouchikhi T, Rhayour K et al (1993) Improved method for the determination of antimicrobial activity of essential oils in agar medium. J Essent Oil Res 5:179–184. https://doi.org/10.1080/10412905.1993.9698197
Riaz A, Khan RA, Mirza T et al (2014) In vitro/in vivo effect of Citrus limon (L. Burm. f.) juice on blood parameters, coagulation and anticoagulation factors in rabbits. Pak J Pharm Sci 27:907–915
Rozza AL, Moraes TDM, Kushima H et al (2011) Gastroprotective mechanisms of Citrus lemon (Rutaceae) essential oil and its majority compounds limonene and β-pinene: Involvement of heat-shock protein-70, vasoactive intestinal peptide, glutathione, sulfhydryl compounds, nitric oxide and prostaglandin E. Chem Biol Interact 189:82–89. https://doi.org/10.1016/j.cbi.2010.09.031
Sacchetti G, Maietti S, Muzzoli M et al (2005) Comparative evaluation of 11 essential oils of different origin as functional antioxidants, antiradicals and antimicrobials in foods. Food Chem 91:621–632. https://doi.org/10.1016/j.foodchem.2004.06.031
Sanguinetti M, Posteraro B, Romano L et al (2007) In vitro activity of Citrus bergamia (bergamot) oil against clinical isolates of dermatophytes. J Antimicrob Chemother 59:305–308. https://doi.org/10.1093/jac/dkl473
Sathish S, Narendrakumar G, Sundari N et al (2016) Extraction of pectin from used citrus Limon and optimization of process parameters using response surface methodology. Res J Pharm Technol 9:1451–1456. https://doi.org/10.5958/0974-360X.2016.00453.4
Silva L, Sousa J, Toscano C, Viana I (2022) Deep dermatophytosis caused by Trichophyton rubrum in immunocompromised patients. An Bras Dermatol 97:223–227. https://doi.org/10.1016/j.abd.2021.05.014
Sit NW, Chan YS, Lai SC et al (2018) In vitro antidermatophytic activity and cytotoxicity of extracts derived from medicinal plants and marine algae. J Mycol Med 28:561–567. https://doi.org/10.1016/j.mycmed.2018.07.001
Spadaro F, Circosta C, Costa R et al (2012) Volatile fraction composition and biological activity of lemon oil (Citrus limon L. Burm.): comparative study of oils extracted from conventionally grown and biological fruits. J Essent Oil Res 24:187–193. https://doi.org/10.1080/10412905.2012.659518
Sugar AM, Alsip SG, Galgiani JN et al (1987) Pharmacology and toxicity of high-dose ketoconazole. Antimicrob Agents Chemother 31:1874–1878. https://doi.org/10.1128/AAC.31.12.1874
Teixeira JPF, Marques MOM, Figueiredo JO (2013) Chemical composition of essential oils of fifteen lemon genotypes in two harvest seasons. Citrus Res Technol. https://doi.org/10.5935/2236-3122.20130008
Tolba H, Moghrani H, Benelmouffok A et al (2015) Essential oil of Algerian Eucalyptus citriodora: chemical composition, antifungal activity. J Mycol Med 25:e128–e133. https://doi.org/10.1016/j.mycmed.2015.10.009
van Vuuren SF, Viljoen AM (2007) Antimicrobial activity of limonene enantiomers and 1,8-cineole alone and in combination. Flavour Fragr J 22:540–544. https://doi.org/10.1002/ffj.1843
Vekiari SA, Protopapadakis EE, Papadopoulou P et al (2002) Composition and seasonal variation of the essential oil from leaves and peel of a cretan lemon variety. J Agric Food Chem 50:147–153. https://doi.org/10.1021/jf001369a
Viana MDM, Cardoso RM, Silva NKGT et al (2016) Anxiolytic-like effect of Citrus limon (L.) Burm f. essential oil inhalation on mice. Rev Bras Plantas Med 18:96–104. https://doi.org/10.1590/1983-084X/15_047
Viuda-Martos M, Ruiz-Navajas Y, Fernández-López J, Perez-Álvarez J (2008) Antibacterial activity of lemon (Citrus lemon L.), mandarin (Citrus reticulata L.), grapefruit (Citrus paradisi L.) and orange (Citrus sinensis L.) essential oils. J Food Saf 28:567–576. https://doi.org/10.1111/j.1745-4565.2008.00131.x
Zhang H, Chen Y, Wang S et al (2020) Extraction and comparison of cellulose nanocrystals from lemon (Citrus limon) seeds using sulfuric acid hydrolysis and oxidation methods. Carbohydr Polym. https://doi.org/10.1016/j.carbpol.2020.116180
Acknowledgements
This study was supported by the Laboratory of Reaction Engineering of USTHB and the Laboratory of Mycology of Pasteur Institute, Algiers, Algeria. The authors gratefully acknowledge support from the Directorate-General for Scientific Research and Technological Development of Algeria.
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Hadj Larbi, N., Moghrani, H., Nasrallah, N. et al. Influence of harvest season on the chemical composition and antifungal activity of Citrus limon essential oil. Rend. Fis. Acc. Lincei 34, 295–303 (2023). https://doi.org/10.1007/s12210-023-01132-w
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DOI: https://doi.org/10.1007/s12210-023-01132-w