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Essential Oils as Antimicrobial Agents—Myth or Real Alternative?

Last updated: 04-06-2020

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Essential Oils as Antimicrobial Agents—Myth or Real Alternative?

PMID: 31195752
Essential Oils as Antimicrobial Agents—Myth or Real Alternative?
Katarzyna Wińska ,1,* Wanda Mączka ,1,* Jacek Łyczko ,1 Małgorzata Grabarczyk ,1 Anna Czubaszek ,2 and Antoni Szumny 1
Katarzyna Wińska
1Department of Chemistry, Wrocław University of Environmental and Life Sciences, Norwida 25, 50-375 Wrocław, Poland; lp.ude.rwpu@okzcyl.kecaj (J.Ł.); lp.teno@bargam (M.G.); lp.ude.rwpu@ynmuzs.inotna (A.S.)
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Wanda Mączka
1Department of Chemistry, Wrocław University of Environmental and Life Sciences, Norwida 25, 50-375 Wrocław, Poland; lp.ude.rwpu@okzcyl.kecaj (J.Ł.); lp.teno@bargam (M.G.); lp.ude.rwpu@ynmuzs.inotna (A.S.)
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Jacek Łyczko
1Department of Chemistry, Wrocław University of Environmental and Life Sciences, Norwida 25, 50-375 Wrocław, Poland; lp.ude.rwpu@okzcyl.kecaj (J.Ł.); lp.teno@bargam (M.G.); lp.ude.rwpu@ynmuzs.inotna (A.S.)
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Małgorzata Grabarczyk
1Department of Chemistry, Wrocław University of Environmental and Life Sciences, Norwida 25, 50-375 Wrocław, Poland; lp.ude.rwpu@okzcyl.kecaj (J.Ł.); lp.teno@bargam (M.G.); lp.ude.rwpu@ynmuzs.inotna (A.S.)
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Anna Czubaszek
2Department of Fermentation and Cereals Technology, Wrocław University of Environmental and Life Sciences, Chełmońskiego 37/41, 51-630 Wrocław, Poland; lp.ude.rwpu@kezsabuzc.anna
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Antoni Szumny
1Department of Chemistry, Wrocław University of Environmental and Life Sciences, Norwida 25, 50-375 Wrocław, Poland; lp.ude.rwpu@okzcyl.kecaj (J.Ł.); lp.teno@bargam (M.G.); lp.ude.rwpu@ynmuzs.inotna (A.S.)
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Francesca Mancianti, Academic Editor
Author information Article notes Copyright and License information Disclaimer
1Department of Chemistry, Wrocław University of Environmental and Life Sciences, Norwida 25, 50-375 Wrocław, Poland; lp.ude.rwpu@okzcyl.kecaj (J.Ł.); lp.teno@bargam (M.G.); lp.ude.rwpu@ynmuzs.inotna (A.S.)
2Department of Fermentation and Cereals Technology, Wrocław University of Environmental and Life Sciences, Chełmońskiego 37/41, 51-630 Wrocław, Poland; lp.ude.rwpu@kezsabuzc.anna
*Correspondence: lp.ude.rwpu@aksniw.anyzratak (K.W.); lp.ude.rwpu@akzcam.adnaw (W.M.); Tel.: +48-71-320-5213 (K.W. & W.M.)
Received 2019 Apr 30; Accepted 2019 Jun 4.
Copyright © 2019 by the authors.
Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/ ).
This article has been cited by other articles in PMC.
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Abstract
Herbs and the essential oils derived from them have been used from the beginning of human history for different purposes. Their beneficial properties have been applied to mask unpleasant odors, attract the attention of other people, add flavor and aroma properties to prepared dishes, perfumes, and cosmetics, etc. Herbs and essential oils (EOs) have also been used in medicine because of their biological properties, such as larvicidal action, analgesic and anti-inflammatory properties, antioxidant, fungicide, and antitumor activities, and many more. Many EOs exhibit antimicrobial properties, which is extremely important in fields of science and industry, such as medicine, agriculture, or cosmetology. Among the 250 EOs which are commercially available, about a dozen possess high antimicrobial potential. According to available papers and patents, EOs seem to be a potential alternative to synthetic compounds, especially because of the resistance that has been increasingly developed by pathogenic microorganisms. In this review we summarize the latest research studies about the most-active EOs that are known and used because of their antimicrobial properties. Finally, it is noteworthy that the antimicrobial activities of EOs are not preeminent for all strains. Further investigations should, thus, focus on targeting EOs and microorganisms.
Keywords: essential oils, antibacterial activity, antifungal activity, lavender oil, thyme oil, peppermint oil, cajuput oil, cinnamon oil, eucalyptus oil, clove oil, sage oil, tea tree oil
1. Introduction
Essential oils (EOs) are defined as volatile secondary metabolites of plants that give the plant a distinctive smell, taste, or both. EOs are produced by more than 17,500 species of plants from many angiosperm families, e.g., Lamiaceae, Rutaceae, Myrtaceae, Zingiberaceae, and Asteraceae, but only about 300 of them are commercialized [ 1 ]. Compounds included in the EOs are synthesized in the cytoplasm and plastids of plant cells through the pathways of malonic acid, mevalonic acid, and methyl-d-erythritol-4-phosphate (MEP). They are produced and stored in complex secretory structures, such as glands, secretory cavities, and resin conduits, and are present as drops of liquid in the leaves, stems, flowers and fruits, bark, and roots of plants. Despite containing two or three main components at a level of 20–70%, EOs are very complex mixtures of mainly terpenes, terpenoids, and phenylpropanoids. They may also contain many other compounds, such as fatty acids, oxides, and sulfur derivatives [ 2 ].
EOs are usually obtained as a result of hydrodistillation, steam distillation, dry distillation, or the mechanical cold pressing of plants. At the laboratory scale, the classical method is based on the use of the Clevenger steam distillation apparatus, discovered in 1928. Due to several disadvantages (i.e., placement of valve, fragility), this apparatus was modified by Jakub Deryng in 1951 [ 3 ] and it is widely used in Central European countries. Modifications of the simultaneous distillation-extraction (SDE) equipment were described in the manuscript of Arora et al. [ 4 ]. The effectiveness of these modifications was described in detail by Baj et al. [ 5 ]. At the laboratory scale, modern methods also include processes supported by microwaves and extraction in supercritical fluids. EOs can also be isolated using fermentation, crushing, extraction, or hydrolysis. However, depending on the chosen method, the chemical composition of the obtained EO can unfortunately be different.
Humans have used EOs for thousands of years, not only as ingredients of perfumes or as seasonings for the aromatization of food, but also in folk medicine, because of their many different biological properties, including antimicrobial properties [ 6 ]. The antimicrobial qualities are essential in managing the rapidly growing issue of drug-resistant microorganisms. In 2016, about 6 million people died globally due to infections of the upper respiratory tract, tuberculosis, or diarrheal diseases. At the same time, the number of strains of microorganisms resistant to existing antibiotics is constantly increasing. Patients with infections caused by drug-resistant bacteria are, thus, exposed to an increased risk of worse clinical results and even death. Such patients also consume more healthcare resources than patients infected with non-resistant strains of the same bacteria. According to the WHO report on drug resistance, the most serious problems include the resistance of Klebsiella pneumoniae to third-generation cephalosporins and carbapenem, Escherichia coli to third-generation cephalosporins and fluoroquinolone, Staphylococcus aureus to methicillin, Streptococcus pneumoniae to penicillin, and Salmonella sp. to fluoroquinolones. Among the fungal infections, the most common problem is candidiasis caused mainly by Candida albicans and less often by C. glabrata and C. parapsilosis, with more than 20 species of Candida that can cause human infection [ 7 ]. Other examples of common fungal infections are aspergillosis, histoplasmosis, and skin mycosis (commonly known as ringworm) [ 8 ].
In food production, inhibiting the growth of microorganisms through the use of socially acceptable preservatives is a serious problem. Society’s reluctance to use antibiotics and synthetic preservatives, such as benzoic acid, sorbic acid, lactic acid, propionic acid, acetic acid, and its derivatives, parabens or inorganic sulfites, nitrites, and nitrates, necessitates finding alternative solutions [ 9 ]. This may be an application for EOs, especially since chemical preservatives cannot eliminate several pathogenic bacteria, such as Listeria monocytogenes, in food products or delay the growth of spoilage microorganisms. In addition, natural products are inherently better tolerated in the human body, usually with fewer side effects [ 10 ].
2. Description of EOs
In the following section, the antimicrobial activity of selected EOs from above-mentioned aromatic and medicinal plants is discussed. The table of selected oils and strains of microorganisms they are active against is part of the supplementary information ( Table S2 ). Additionally, in the supplementary information, we have included GC-MS chromatograms ( Figures S1–S9 ) and a summary table of ingredients discussed in the study of oils ( Table S1 ).
2.1. Lavender EO
2.1.1. The Sources of Lavender EO
Lavender is one of the most commonly cultivated plants in the world on account of its EO properties. The main cultivation areas of lavender are in Europe, the Middle East, Asia, and North Africa [ 11 ]. Lavender belongs to the Lamiaceae family, formally called Labiatea. The genus Lavandula includes about 40 different species and hundreds of varieties and its hybrids. The variability of the composition between different species is described in the review article written by Aprotosoaie et al. [ 12 ]. The three species most commonly grown types are: L. angustifolia Mill. (narrow-leaved lavender, usually medical), L. stoechas (French lavender), L. latifolia, and their hybrids. L. angustifolia Mill. (formerly synonymous with L. officinalis L. or L. vera DC), is a species with the most significant industrial importance because of the EO derived from it. EO of lavender has unique biological activity, not only antimicrobial properties [ 13 ]. World trade in lavender EO is estimated at 50 million dollars [ 14 ].
2.1.2. Chemical Composition of Lavender EO
Lavender EO is a colorless or pale yellow liquid with a characteristic odor. The chemical composition is well known, with detailed data specified in the European Pharmacopoeia 9, Polish Pharmacopoeia VIII, and PNISO (Polish ISO standard) 3515: 2004. Lavender EO is obtained after distillation with water vapor of fresh or dried tips of blooming plants. The main components are R enantiomers of linalool (20–45%) and linalyl acetate (25 to 46%). The high content of these ingredients determines the quality of the oil. The content of other ingredients should be in the following ranges: limonene (>1.0%), eucalyptol (1.2%), terpin-4-ol (0.1–6.0) %), lawandulol ( β-thujone > 1,8-cineneol [ 111 ].
2.8.3. Antimicrobial Activity of Sage Oil
The use of sage EO in phytopharmacy has recently been described in two review articles [ 9 , 103 ]. Both the plant raw material as well as the extracts and EO obtained from sage are used as herbal medicines with mainly sanitization and antiseptic effects. EO of Salvia officinalis was active against severe acute respiratory coronavirus SARS-CoV (RNA virus), which was obtained from the sputum of a patient hospitalized with a diagnosis of SARS (severe acute respiratory syndrome) in Frankfurt University Hospital. It is worth noting that the overriding clinical feature of SARS is the rapidity with which many patients develop symptoms of acute respiratory distress syndrome (ARDS). Essential oil was weakly active at IC50 = 870 mg/ mL [ 112 ].
Sage EO has antibacterial activity against Escherichia coli, Bacillus subtilis [ 113 ], Salmonella typhi, S. enteritidis, Shigella sonei [ 114 ], Staphylococcus aureus [ 115 ], S. epidermidis, S. mutans [ 116 ], and Shigella sonei [ 9 ]. It is active against Gram-positive and Gram-negative bacteria [ 117 ]. The antimicrobial activity of the sage EO is attributed mainly to the presence of camphor, thujone, and 1,8-cineole [ 103 ].
Moreover, plants of the genus Salvia are used as a component of herbal teas and as flavoring for food. At the same time, the number of microorganisms developing tolerance to existing preservative techniques is constantly growing, and the unwillingness to use synthetic preservatives and antibiotics is prevalent. Therefore, the interest for food processors and consumers in antibacterial preservatives of plant origin, including the possibility of using EOs, is increasing [ 9 ]. For example, sage EO at a concentration of 2.0% has a bacteriostatic effect on the strains of Salmonella anatum [ 118 ] and Salmonella enteritidis growing in minced meat. Unfortunately, such a high concentration of essential oil had a negative effect on taste. This problem was solved by using a lower concentration of the sage EO and the addition of sodium chloride, and the products were stored at a low temperature. However, with other meat products, there may be a problem with the formulation of the finished product, because both the NaCl concentration and the sage EO can negatively affect the taste sensation [ 119 ].
Because of the observed high vapor permeability of sage EO, it can be used as a disinfectant against airborne microorganisms, such as Bacillus, Pseudomonas, Enterococcus hirae, Staphylococcus aureus, Aeromonas hydrophila, Aeromonas sobria, and Klebsiella oxytoca [ 120 , 121 ]. Sage EO is also active against yeast Candida albicans [ 115 ], Candida glabrata, Candida krusei and Candida parapsilosis [ 103 ] and fungal strains, such as Aspergillus carbonarius [ 121 , 122 ], Aspergillus niger [ 123 ], Ashbiya gossypii, Rhizopus oryzae, Trichoderma reesei [ 124 ], Alternaria solani, Ascochyta rabies, Botrytis cinerea, Monilia laxa, Penicllum italicum, and Rhizoctonia solani [ 125 ].
2.9. Tea Tree EO
2.9.1. Source
Tea tree EO is a product of water vapor distillation of leaves and top twigs of Melaluleca alternifolia Maiden and Betch and other Melaleuca species (M. linariifolia Smith, M. dissitiflora F. Mueller) [ 33 ]. According to research [ 126 ] aimed at standardizing the raw material for the production of essential oil for pharmaceutical purposes, Melaleuca alterniforia is a shrub with a height of about 7 m, characterized by stratified and flaky bark and oblong, pointed leaves with a characteristic pattern.
2.9.2. Chemical Composition of Tea Tree EO
The main components of tea tree EO are terpine-4-ol (≥30%), teripene (about 20%), α-terpinene (about 8%), ρ-cymene (about 8%), α-pinene (about 3%), terpinolene (about 3%), and 1,8-cineol (≤15%) [ 127 ]. However, it should be noted that individual Melaleuca species have a very diverse content. As shown by Amri et al. [ 128 ], cultivars growing in Tunisia (M. armillaris, M. acuminata, M. styphelioides) may contain only traces of terpinene-4-ol, γ-terpinene, or ρ-cymene, in favor of trans-pinocarveol (25.1% M. acuminata), eugenol methyl (91.1% M. styphelioides), or cis-calamene (19% of M. armillaris). The analyses of more than 800 samples of tea tree EO has identified over 100 of its components.
2.9.3. Antimicrobial Activity of Tea Tree EO
So far, the most promising tea tree EO in terms of antimicrobial properties is derived from a chemotype characterized by 30–40% terpinen-4-ol content [ 8 ]. EO was active against Herpes simplex virus type 1 in vitro. IC50 of this EO was determined as 2.0 µg/mL. EO was able to suppress viral multiplication by >96% [ 8 , 34 ]. Additionally, a randomized, placebo-controlled, investigator-blinded protocol was used to evaluate the efficacy of tea tree essential oil (6% tea tree EO gel) in the treatment of recurrent herpes labialis. The median time of reepithelization after treatment with this EO was 9 days compared to 12.5 days after placebo, indicating some benefit from tea tree EO treatment [ 129 ]. Meanwhile, the antibacterial activity has been determined to a much greater extent. The tea tree EO inhibited the growth of S. aureus and E. coli at a concentration of 0.78% and inhibited the adhesion of S. mutans [ 130 ] and the development of Listeria monocytogenes ATCC 7644 (MIC = 0.10 μL/g) in ground beef [ 131 ].
Tea tree EO, thanks to its antimicrobial properties, has been used in products for oral hygiene and dermatological applications [ 129 , 132 ]. Furthermore, Graziano et al. [ 126 ] determined that tea tree EO reduces the growth of bacteria responsible for halitosis—Porphyromonas gingivalis (MIC and MBC = 0.007%) and Porphyromonas endodontalis (MIC = 0.007% and MBC = 0.5%). The most important element of the study was the finding that tea tree EO not only inhibits the growth of bacteria responsible for halitosis leading to personal and social discomfort, but also limits the production of volatile sulfur compounds—H2S by P. gingivalis and CH3SH by P. endodontalis. Moreover, tea tree EO has shown an inhibitory effect against Candida albicans. For good therapeutic activity, the tea tree EO must contain terpineol at a minimum of 30% and a maximum of 15% cineol to simultaneously achieve very low skin irritation [ 129 ]. The aim of the study conducted by Mertas et al. [ 131 ] was the reduction of yeast resistance to the drug fluconazole due to the simultaneous use of tea tree EO or its main component (terpinen-4-ol). The authors indicated that as many as 62.5% of the 32 resistant strains became susceptible to the drug after 24 h exposure to the essential oil or its component. The minimum fluconazole concentration inhibiting fungal growth also decreased significantly (from 244.0 μg/mL to 38.46 μg/mL), along with its minimum fungicidal concentration (from 254.47 μg/mL to 66.62 μg/mL).
Recently [ 8 ], the antimicrobial properties of commercially available tea tree EOs were investigated. Of the 10 EOs, 5 were active. Identified components of the tea tree EO reduced the survival of the bacteria in the Pseudomonas aeruginosa biofilm and caused oxidative damage in Candida glabrata. On the other hand, EO of Melaleuca alternifolia) had only marginal antifungal activity against Aspergillus niger (MIC = 625 µg/mL), attributed to its active components terpinen-4-ol and α-terpineol [ 133 ]. Another example is Penicillium expansum, which is a cosmopolitan pathogen that can cause damage to fruit crops. Germination of this fungus was completely inhibited at the concentration of tea tree EO 250 µg/mL. Tea tree EO caused damage to the plasma membrane, leading to DNA, protein, lipid, and glucose leakage [ 134 ]. In turn, the effects of tea tree EO on mitochondrial morphology and function in a culture of Botrytis cinerea was investigated. This EO at a concentration of 2 mL/L severely damaged mitochondria, resulting in matrix loss and increased mitochondrial irregularity. The next consequence of mitochondrial damage was the disruption of the tricarboxylic acid cycle and the accumulation of reactive oxygen species [ 135 ].
3. Conclusions
Contrary to common opinion, limited EOs possess demonstrated potential as antimicrobial agents. It should be emphasized that although the antimicrobial activity is well established, the real effect is significantly weaker compared to synthetic compounds (including antibiotics). Gram-positive bacteria seem to be much more susceptible to essential oil than Gram-negative organisms. According to available data, the activity is usually correlated with phenolic, aromatic, or alcohol groups. Due to their high volatility, the effective time of action is limited, and features such as encapsulation could be changed. On the other hand, low toxicity level, as well as their natural origin, makes them an attractive alternative in both the food as well as in cosmetic industries. Several practical application could be implemented in these industries. In summary, it should be underlined that the use of EO in microbial stabilization is possible, but all cases must be individually examined.
Supplementary Materials
The following are available online. Figure S1. The chromatogram of lavender oil; Figure S2. The chromatogram of thyme oil; Figure S3. The chromatogram of peppermint oil; Figure S4. The chromatogram of cajeput oil; Figure S5. The chromatogram of cinnamon oil; Figure S6. The chromatogram of eucalyptus oil; Figure S7. The chromatogram of clove oil; Figure S8. The chromatogram of sage oil; Figure S9. The chromatogram of tea tree oil; Table S1. Chemical composition of Eos; Table S2: The antimicrobiological activity of EOs, Materials and Methods.
Click here for additional data file. (794K, pdf)
Author Contributions
K.W., W.M. and J.Ł., writing—original draft preparation; M.G., A.S. and A.C., writing—review; A.S., K.W., W.M., J.Ł., A.C., GC-MS analysis.
Funding
This research received no external funding.
Conflicts of Interest
The authors declare no conflict of interest.
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