Evaluation of vapor-phase antifungal activities of selected plant essential oils against fungal strains growing on bread food model
Keywords:essential oil, Penicillium sp., antioxidant activity, antifungal activity, bakery product
The current study aimed to investigate antifungal activities of two commercially available essential oils (EOs), specifically Tea tree oil (Melaleuca alternifolia; TTEO) and St. John's wort oil (Hypericum perforatum; HPEO) against three Penicillium (P.) species: P. citrinum, P. expansum, and P. crustosum in in situ conditions. For this purpose, EOs were applied in the vapor phase to determine the growth inhibition of fungi artificially inoculated on sliced bread. Changes in colony growth rate were evaluated as markers for the mycelial growth inhibition (MGI) effect of the EOs. The antioxidant activities of the EOs were evaluated using the DPPH method. The moisture content (MC) and water activity (aw) of bread as a substrate for fungal growth were also measured. From the DPPH assay, we have found that both EOs (TTEO, HPEO) exhibited strong antioxidant activity (64.94 ±7.34%; 70.36 ±1.57%, respectively). The values for bread MC and aw were 43.01 ±0.341% and 0.947 ±0.006, respectively. Our results suggest that HPEO is the only weak inhibitor of P. citrinum and P. crustosum colony growths. Also, the highest concentrations of TTEO display only the weak capability of mycelial growth inhibition of P. citrinum and P. crustosum. By contrast, the colony growth of P. expansum was enhanced by both EOs at all levels used. In conclusion, the application of both EOs in the vapor phase against selected Penicillium species seems not to be a promising alternative to chemical inhibitors used for bread preservation.
Abdullah, N., Nawawi, A., Othman, I. 2000. Fungal spoilage of starch-based foods in relation to its water activity (aw). Journal of Stored Products Research, vol. 36, no. 1, p. 47-54. https://doi.org/10.1016/S0022-474X(99)00026-0
Ahmed, M., Pickova, J., Ahmad, T., Liaquat, M., Farid, A., Jahangir, M. 2016. Oxidation of Lipids in Foods. Sarhad Journal of Agriculture, vol. 32, no. 3, p. 230-238. https://doi.org/10.17582/journal.sja/2016.32.3.230.238
Al-Muhtaseb, A. H., McMinn, W. A. M., Magee, T. R. A. 2002. Moisture Sorption Isotherm Characteristics of Food Products: A Review. Food and Bioproducts Processing, vol. 80, no. 2, p. 118-128. https://doi.org/10.1205/09603080252938753
Aman, M., Rai, V. R. 2015. Antifungal activity of fungicides and plant extracts against yellow sigatoka disease causing Mycosphaerella musicola. Current Research in Environmental and Applied Mycology, vol. 5, no. 3, p. 277-284. https://doi.org/10.5943/cream/5/3/11
Balaguer, M. P., Lopez-Carballo, G., Catala, R., Gavara, R., Hernandez-Munoz, P. 2013. Antifungal properties of gliadin films incorporating cinnamaldehyde and application in active food packaging of bread and cheese spread foodstuffs. International Journal of Food Microbiology, vol. 166, no. 3, p. 369-377. https://doi.org/10.1016/j.ijfoodmicro.2013.08.012
Barnes, J., Anderson, L. A., Phillipson, J. D. 2001. St John's wort (Hypericum perforatum L.): a review of its chemistry, pharmacology and clinical properties. Journal of Pharmacy and Pharmacology, vol. 53, no. 5, p. 583-600. https://doi.org/10.1211/0022357011775910
Belz, M. C. E., Mairinger, R., Zannini, E., Ryan, L. A. M., Cashman, K. D., Arendt, E. K. 2012. The effect of sourdough and calcium propionate on the microbial shelf-life of salt reduced bread. Applied Microbiology and Biotechnology, vol. 96, no. 2, p. 493-501. https://doi.org/10.1007/s00253-012-4052-x
Burt, S. 2004. Essential oils: their antibacterial properties and potential applications in foods - a review. International Journal of Food Microbiology, vol. 94, no. 3, p. 223-253. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022
Burt, S. A., Reinders, R. D. 2003. Antibacterial activity of selected plant essential oils against Escherichia coli O157: H7. Letters in Applied Microbiology, vol. 36, no. 3, p. 162-167. https://doi.org/10.1046/j.1472-765X.2003.01285.x
Chidi, F., Bouhoudan, A., Khaddor, M. 2020. Antifungal effect of the tea tree essential oil (Melaleuca alternifolia) against Penicillium griseofulvum and Penicillium verrucosum. Journal of King Saud University - Science, vol. 32, no. 3, p. 2041-2045. https://doi.org/10.1016/j.jksus.2020.02.012
Chouhan, S., Sharma, K., Guleria, S. 2017. Antimicrobial Activity of Some Essential Oils - Present Status and Future Perspectives. Medicines, vol. 4, no. 3, 21 p. https://doi.org/10.3390/medicines4030058
Cox, S. D., Mann, C. M., Markham, J. L., Bell, H. C., Gustafson, J. E., Warmington, J. R., Wyllie, S. G. 2000. The mode of antimicrobial action of the essential oil of Melaleuca alternifolia (tea tree oil). Journal of Applied Microbiology, vol. 88, no. 1, p. 170-175. https://doi.org/10.1046/j.1365-2672.2000.00943.x
Cox, S. D., Mann, C. M., Markham, J. L., Gustafson, J. E., Warmington, J. R., Wyllie, S. G. 2001. Determining the Antimicrobial Actions of Tea Tree Oil. Molecules, vol. 6, no. 2, p. 87-91. https://doi.org/10.3390/60100087
Crockett, S. L. 2010. Essential Oil and Volatile Components of the Genus Hypericum (Hypericaceae). Natural Product Communications, vol. 5, no. 9, p. 1493-1506. https://doi.org/10.1177/1934578X1000500926
Davey, K. R. 1989. A predictive model for combined temperature and water activity on microbial growth during the growth phase. Journal of Applied Bacteriology, vol. 67, no. 5, p. 483-488. https://doi.org/10.1111/j.1365-2672.1989.tb02519.x
de Groot, A. C., Schmidt, E. 2016. Tea tree oil: contact allergy and chemical composition. Contact Dermatitis, vol. 75, no. 3, p. 129-143. https://doi.org/10.1111/cod.12591
Donnelly, J. K., Robinson, D. S. 1995. Invited Review Free Radicals in Foods. Free Radical Research, vol. 22, no. 2, p. 147-176. https://doi.org/10.3109/10715769509147536
Fadel, H. H. M., El-Ghorab, A. H., Hussein, A. M. S., El-Massry, K. F., Lotfy, S. N., Ahmed, M. Y. S., Soliman, T. N. 2020. Correlation between chemical composition and radical scavenging activity of 10 commercial essential oils: Impact of microencapsulation on functional properties of essential oils. Arabian Journal of Chemistry, vol. 13, no. 8, p. 6815-6827. https://doi.org/10.1016/j.arabjc.2020.06.034
Grafakou, M. E., Diamanti, A., Antaloudaki, E., Kypriotakis, Z., Ćirić, A., Soković, M., Skaltsa, H. 2020. Chemical Composition and Antimicrobial Activity of the Essential Oils of Three Closely Related Hypericum Species Growing Wild on the Island of Crete, Greece. Applied Sciences, vol. 10, no. 8, 12 p. https://doi.org/10.3390/app10082823
Irshad, M., Subhani, M. A., Ali, S., Hussain, A. 2020. Biological Importance of Essential Oils. In El-Shemy, H. Essential Oils. Oils of Nature. London, UK : IntechOpen. ISBN: 978-1-83880-851-8. https://doi.org/10.5772/intechopen.87198
Jürgenliemk, G., Nahrstedt, A. 2002. Phenolic Compounds from Hypericum perforatum. Planta Medica, vol. 68, no. 1, p. 88-91. https://doi.org/10.1055/s-2002-20053
Kačániová, M., Galovičová, L., Ivanišová, E., Vukovic, N. L., Štefániková, J., Valková, V., Borotová, P., Žiarovská, J., Terentjeva, M., Felšöciová, S., Tvrdá, E. 2020a. Antioxidant, Antimicrobial and Antibiofilm Activity of Coriander (Coriandrum sativum L.) Essential Oil for Its Application in Foods. Foods, vol. 9, no. 3, 19 p. https://doi.org/10.3390/foods9030282
Kačániová, M., Terentjeva, M., Galovičová, L., Ivanišová, E., Štefániková, J., Valková, V., Borotová, P., Kowalczewski, P. L., Kunová, S., Felšöciová, S., Tvrdá, E., Žiarovská, J., Prokeinová, R. B., Vukovic, N. 2020b. Biological Activity and Antibiofilm Molecular Profile of Citrus aurantium Essential Oil and Its Application in a Food Model. Molecules, vol. 25, no. 17, 21 p. https://doi.org/10.3390/molecules25173956
Kalemba, D., Kunicka, A. 2003. Antibacterial and Antifungal Properties of Essential Oils. Current Medicinal Chemistry, vol. 10, no 10, p. 813-829. https://doi.org/10.2174/0929867033457719
Kim, H. J., Chen, F., Wu, C., Wang, X., Chung, H. Y., Jin, Z. 2004. Evaluation of Antioxidant Activity of Australian Tea Tree (Melaleuca alternifolia) Oil and Its Components. Journal of Agricultural and Food Chemistry, vol. 52, no. 10, p. 2849-2854. https://doi.org/10.1021/jf035377d
Kitanov, G. M. 2001. Hypericin and pseudohypericin in some Hypericum species. Biochemical Systematics and Ecology, vol. 29, no. 2, p. 171-178. https://doi.org/10.1016/S0305-1978(00)00032-6
Krisch, J., Tserennadmid, R., Vágvölgyi, C. 2011. Essential oils against yeasts and moulds causing food spoilage. Science against microbial pathogens: Communicating current research and technological advances. Formatex Research Center, Badajoz, Spain, p. 1135-1142.
Labuza, T. P., McNally, L., Gallagher, D., Hawkes, J., Hurtado, F. 1972. Stability of intermediate moisture foods. 1. Lipid oxidation. Journal of Food Science, vol. 37, no. 1, p. 154-159. https://doi.org/10.1111/j.1365-2621.1972.tb03408.x
Laird, K., Phillips, C. 2012. Vapour phase: a potential future use for essential oils as antimicrobials? Letters in Applied Microbiology, vol. 54, no. 3, p. 169-174. https://doi.org/10.1111/j.1472-765X.2011.03190.x
Legan, J. D. 1993. Mould spoilage of bread: the problem and some solutions. International Biodeterioration & Biodegradation, vol. 32, no. 1-3, p. 33-53. https://doi.org/10.1016/0964-8305(93)90038-4
Li, Y., Shao, X., Xu, J., Wei, Y., Xu, F., Wang, H. 2017. Effects and possible mechanism of tea tree oil against Botrytis cinerea and Penicillium expansum in vitro and in vivo test. Canadian Journal of Microbiology, vol. 63, no. 3, p. 219-227. https://doi.org/10.1139/cjm-2016-0553
Lis‐Balchin, M., Deans, S. G., Eaglesham, E. 1998. Relationship between bioactivity and chemical composition of commercial essential oils. Flavour and Fragrance Journal, vol. 13, no. 2, p. 98-104. https://doi.org/10.1002/(SICI)1099-1026(199803/04)13:2<98::AID-FFJ705>3.0.CO;2-B
Luz, C., Calpe, J., Saladino, F., Luciano, F. B., Fernandez‐Franzón, M., Mañes, J., Meca, G. 2018. Antimicrobial packaging based on ɛ‐polylysine bioactive film for the control of mycotoxigenic fungi in vitro and in bread. Journal of Food Processing and Preservation, vol. 42, no. 1, 6 p. https://doi.org/10.1111/jfpp.13370
Lyles, J. T., Kim, A., Nelson, K., Bullard-Roberts, A. L., Hajdari, A., Mustafa, B., Quave, C. L. 2017. The Chemical and Antibacterial Evaluation of St. John's Wort Oil Macerates Used in Kosovar Traditional Medicine. Frontiers in Microbiology, vol. 8, 19 p. https://doi.org/10.3389/fmicb.2017.01639
Mathis, C., Ourisson, G. 1964. Étude chimio-taxonomique du genre Hypericum: II. Identification de constituants de diverses huiles essentielles d'Hypericum (Chemotaxonomic study of the genus Hypericum: II. Identification of the constituents of various essential oils of Hypericum). Phytochemistry, vol. 3, no. 1, p. 115-131. (In French) https://doi.org/10.1016/S0031-9422(00)84003-0
Milosevic, T., Solujic, S., Sukdolak, S. 2007. In Vitro Study of Ethanolic Extract of Hypericum perforatum L. on Growth and Sporulation of Some Bacteria and Fungi. Turkish Journal of Biology, vol. 31, no. 4, p. 237-241.
Omarova, M. A., Artamonova, N. A. 1999. Classes and fatty-acid composition of lipids from Hypericum perforatum. Chemistry of Natural Compounds, vol. 35, no. 6, p. 684-685. https://doi.org/10.1007/BF02236306
Orčić, D. Z., Mimica-Dukić, N. M., Francišković, M. M., Petrović, S. S., Jovin, E. Đ. 2011. Antioxidant activity relationship of phenolic compounds in Hypericum perforatum L. Chemistry Central Journal, vol. 5, no. 1, 8 p. https://doi.org/10.1186/1752-153X-5-34
Orhan, I. E., Kartal, M. 2015. LC-DAD-MS-Assisted Quantification of Marker Compounds in Hypericum perforatum L. (St. John’s Wort) and its Antioxidant Activity. Turkish Journal of Pharmaceutical Sciences, vol. 12, no. 3, p. 279-286. https://doi.org/10.5505/tjps.2015.47965
Passarinho, A. T. P., Dias, N. F., Camilloto, G. P., Cruz, R. S., Otoni, C. G., Moraes, A. R. F., Soares, N. D. F. F. 2014. Sliced Bread Preservation through Oregano Essential Oil‐Containing Sachet. Journal of Food Process Engineering, vol. 37, no. 1, p. 53-62. https://doi.org/10.1111/jfpe.12059
Patel, Y. J. K., Smith, M. D. P., de Belleroche, J., Latchman, D. 2005. Hsp27 and Hsp70 administered in combination have a potent protective effect against FALS-associated SOD1-mutant-induced cell death in mammalian neuronal cells. Molecular Brain Research, vol. 134, no. 2, p. 256-274. https://doi.org/10.1016/j.molbrainres.2004.10.028
Pirbalouti, A. G., Samani, M. R., Hashemi, M., Zeinali, H. 2014. Salicylic acid affects growth, essential oil and chemical compositions of thyme (Thymus daenensis Celak.) under reduced irrigation. Plant Growth Regulation, vol. 72, no. 3, p. 289-301. https://doi.org/10.1007/s10725-013-9860-1
Puvača, N., Čabarkapa, I., Bursić, V., Petrović, A., Aćimović, M. 2018. Antimicrobial, antioxidant and acaricidal properties of tea tree (Melaleuca alternifolia). Journal of Agronomy, Technology and Engineering Management, vol. 1, no. 1, p. 29-38.
Rajkapoor, B., Burkan, Z. E., Senthilkumar, R. 2010. Oxidants and human diseases: role of antioxidant medicinal plants-a review. Pharmacology online, vol. 1, p. 1117-1131.
Rančić, A., Soković, M., Vukojević, J., Simić, A., Marin, P., Duletić-Laušević, S., Djoković, D. 2005. Chemical Composition and Antimicrobial Activities of Essential Oils of Myrrhis odorata (L.) Scop, Hypericum perforatum L and Helichrysum arenarium (L.) Moench. Journal of Essential Oil Research, vol. 17, no. 3, p. 341-345. https://doi.org/10.1080/10412905.2005.9698925
Ravindran, R., Jaiswal, A. K. 2016. Exploitation of Food Industry Waste for High-Value Products. Trends in Biotechnology, vol. 34, no. 1, p. 58-69. https://doi.org/10.1016/j.tibtech.2015.10.008
Rogawansamy, S., Gaskin, S., Taylor, M., Pisaniello, D. 2015. An Evaluation of Antifungal Agents for the Treatment of Fungal Contamination in Indoor Air Environments. International Journal of Environmental Research and Public Health, vol. 12, no. 6, p. 6319-6332. https://doi.org/10.3390/ijerph120606319
Roos, Y. H., Jouppila, K., Söderholm, E. S. 1999. Crystallization of amorphous food components and polymers. Water Management in the Design and Distribution of Quality Foods, p. 429-452.
Sánchez‐Moreno, C., Larrauri, J. A., Saura‐Calixto, F. 1998. A procedure to measure the antiradical efficiency of polyphenols. Journal of the Science of Food and Agriculture, vol. 76, no. 2, p. 270-276. https://doi.org/10.1002/(SICI)1097-0010(199802)76:2<270::AID-JSFA945>3.0.CO;2-9
Schwob, I., Bessière, J. M., Viano, J. 2002. Composition of the essential oils of Hypericum perforatum L. from southeastern France. Comptes Rendus Biologies, vol. 325, no. 7, p. 781-785. https://doi.org/10.1016/S1631-0691(02)01489-0
Sparenberg, B. 1993. MAO-inhibierende Eigenschaften von Hypericuminhaltsstoffen und Untersuchungen zur Analytik und Isolierung von Xanthonen aus Hypericum perforatum L. (MAO-inhibiting properties of hypericumin ingredients and studies on the analysis and isolation of xanthones from Hypericum perforatum). Dissertation thesis. (In German)
Talibi, I., Askarne, L., Boubaker, H., Boudyach, E. H., Msanda, F., Saadi, B., Aoumar, A. A. B. 2012. Antifungal activity of some Moroccan plants against Geotrichum candidum, the causal agent of postharvest citrus sour rot. Crop Protection, vol. 35, p. 41-46. https://doi.org/10.1016/j.cropro.2011.12.016
Vermeulen, A., Marvig, C. L., Daelman, J., Xhaferi, R., Nielsen, D. S., Devlieghere, F. 2015. Strategies to increase the stability of intermediate moisture foods towards Zygosaccharomyces rouxii: The effect of temperature, ethanol, pH and water activity, with or without the influence of organic acids. Food Microbiology, vol. 45, p. 119-125. https://doi.org/10.1016/j.fm.2014.01.003
Verotta, L., Appendino, G., Jakupovic, J., Bombardelli, E. 2000. Hyperforin Analogues from St. John's Wort (Hypericum perforatum). Journal of Natural Products, vol. 63, no. 3, p. 412-415. https://doi.org/10.1021/np9903752
Wińska, K., Mączka, W., Łyczko, J., Grabarczyk, M., Czubaszek, A., Szumny, A. 2019. Essential Oils as Antimicrobial Agents - Myth or Real Alternative? Molecules, vol. 24, no. 11, 21 p. https://doi.org/10.3390/molecules24112130
Wu, F., Jin, Y., Xu, X., Yang, N. 2017. Electrofluidic pretreatment for enhancing essential oil extraction from citrus fruit peel waste. Journal of Cleaner Production, vol. 159, p. 85-94. https://doi.org/10.1016/j.jclepro.2017.05.010
Yeşilada, E., Honda, G., Sezik, E., Tabata, M., Fujita, T., Tanaka, T., Takeda, Y., Takaishi, Y. 1995. Traditional medicine in Turkey. V. Folk medicine in the inner Taurus Mountains. Journal of Ethnopharmacology, vol. 46, no. 3, p. 133-152. https://doi.org/10.1016/0378-8741(95)01241-5
Yu, D., Wang, J., Shao, X., Xu, F., Wang, H. 2015. Antifungal modes of action of tea tree oil and its two characteristic components against Botrytis cinerea. Journal of Applied Microbiology, vol. 119, no. 5, p. 1253-1262. https://doi.org/10.1111/jam.12939
Zhang, X., Guo, Y., Guo, L., Jiang, H., Ji, Q. 2018. In Vitro Evaluation of Antioxidant and Antimicrobial Activities of Melaleuca alternifolia Essential Oil. BioMed Research International, vol. 2018, 8 p. https://doi.org/10.1155/2018/2396109
How to Cite
Copyright (c) 2021 Potravinarstvo Slovak Journal of Food Sciences
This work is licensed under a Creative Commons Attribution 4.0 International License.Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).