molecules Review Essential Oils of Oregano: Biological Activity beyond Their Antimicrobial Properties Nayely Leyva-López, Erick P. Gutiérrez-Grijalva, Gabriela Vazquez-Olivo and J. Basilio Heredia * Centro de Investigación en Alimentación y Desarrollo A.C., Carretera a El Dorado km 5.5 Col. El Diez C.P., Culiacán, Sinaloa 80129, Mexico; [email protected] (N.L.-L.); [email protected] (E.P.G.-G.); [email protected] (G.V.-O.) * Correspondence: [email protected]; Tel.: +52-166-776-05536 Received: 25 May 2017; Accepted: 10 June 2017; Published: 14 June 2017 Abstract: Essential oils of oregano are widely recognized for their antimicrobial activity, as well as their antiviral and antifungal properties. Nevertheless, recent investigations have demonstrated that these compounds are also potent antioxidant, anti-inflammatory, antidiabetic and cancer suppressor agents. These properties of oregano essential oils are of potential interest to the food, cosmetic and pharmaceutical industries. The aim of this manuscript is to review the latest evidence regarding essential oils of oregano and their beneficial effects on health. Keywords: oregano species; terpenoids; antioxidant; anti-inflammatory; antidiabetic 1. Introduction According to the Encyclopedic Dictionary of Polymers, essential oils (EOs) are “volatile oils or essences derived from vegetation and characterized by distinctive odors and a substantial measure of resistance to hydrolysis” [1]. In general, EOs are complex mixtures of volatile compounds that are present in aromatic plants [2–4]. These compounds can be isolated from distinct anatomic parts of the plants mainly by distillation and pressing [5,6]. The main components in EOs are terpenes, but aldehydes, alcohols and esters are also present as minor components [7]. EOs are synthetized by plants in order to protect themselves from pests and microorganisms, to attract pollinating insects and for signaling processes, but recent studies have demonstrated that EOs might have beneficial effects on human health [6–12]. A great variety of plants are known and valued for their EO content. Oregano species are among the most widely used. Oregano is the name used to refer to a great variety of plants that share a particular flavor and odor [13]. At least 61 species and 17 genera belonging to six different botanical families are known as oregano. Verbenaceae and Lamiaceae are the most conspicuous families due to their economic importance. Within the Lamiaceae family are the plants belonging to the genera Origanum and Hedeoma; while the genera Lippia and Lantana belong to the Verbenaceae family. The other families are Rubiaceae, Apiaceae and Asteraceae [4,14]. Hedeoma patens, Lippia graveolens, Lippia palmeri, Lippia alba, Origanum dictamnus, Origanum hirtum, Origanum onites, Origanum vulgare are some examples of oregano species producing EOs [4,15–18]. EOs have great importance for the pharmaceutical, food and cosmetic industries [4]. Furthermore, there is evidence establishing that essential oils of oregano (EOO) might exert positive effects on human health. Therefore, the present manuscript will review recent investigations regarding the composition of essential oils of different oregano species and their biological activity, such as antioxidant, anti-inflammatory, anti-diabetic and antiproliferative properties. Molecules 2017, 22, 989; doi:10.3390/molecules22060989 www.mdpi.com/journal/molecules Molecules 2017, 22, 989 2 of 23 24 2. Essential Oils Composition of Oregano Species 2. Essential Oils Composition of Oregano Species The composition of EOO has been extensively studied. EOO are very complex mixtures of compounds,The composition in which the of EOOmajor has constituents been extensively are terpenes, studied. generally EOO mono- are very and complex sesquiterpenes. mixtures The of principalcompounds, terpenes in which identified the major in the constituents different species are terpenes, of oregano generally are carvacrol, mono- thymol, and sesquiterpenes. γ-terpinene γ andThe principalp-cymene; terpenes while terpinen-4-ol, identified in linalool, the different β-myrcene, species oftrans oregano-sabinene are carvacrol,hydrate, and thymol, β-caryophyllene-terpinene β β areand alsop-cymene; present while (Figure terpinen-4-ol, 1). The proportion linalool, of thes-myrcene,e and othertrans components-sabinene hydrate, in the EOO and within-caryophyllene the same speciesare also defines present the (Figure chemotype.1). The Generally, proportion the of chem theseotype and otheris named components after the major in the component EOO within of thethe EO,same e.g., species carvacrol, defines thymol, the chemotype. β-citronellol, Generally, 1,8-cineole, the chemotype etc. For exam is namedple, Lukas after theet al. major [19] componentdefined three of β chemotypesthe EO, e.g., of carvacrol, O. vulgare thymol, according-citronellol, to the proportion 1,8-cineole, of cy etc.myl-compounds, For example, Lukassabinyl-compounds et al. [19] defined and linalool/linalylthree chemotypes acetate of O. in vulgare extractsaccording of 502 individual to the proportion plants from of cymyl-compounds, 17 countries and sabinyl-compounds51 populations. On theand other linalool/linalyl hand, González-Fuentes acetate in extracts et al of. [20] 502 reported individual two plants chemotypes from 17 of countries L. graveolens and 51collected populations. from twoOn the different other hand, regions. Gonz Theseález-Fuentes authors found et al. [20 one] reported chemotype two rich chemotypes in carvacrol of L. and graveolens thymolcollected (wild type), from whiletwo different the other regions. one (a cultivated These authors type) found showed one less chemotype content of rich these in carvacrol terpenes. and thymol (wild type), while the other one (a cultivated type) showed less content of these terpenes. Figure 1. SomeSome of of the the major major constituents of the essential oils of oregano. It is is also also important important to to mention mention that that the the constituents constituents and and concentration concentration of the of thecompounds compounds of the of EOOthe EOO usually usually vary varydue to due a great to a greatdiversity diversity of factor ofs factors such as such species, as species, pests, soil pests, conditions, soil conditions, harvest season,harvest geographical season, geographical location, location,climatic climaticand growth and growthconditions conditions [21–29].[ 21The–29 drying]. The dryingmethod method of the oregano,of the oregano, the extraction the extraction technique technique and the andanatomical the anatomical part of the part plant of theused plant for extraction used for extraction also influence also theinfluence EO yield the EO and yield composition. and composition. For instance, For instance, Nova Novakk et al. et [30] al. [ 30studied] studied the the influence influence of of drying temperature on the contentcontent ofof EOsEOs inin O.O. vulgarevulgaressp. ssp. hirtumhirtum.. NaturalNatural ((≈≈2222 °C)◦C) and and thermostated thermostated drying (30, 40 40 and and 45 45 °C)◦C) were were the the temperatures temperatures evaluated. evaluated. It was It wasfound found that by that applying by applying 40 °C or 40 45◦C °C or during 45 ◦C theduring drying the dryingprocess process a higher a higheramount amount of EO can of EO becan obtained, be obtained, 4.96 and 4.96 5.09 and mL/100 5.09 mL/100 g, respectively, g, respectively, than whenthan when using using natural natural drying drying (4.46 (4.46mL/100 mL/100 g) or g)30 or °C 30 (4.16◦C (4.16 mL/100 mL/100 g). A g). significant A significant reduction reduction of the of contentthe content of EOO of EOO was was expected expected when when using using higher higher drying drying temperatures; temperatures; nevertheless, nevertheless, the the authors mentioned that they used relatively low temperatures to to avoid avoid the the loss of EOs. On On the the other other hand, hand, Figiel et al. [31] [31] evaluated evaluated the effe effectct of different different drying methods on the concentration of EOs of Polish O. vulgare plants. The methods tested were convective drying at 60 ◦°C,C, vacuum-microwave drying (360 W) and a combination combination of of convective convective pre-dryi pre-dryingng and vacuum-microwave finish-drying. finish-drying. The total of EOs concentration extracted from fresh oregano (33.0(33.0 g/kg)g/kg) decreased decreased significantly significantly regardless the method used. However, However, the loss of EOO was was less less wh whenen vacuum-microwave vacuum-microwave drying method was used (27.9 mg/kg), when when compared compared with with the convective (10.2 g/kg)g/kg) and and the the combined drying (13.1 g/kg).g/kg). The authors referred referred to to exposition exposition of of volatile volatile compou compoundsnds to to hot hot air air for for long long periods, periods, the the oxidation oxidation of theseof these compounds compounds due due to tooxygen oxygen presence presence and and the the inte interactionsractions of of volatiles volatiles with with water water as as the the main factors affectingaffecting thethe lossloss of of EOs EOs in inO. O. vulgare vulgare.. Authors Authors also also mentioned mentioned that that due due to concentration to concentration of EOs of EOs is affected by drying method so is the aroma quality of the dried sample. Therefore, vacuum- Molecules 2017, 22, 989 3 of 24 is affected by drying method so is the aroma quality of the dried sample. Therefore, vacuum-microwave drying is recommended in O. vulgare in order to preserve the characteristic fresh and green notes of this oregano. In a more recent study Calín-Sánchez et al. [32] evaluated the effect of the three drying methods (convective drying, vacuum-microwave drying and a combination of convective pre-drying and vacuum-microwave finish-drying) on volatile compounds of O. majorana. The total of EOs concentration extracted from fresh oregano (33.0 g/kg) decreased significantly regardless the method used. However, the loss of EOO was less when vacuum-microwave drying method was used (27.9 mg/kg) when compared with the convective (10.2 g/kg) and the combined drying (13.1 g/kg).