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Biological Properties and Prospects for the Application of Eugenol—A Review

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Biological Properties and Prospects for the Application of Eugenol—A Review International Journal of Molecular Sciences Review Biological Properties and Prospects for the Application of Eugenol—A Review Magdalena Ulanowska and Beata Olas * Department of General Biochemistry, University of Lodz, Pomorska 141/3, 90-236 Lodz, Poland; [email protected] * Correspondence: [email protected]; Tel.: +48-42-6354484 Abstract: Eugenol is a phenolic aromatic compound obtained mainly from clove oil. Due to its known antibacterial, antiviral, antifungal, anticancer, anti-inflammatory and antioxidant properties, it has long been used in various areas, such as cosmetology, medicine, and pharmacology. However, high concentrations can be toxic. A dose of 2.5 mg/kg body weight is regarded as safe. This paper reviews the current state of knowledge regarding the activities and application of eugenol and its derivatives and recent research of these compounds. This review is based on information concerning eugenol characteristics and recent research from articles in PubMed. Eugenol remains of great interest to researchers, since its multidirectional action allows it to be a potential component of drugs and other products with therapeutic potential against a range of diseases. Keywords: eugenol; clove oil; antibacterial; antifungal; antioxidant 1. Introduction Eugenol is a well-known and well-studied compound. It was first isolated in 1929 as a volatile compound from Eugenia caryophyllata, and commercial production began in the USA in 1940 [1,2]. Citation: Ulanowska, M.; Olas, B. Due to its numerous properties, eugenol has found a wide range of uses in many Biological Properties and Prospects areas of life. In addition, because of the growing interest in unconventional, traditional for the Application of Eugenol—A Review. Int. J. Mol. Sci. 2021, 22, 3671. medicines that contain natural ingredients, it remains an important object of scientific https://doi.org/10.3390/ijms22073671 research as a potential component of various medicinal products, including those intended for treating human lung cancer [3,4]. Isoeugenol derivatives have become a popular subject Received: 2 March 2021 of research due to their fungicidal and insecticidal properties, because they exhibit greater Accepted: 25 March 2021 antimicrobial activity than eugenol [2]. This study reviews the current state of knowledge Published: 1 April 2021 regarding the multidirectional action and application of eugenol and its derivatives and recent research into these compounds. Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in 2. Characteristics of Eugenol published maps and institutional affil- Eugenol (C10H12O2; phenylpropanoid, Figure1) is an aromatic compound belong- iations. ing to the group of phenols. It is commonly obtained from the natural essential oils of plants from the Lamiaceae, Lauraceae, Myrtaceae and Myristicaceae families, and is the most important component of clove oil (Syzygium aromaticum). Although it is known to oc- cur in various concentrations depending on the species (Table1), the richest source is Copyright: © 2021 by the authors. S. aromaticum, where it constitutes between 9381.7 mg and 14,650 mg per 100 g of fresh Licensee MDPI, Basel, Switzerland. plant material and is primarily responsible for its characteristic aroma [2,5–8]. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Int. J. Mol. Sci. 2021, 22, 3671. https://doi.org/10.3390/ijms22073671 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, 3671 2 of 13 Figure 1. Chemical structure of eugenol. Eugenol is a clear to pale yellow liquid with an oily consistency and a spicy aroma. It is sparingly soluble in water and well soluble in organic solvents. Eugenol can be produced synthetically in two ways, one of which involves the allylation of guaiacol with allyl chloride. The biotechnological method is based on the biotransformation of a wide range of microorganisms, such as Corynebacterium spp., Streptomyces spp., and Escherichia coli [2,6–8]. Eugenol has low chemical stability and is sensitive to oxidation and various chemical interactions. When orally administered, it is rapidly absorbed by various organs and metabolized in the liver. Therefore, encapsulation of eugenol seems to be the best solution to prevent early absorption, improve its water solubility, and, thus, increase its activity (e.g., it has been reported that the amount of eugenol delivered increases at least sixfold in infected cells when delivered as solid lipid nanoparticles [2]). The eugenol inclusion complexes may have enhanced thermal stability and, as a result, provide slow release of eugenol. These may be microemulsions containing eugenol prepared by simply dissolving the eugenol (0.75–1.5% w/w) essential oil in micelles of surfactants [2,9]. Table 1. Occurrence of eugenol and its concentration in particular parts of plants [10]. Plant Part Concentration (mg/g) Flower Clove, Clovetree 1809 Leaf, stem Clover pepper Fruit 36 Betel Pepper Leaf 17.85 Carrot Seed 7 Tulsi Leaf 4.2–4.97 Ceylon Cinnamon, Cinnamon Bark 3.52 Turmeric Leaf, essential oil 2.1 Bay, Bay Laurel Leaf 1.34 Chinese Ginger Rhizome 0.4 Nutmeg Seed 0.32 Small-Flowered Oregano Shoot 0.055–0.125 Eugenol has demonstrated various antioxidant, analgesic, antimutagenic, anti-platelet, antiallergic, anti-swelling, and anti-inflammatory properties. It has also displayed antimi- crobial effects against many human pathogens, including a wide group of Gram-positive and Gram-negative bacteria and fungi and a number of parasites, including Giardia lamblia, Fasciola gigantica, and Haemonchus contortus. Furthermore, eugenol can protect against carbon tetrachloride (CCl4)-induced hepatotoxicity [2,4,5,7,11]. Int. J. Mol. Sci. 2021, 22, 3671 3 of 13 Despite many important properties, eugenol can cause irritation and allergy. There have been reports of allergic contact dermatitis, presenting as hand eczema in dentistry workers like dentists or dental assistants (due to the use of eugenol in dentistry), as well as allergic contact gingivitis or burning mouth syndrome [12]. 3. Antioxidant Activity Eugenol is a popular antioxidant and monoamine oxidase (MAO) inhibitor, and it is also known to exhibit neuroprotective properties [13]. Eugenol is known to scavenge free radicals, inhibit the generation of reactive oxygen species, prevent the production of reactive forms of nitrogen, increase cyto-antioxidant potential, and protect the function of microbial DNA and proteins. Eugenol can also help repair oxidative damage, eliminate damaged molecules, and prevent mutations that could develop into cancer [1,7,14]. The antioxidative potential of eugenol has been attributed to its structure, which allows it to fix phenoxy radicals by receiving donated hydrogen atoms [15]. Both clove oil and eugenol demonstrate strong antioxidant potential. Pérez-Rosés et al. [16] found both to have a strong DPPH (2,2-diphenyl-1-picrylhydrazyl) radical scavenging effect (half maximal inhibitory concentration (IC50) = 13.2 µg/mL for clove oil; 11.7 µg/mL for eugenol) and to inhibit reactive oxygen species (ROS) production in human neutrophils stimulated by phorbol 12-myristate 13-acetate (IC50 = 7.5 µg/mL for clove oil; 1.6 µg/mL for eugenol) or H2O2 (IC50 = 22.6 µg/mL for clove oil; 27.1 µg/mL for eugenol). They also inhibit the production of nitric oxide (IC50 = 39.8 µg/mL for clove oil; 19.0 µg/mL for eugenol) and demonstrate high myeloperoxidase (MPO) inhibition in human leukocytes (IC50 = 16.3 µg/mL for clove oil; 19.2 µg/mL for eugenol). While eugenol is known to have antioxidant and anti-inflammatory properties at low doses, a pro-oxidative effect can occur at higher concentrations, resulting in the formation of free radicals. In addition, many studies have shown that the administration of high concentrations of clove oil can increase the number of DNA breaks in normal human fibroblast cells [1,8,10,17]. 4. Antimicrobial Activity of Eugenol Eugenol has demonstrated antibacterial properties against many species, such as Staphylococcus aureus, Pseudomonas aeruginosa, and Escherichia coli, and this potential has been attributed to the free OH group in its structure. Against Gram-negative bacteria, eugenol is believed to act by damaging the cytoplasmic membrane; being a hydrophobic molecule, it can easily penetrate the lipopolysaccharide cell membrane and enter the cytoplasm. Once present in the cell, it can cause alterations to the cell structure, resulting in the leakage of intracellular components. In Enterobacter aerogenes, it has been proposed that the hydroxyl group on eugenol in- hibits the action of protease, histidine carboxylase, and amylase by binding to them ([2,18]). Similarly, eugenol has been found to potentially inhibit the activity of membrane-bound ATPase in Escherichia coli and Listeria monocytogenes [19]. It has also demonstrated synergistic effects with conventional antimicrobials [9]. It is further believed that eugenol is capable of producing intracellular reactive oxygen species (ROS), which can cause cell death by inhibiting cell growth, disrupting the cell membrane, and damaging DNA [20]. Eugenol was found to inhibit the growth of human isolates of Streptococcus agalactiae (planktonic GBS—group B streptococci strain), including those resistant to erythromycin and clindamycin [21]. After a five-hour incubation with 0.125% to 0.5% eugenol, the GBS planktonic cells demonstrated leakage
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