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. 2018 Feb 2;7(2):19. doi: 10.3390/foods7020019

Characterization of Essential Oils Obtained from Abruzzo Autochthonous Plants: Antioxidant and Antimicrobial Activities Assessment for Food Application

Marika Pellegrini 1, Antonella Ricci 1,*, Annalisa Serio 1, Clemencia Chaves-López 1, Giovanni Mazzarrino 1, Serena D’Amato 1, Claudio Lo Sterzo 1, Antonello Paparella 1
PMCID: PMC5848123  PMID: 29393893

Abstract

In the present study, the essential oils (EOs) of some officinal plants from Abruzzo territory (Italy) were evaluated for their antimicrobial and antioxidant activities and their volatile fraction chemical characterization. The EOs were extracted from Rosmarinus officinalis, Origanum vulgare, Salvia officinalis, Mentha piperita, Allium sativum, Foeniculum vulgare, Satureja montana, Thymus vulgaris and Coriandrum sativum seeds. The antimicrobial activity was screened against thirteen Gram-positive and Gram-negative strains to determine the Minimal Inhibitory Concentration (MIC). The total phenolic content (TPC) and the antioxidant capacity (AOC) were assessed by means of Folin-Ciocâlteu method, and Trolox Equivalent Antioxidant Capacity with 2,2′-azinobis-(3-ethylbenzothiazoline-6-sulfonic acid (TEAC/ABTS), Ferric Reducing Antioxidant Power (FRAP) and 2,2-diphenyl-1-picrylhydrazyl (DPPH) assays respectively. Among the nine EOs tested, T. vulgaris, S. montana, O. vulgare and C. sativum EOs showed MIC values ranging from 0.625 to 5 μL/mL. The AOC and TPC results for these species were also interesting. The major components for these EOs were thymol for T. vulgaris (44%) and O. vulgare (40%), linalool (77%) for C. sativum, and carvacrol for S. montana (54%). The results allowed the study to establish that these EOs are good candidates for potential application as biopreservatives in foods and/or food manufacture environments.

Keywords: essential oils, antimicrobial, antioxidant, GC-MS

1. Introduction

Food spoilage can be defined as the alteration of a product due to microbial, chemical, or physical mechanisms that lead a food to become undesirable or unacceptable for human consumption [1]. In food products manufacture, many effective preservation strategies are applied against food spoilage, involving mainly the employment of synthetic preservatives. However, the increasing negative consumer perception of synthetic additives and the worldwide growing problem of allergies, is causing the food industry to search for more effective preservation strategies [2].

An alternative strategy to synthetic chemical preservatives is represented by the employment of essential oils (EOs). Commonly employed in foods as aromatizing and flavoring agents [2], these plant volatile fractions can be exploited by the food industry for their antimicrobial [3,4] and antioxidant [5] properties. EOs, in fact, possess the ability to permeabilize the membrane of microorganisms, with consequent loss of vital intracellular constituents and interruption of the cellular metabolism and enzyme kinetics [6]. In addition, terpenes and terpenoids, alkaloids and phenolic compounds present in these volatile fractions are recognized antioxidant substances [7,8,9].

According to European Pharmacopeia, the EOs can be obtained by steam distillation or by hydrodistillation [10] and their yield and composition are influenced by the presence of several factors, such as location, climate, plant species, methodology and experimental procedures [11,12].

In the Italian territory, Abruzzo is one of the central area regions characterized by a multitude of environments and microclimates and with the richest flora of Italy and the Mediterranean basin [13]. In the Abruzzo territory, different plant species are cultivated and exploited for their therapeutic and alimentary properties [14]; among them, Rosmarinus officinalis, Origanum vulgare, Salvia officinalis, Mentha piperita, Allium sativum, Foeniculum vulgare, Satureja montana, Thymus vulgaris, and Coriandrum sativum, are the aromatic plants commonly employed in the Mediterranean diet [15,16,17].

In scientific literature, different data that showed the antimicrobial and antioxidant potentials of the EOs recovered from these vegetal species are reported [18,19,20,21]. However, limited data are available for the EOs obtained from these Abruzzo plant species. In this perspective, the aims of the study were the extraction and the Gas Chromatography-Mass Spectrometry (GC-MS) characterization of the EOs from Abruzzo officinal plants and assessment of their antimicrobial properties against several food-borne strains, as well as their antioxidant capacities and total phenolic contents.

2. Materials and Methods

2.1. Plant Material

The matrices were obtained from Abruzzo territory farmers. The cultures were obtained with organic agriculture and after the harvesting, the matrices were dried on fields and stored at room temperature in dry and dark conditions for few days. The matrices were then transferred in the laboratory for extractions and analyses. Regarding A. sativum, after the harvesting, the bulbs were transferred in the laboratory, cleaned and the resultant cloves were vacuum-packed and refrigerated until extraction and analyses.

2.2. Essential Oils Extraction

Essential oils were extracted from the matrices by means of an E0105 12 lt PLUS Essential Oils Extractor (Albrigi Luigi Srl, Verona, Italy). For all plant materials, after two hours of distillation, no significant volume increase was observed in the collector tube, thus all matrices were subjected to 2 h steam distillation, except for garlic cloves which were subjected to 2 h hydrodistillation. After extraction, the EOs were transferred to an amber glass vial with anhydrous sodium sulfate (Sigma Aldrich, Saint Louis, MO, USA), conditioned with argon and sealed. Each matrix extraction was conducted in triplicate. The collected EOs were stored under refrigeration at 4 °C.

2.3. Chemical Compositions of EOs

The GC-MS analyses of the EOs were carried out by a Clarus 580 GC (PerkinElmer, Waltham, MA, USA) coupled to a Clarus GC/MS SQ (PerkinElmer), in full scan mode (50 to 600 amu). The identifications of the volatile compounds were obtained matching the mass spectra with the NIST Mass Spectral Library 2.0 (NIST, Gaithersburg, MD, USA) and confirmed by calculating the retention index, as proposed by Lee et al. [22], referred to a series of n-hydrocarbons (C8–C40 n-alkanes, Sigma Aldrich), compared with those present in the NIST Chemistry WebBook (http://webbook.nist.gov/chemistry/). The semi-quantitative results were calculated by means of the Turbomass 6.1.0.1963 software (PerkinElmer).

The GC apparatus was equipped with a fused silica Rxi-5ms column (30 m × 250 μm × 0.25 μm Restek, Milan, Italy). For all the EOs, excepting A. sativum, the oven temperature program started from 45 °C (holding 10 min) and ramped at a rate of 2.5 °C/min to 180 °C (holding 5 min); for A. sativum EOs, the oven temperature program started from 50 °C (holding 1 min), ramped at a rate of 5 °C/min to 145 °C (holding 15 min), ramped at a rate of 7 °C/min to 175 °C and then ramped at a rate of 4 °C/min to 250 °C (holding 15 min); the carrier gas was helium at flow 1 mL/min; the injector temperature and the transfer line temperature were set at 250 °C. A 1% v/v solution of the EOs sample in hexane was prepared and 1 µL was injected in a splitless mode.

2.4. Antioxidant Capacity and Total Phenolic Content

To assess the antioxidant capacity and total phenolic content, 0.2–2 mg/mL methanolic solutions of each EO were subjected to the different spectrophotometric assays carried out by a Lambda Bio 20 ultraviolet-visible (UV/vis) spectrophotometer (PerkinElmer). The different assays conditions were presented below.

2.4.1. Trolox Equivalent Antioxidant Capacity with 2,2′-azinobis-(3-ethylbenzothiazoline-6-sulfonic acid (TEAC/ABTS) Assay

The TEAC/ABTS assay was determined as described by Masaldan et al. [23]. The TEAC/ABTS results of the samples were estimated in terms of mmol Trolox equivalent (TE)/g EO as the mean of three replicates.

2.4.2. Ferric Reducing Antioxidant Power (FRAP) Assay

The FRAP was determined by using the potassium ferricyanide-ferric chloride method described by Oyaizu [24]. The FRAP of the samples was estimated in terms of mg Trolox equivalent (TE)/g EO as the mean of three replicates.

2.4.3. 2,2-diphenyl-1-picrylhydrazyl (DPPH) Assay

The radical-scavenging activity of the EOs methanolic solutions was measured according to the method described by Brand-Williams et al. [25]. The DPPH results were expressed in terms of µg Trolox equivalent (TE)/g EO as the mean of three replicates.

2.4.4. Total Phenolic Content (TPC)

TPC was determined by the Folin-Ciocâlteu method described by Lateef Gharib & Teixeira da Silva [26]. The TPC results were expressed in terms of mg Gallic acid equivalents (GAE)/g EO as the mean of three replicates.

2.5. Antimicrobial Activity

2.5.1. Microbial Strains and Growth Conditions

Thirteen strains, listed in Table 1, and belonging to the Faculty of Bioscience and Technology for Food, Agriculture and Environment collection, were employed in the assessment of antimicrobial activity. The strains were stored at −80 °C in cryovials, containing anti-freezing agent (glycerol 20% v/v Sigma) and periodically confirmed by means of plate counts. Before each trial, bacterial strains were cultured overnight in Tryptone Soy agar medium (TSA, Oxoid Thermofisher, Rodano, Italy); after 24–48 h, the cells were inoculated into Tryptone Soy broth (TSB, Oxoid Thermofisher) and incubated to obtain a working fresh culture (early stationary phase). Fresh cultures were collected by centrifugation at 1300 rpm (Eppendorf-Centrifuge 5415D, Hamburg, Germany) for 5 min and washed for three times with phosphate buffer saline (50 mM pH 7.0). Inocula were standardized at about 5 × 105 CFU/mL, by means of Lambda Bio 20 spectrophotometer (PerkinElmer). Strains origin and incubation conditions were also presented in Table 1.

Table 1.

Strains employed for the trial and culture and standardization conditions.

Strains Origin Incubation Temperature (°C) Incubation Time (h)
Pseudomonas fluorescens P34 Dairy products 28 24
Brochothrix thermosphacta B2 Poultry meat 30 48
Brochothrix thermosphacta B1 Poultry meat 30 48
Salmonella Enteritidis S2 Meat 37 24
Salmonella Typhimurium S4 Meat 37 24
Enterococcus faecium P14 Fish 30 48
Enterococcus faecium ATCC 19434 Type strain 30 48
Listeria monocytogenes LM 4 Meat products 37 48
Listeria monocytogenes ATCC 19144 Type strain 37 48
Listeria monocytogenes ATCC 7644 Type strain 37 48
Staphylococcus aureus STA 32 Dairy products 37 48
Staphylococcus aureus STA 47 Dairy products 37 48
Staphylococcus aureus STA 39 Dairy products 37 48
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2.5.2. Determination of Minimal Inhibitory Concentration

The EOs were investigated for their Minimal Inhibitory Concentration (MIC) values according to the microdilution method, as described by Clinical and Laboratory Standards Institute (CLSI) guidelines [27]. The EOs were dissolved in PBS (Phosphate Buffer Saline) 50 mM pH 7.0 and Tween 80 (1%) to reach the initial concentration of 4.0%; working emulsions were obtained by vortexing for 5 min. The emulsions were sterilized through 0.22 µm politetrafluoroetilene (PTFE) Minisart syringe filter (Sartorius, Göttingen, Germany). The inocula were prepared as described in Section 2.5.1. A positive (100 μL of TSB medium and 100 μL inoculum) and a negative control (200 μL of sterile TSB medium) were considered for each strain. The lowest EOs concentrations that prevented growth after 48 h of incubation, was interpreted as the MIC. The Minimum Bactericidal Concentration (MBC) was determined by inoculating the content of wells were no growth was observed, on TSA plates and by incubating the plates at the temperatures reported in Table 1. The MBC was recorded as the lowest concentration not allowing bacterial growth on plates [28].

2.6. Statistical Analysis

Experimental results were expressed as means ± standard deviations. Data obtained were subjected to ANOVA (analysis of variance), and a Tukey’s HSD post-hoc test was applied at p < 0.05, using Microsoft Xlstat 2016 statistical software (Addinsoft, Paris, France). Correlations between TPC and AOC (antioxidant capacity) results and antimicrobial activities, were calculated using Microsoft Xlstat 2016 statistical software (Addinsoft) by means of Pearson Correlation.

3. Results & Discussion

3.1. Essential Oil Extractions

The extraction yields were calculated considering the mass (g) of the obtained EOs and the mass (g) of dried material processed. The yield results were expressed as the mean of the three replicates of the extraction ± standard deviation.

R. officinalis, O. vulgare, S. officinalis, M. piperita, A. sativum, F. vulgare, C. sativum, S. montana, T. vulgaris yields % were: 0.487 ± 0.011, 2.900 ± 0.012, 0.249 ± 0.001, 1.034 ± 0.057, 0.371 ± 0.011, 0.340 ± 0.016, 0.265 ± 0.010, 0.491 ± 0.027, 1.506 ± 0.096, respectively. The obtained yields were similar to ranges usually reported in the literature for the same species [26,29,30,31,32,33].

3.2. Chemical Characterization

The chemical compositions of the different EOs were reported in Table 2.

Table 2.

Gas Chromatography-Mass Spectrometry (GC-MS) characterization of essential oils (EOs).

ID RID RIE R. officinalis O. vulgare S. officinalis A. sativum F. vulgare M. piperita C. sativum S. montana T. vulgaris
Diallyl sulfide 848 847 - - - 0.55 ± 0.04 c - - - - -
Methyl allyl disulfide 910 911 - - - 0.29 ± 0.00 c - - - - -
α-Pinene 939 939 16.64 ± 0.22 b 0.47 ± 0.02 i 1.20 ± 0.10 f,g - 5.18 ± 0.73 c 0.86 ± 0.03 e 0.28 ± 0.00 e - 0.37 ± 0.01 f,g
Camphene 953 956 3.39 ± 0.04 f - 1.38 ± 0.03 f - - - - - -
Thuja-2,4(10)-diene 957 960 0.32 ± 0.01 l - - - - - - - -
1-Octen-3-ol 978 979 - 0.57 ± 0.02 h,i - - - - - 1.43 ± 0.02 e -
β-Pinene 979 981 2.35 ± 0.03 g - 2.77 ± 0.16 e - 1.03 ± 0.05 e 0.52 ± 0.01 e - - 1.87 ± 0.09 f
β-Myrcene 992 993 0.72 ± 0.01 k - - - 0.65 ± 0.06 e - 0.28 ± 0.03 e 0.55 ± 0.03 e 0.56 ± 0.02 g,h
α-Phellandrene 1005 1006 - - - - 10.49 ± 0.02 b - - - -
trans-β-Ocimene 1015 1014 0.38 ± 0.02 l - - - - - - - -
p-Cymene 1024 1021 1.75 ± 0.01 i 8.30 ± 0.02 c 0.52 ± 0.03 g - 3.33 ± 0.24 d - 0.31 ± 0.00 e 10.78 ± 0.41 b 18.57 ± 0.71 b
Limonene 1029 1029 - - - 4.56 ± 0.38 c,d - 0.33 ± 0.00 e 0.69 ± 0.04 e -
1,8-Cineole 1032 1034 15.71 ± 0.18 c - 10.02 ± 0.36 c - - 5.35 ± 0.38 c,d - 0.53 ± 0.01 e -
γ-Terpinene 1060 1061 0.46 ± 0.02 k,l 9.38 ± 0.01 c - - - - 1.19 ± 0.07 d,e 6.46 ± 0.71 c 4.92 ± 0.13 c,d
cis-Sabinene hydrate 1066 1064 - - - - - - - - 3.17 ± 0.03 e
Diallyl disulfide 1080 1079 - - - 20.16 ± 2.84 b - - - - -
Terpinolene 1087 1085 - - - - - - - - 4.54 ± 0.06 d
Fenchone 1088 1088 - - - - 10.12 ± 0.07 b - - - -
(S)-(+)-Linalool 1100 1099 2.02 ± 0.01 h 1.95 ± 0.10 e,f - - - 0.86 ± 0.04 e 77.07 ± 1.82 a 2.09 ± 0.10 d,e 0.37 ± 0.01 g,h
α-Thujone 1102 1104 30.46 ± 0.49 a
1-Octen-3-ol, acetate 1110 1113 - - - - - - - - 1.27 ± 0.01 f,g
Menthone 1126 1116 - - - - - 6.87 ± 0.11 b,c - - -
l-Pinocarveol 1135 1132 0.23 ± 0.01 l - - - - - - - -
Camphor 1139 1137 22.07 ± 0.23 a - 11.53 ± 0.34 b - - - 2.60 ± 0.10 c,d - 0.29 ± 0.02 h
Borneol 1162 1160 11.99 ± 0.04 d 0.66 ± 0.01 g,h,i 3.92 ± 0.02 d - - - 0.48 ± 0.01 e 4.51 ± 0.37 c,d -
Menthofuran 1164 1165 - - - - - 7.81 ± 0.59 b - - -
Menthol 1171 1178 - - - - - 53.39 ± 0.24 a - - -
Isocamphopinone 1175 1174 1.08 ± 0.00 j - - - - - - - -
Terpinene-4-ol 1179 1176 0.26 ± 0.01 l 0.38 ± 0.01 i 1.43 ± 0.09 f - - - 0.55 ± 0.03 e - -
2-Vinyl-1.3-dithiane 1182 1084 - - - 4.60 ± 0.09 c - - - - -
Isomenthol 1194 1192 - - - - - - - - -
α-Terpineol 1195 1195 1.49 ± 0.08 i 1.64 ± 0.04 f,g,h,i 0.51 ± 0.01 g - 0.49 ± 0.03 e - 0.59 ± 0.03 e 1.61 ± 0.02 e 4.48 ± 0.09 d
Myrtenol 1196 1194 2.35 ± 0.03 g - - - - - - - 2.82 ± 0.15 e
Estragole 1199 1198 - - - - 44.86 ± 0.26 a - - -
Verbenone 1205 1203 0.44 ± 0.05 l - - - - - - - -
Isopulegone 1237 1237 - - - - - 2.01 ± 0.03 e - - -
Piperitone 1253 1250 - - - - - 0.21 ± 0.02 e - - -
cis-Geraniol 1254 1256 - - - - - - 5.24 ± 0.39 b - -
Thymol methyl ether 1255 1257 - 1.04 ± 0.01 f,g,h - - - - - - -
Neomenthyl acetate 1273 1270 - - - - - 0.81 ± 0.06 e - - -
trans-anethol 1285 1282 - - - 6.55 ± 0.06 c - - - -
Bornyl acetate 1286 1286 5.62 ± 0.01 e - - - - - - - -
Thymol 1290 1290 - 40.32 ± 1.12 a - - - - - 2.53 ± 0.14 d,e 43.68 ± 0.54 a
Menthyl acetate 1295 1294 - - - - - 4.61 ± 0.01 d - - -
Carvacrol 1299 1299 - 16.20 ± 0.05 b - - 0.63 ± 0.01 e - 1.03 ± 0.03 d,e 54.17 ± 2.33 a 5.51 ± 0.12 c
Diallyl trisulfide 1301 1300 - - - 65.39 ± 2.50 a - - - - -
Isocaryophyllene 1438 1434 3.37 ± 0.20 f 2.90 ± 0.07 e 10.49 ± 0.00 c - 1.05 ± 0.05 e 1.67 ± 0.03 e 0.62 ± 0.02 e 2.91 ± 0.11 d,e 1.61 ± 0.03 f
Humulene 1467 1467 0.72 ± 0.02 k 0.77 ± 0.03 g,h,i 10.01 ± 0.35 c - 0.49 ± 0.01 e - - - -
Germacrene-d 1487 1490 - 0.90 ± 0.01 f,g,h,i - - - 0.87 ± 0.02 e - - 0.55 ± 0.01 g,h
β-Bisabolene 1506 1509 - 4.64 ± 0.06 d - - - - 0.83 ± 0.04 d,e 1.82 ± 0.03 e 1.64 ± 0.01 f
γ-Cadinene 1513 1514 - - - - - - - 0.54 ± 0.02 e -
δ-Cadinene 1523 1522 - 0.65 ± 0.01 g,h,i 0.45 ± 0.01 g - - - - 0.54 ± 0.02 e -
Diallyl tetrasulfide 1555 1557 - - - 1.49 ± 0.07 c - - - - -
Caryophyllene oxide 1581 1583 - 1.73 ± 0.01 f,g 1.92 ± 0.05 e,f - - 1.21 ± 0.04 e 3.16 ± 0.17 c 1.41 ± 0.05 e -
Ledene 1585 1589 - - 10.12 ± 0.44 c - - - - - -
Total identified compounds 93.35 ± 0.43 92.52 ± 0.84 97.04 ± 0.46 92.47 ± 0.39 90.44 ± 0.87 93.17 ± 0.39 94.55 ± 1.69 92.56 ± 3.94 96.22 ± 1.47
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Results were expressed as mean relative abundances % of three replicates. In the table: ID, component name; RID, retention index retrieved from http://webbook.nist.gov/chemistry/ for the same analysis conditions; RIE, experimental retention index referred to C8–C40 n-alkane mixture standard. Statistical groups were defined by progressive alphabetical letters (case-letter). For the same matrix (same column), results followed by the same case-letter are not significantly different according to Tukey’ HSD post hoc test (p > 0.05).

Regarding R. officinalis EO, the components identified were in accordance with those reported by other authors [34,35,36] for this officinal plant. The major components (p < 0.05) of the mixture were camphor (22%), α-pinene (17%), 1,8-cineole (16%) and borneol (12%). These approximately equal ratios have been already recognized to be characteristic of some R. officinalis species from Italy and nearby countries [15,37]; however, 1,8-cineole chemotype is generally reported for rosemary plants cultivated in different other locations of Italy [35,37,38].

For O. vulgare EO, the major constituent (p < 0.05) was thymol (40%), followed by carvacrol (16%), γ-terpinene (9%) and p-cymene (8%). The obtained data were similar with those reported by De Martino et al. [39] for thymol/carvacrol chemotypes cultivated in a southern region of Italy, by Vazirian et al. [40] and Daferera et al. [41] for Iranian and Greek oregano EOs, respectively. The main compound of O. vulgare EO is usually carvacrol or thymol, while other authors stated that camphor was the main constituent [15,42,43].

S. officinalis EO showed α-tujone (41%) as main constituent (p < 0.05), followed by camphor (12%) and equal ratios (p > 0.05) of 1,8-cineole/isocaryophyllene/humulene/ledene (total abundance of 42%). The chemical composition was in accordance with those reported in literature by different authors for some European and Iranian sages [44,45], anyhow in these works lower concentrations of α-tujone were recorded.

For A. sativum EO a total of six compounds were identified. The principal component (p < 0.05) was diallyl disulfide (65%), followed by diallyl trisulfide (20%), in accordance with the results reported by Dziri et al. [46]. These compounds represent two of the main compounds produced during the thermal or long-term decomposition of allicin, the unstable garlic main constituent released from the alliin upon an injury and by means of the activity of the enzyme alliinase [47].

T. vulgaris EO presented thymol (44%) as major compound (p < 0.05), thus in our case the thyme chemotype was thymol. In scientific literature there are contrasting data about the area cultivation-related chemotype, being T. vulgaris characterized by an evident chemotype variation that lead to different monoterpene co-occurrence and composition [48].

Regarding F. vulgare EO, the major component (p < 0.05) was estragole (45%), followed by similar values (p > 0.05) of fenchone (10%) and α-phellandrene (10%). For M. piperita, menthol (53%) was the EO main compound (p < 0.05), followed by menthofuran (8%) and menthone (7%). (S)-(+)-Linalool was the principal constituent (p < 0.05) of C. sativum EO obtained from plant seeds, for which a 77% of the total volatile mixture was accountable. In S. montana EO, carvacrol was the compound with the highest (p < 0.05) relative abundance (54%). For these last four EOs, the obtained data were in accordance with those reported in the literature from other authors [49,50,51,52,53,54].

The GC-MS chemical characterization of the analyzed samples allowed to identify the main components of the extracted EOs (total identified compounds > 90%); in addition, the data comparison with scientific literature underlined the influence of the environmental conditions of plant cultures on the composition of their volatile fraction.

3.3. Total Phenolic Content and Antioxidant Activity

Total phenolic content (TPC) results were showed in Table 3. The highest TPC (p < 0.05) was recorded for T. vulgaris EO (6.42 mg GAE/g EO), followed by O. vulgare (4.69 mg GAE/g EO) and S. montana (4.40 mg GAE/g EO). The other EOs showed lower values (p < 0.05) with a TPC range of 0.05–0.28 mg GAE/g EO and no significant differences among them (p > 0.05).

Table 3.

Total phenolic content (TPC) and antioxidant activity results Ferric Reducing Antioxidant Power (FRAP), 2,2-diphenyl-1-picrylhydrazyl (DPPH) and Trolox Equivalent Antioxidant Capacity with 2,2′-azinobis-(3-ethylbenzothiazoline-6-sulfonic acid (TEAC/ABTS) of EOs and Pearson correlation coefficients between the different antioxidant activity assays and total phenolic content.

Assay TPC FRAP DPPH ABTS
Rosmarinus officinalis 0.111 ± 0.002 c 188.270 ± 0.437 a 10.288 ± 0.258 c,d 0.084 ± 0.001 e
Origanum vulgare 4.688 ± 0.304 b 168.220 ± 1.837 b 23.963 ± 2.435 b 1.765 ± 0.005 b
Salvia officinalis 0.178 ± 0.008 c 12.304 ± 0.022 f 8.709 ± 0.885 c,d 0.098 ± 0.005 e
Mentha piperita 0.338 ± 0.018 c 0.543 ± 0.044 h 11.289 ± 0.514 c 0.154 ± 0.006 d
Allium sativum 0.050 ± 0.001 c 3.924 ± 0.142 g 7.868 ± 0.158 d 0.037 ± 0.003 g
Foeniculum vulgare 0.283 ± 0.013 c 15.202 ± 0.175 e 11.466 ± 0.636 c 0.043 ± 0.003 g
Coriandrum sativum 0.046 ± 0.004 c 4.122 ± 0.241 g 10.656 ± 1.043 c,d 0.067 ± 0.004 f
Satureja montana 4.398 ± 0.252 b 159.280 ± 1.575 c 27.015 ± 0.959 a 1.997 ± 0.003 a
Thymus vulgaris 6.419 ± 0.219 a 126.869 ± 0.175 d 21.751 ± 0.862 b 1.131 ± 0.012 c
Pearson Correlation Coefficients
Assay FRAP ABTS DPPH
TPC 0.642 0.691 0.905
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Regarding TPC and AOC (antioxidant activity): results were expressed as mg Gallic acid equivalents (GAE)/g EO for TPC assay; mg Trolox equivalent (TE)/g EO for FRAP assay; µg Trolox equivalent (TE)/g EO for DPPH assay; mmol Trolox equivalent/g EO for ABTS assay. The showed values were the mean of three replicates. For the same assay (same column), results followed by the same case-letter are not significantly different according to Tukey’ HSD post hoc test (p > 0.05). For Pearson Correlation Coefficients: the positive/negative strength of correlation was considered: low for ±0.1 < r < ±0.3, moderate for ±0.3 < r < ±0.7, and strong for r > ±0.7; for values of r < ±0.1 the variables were considered not correlated.

Antioxidant activity (FRAP, DPPH, TEAC/ABTS) results were also reported in Table 3. The different assays established that O. vulgare, S. montana and T. vulgaris were the EOs with the best antioxidant capacity according to free radical scavenging methods (DPPH and TEAC/ABTS). The FRAP assay underlined also the antioxidant potential of R. officinalis EO.

Even if the vegetal matrix had different origins, the methodology of the investigation and expression of results made difficult a direct comparison between TPC and AOC data and the literature. The presented ranges were similar to those presented by several authors for different essential oils [15,20,26,43,55].

A Pearson correlation test between the AOC and TPC data was carried out and the coefficients results obtained were presented in Table 3. As reported, among the different assays, a moderate (TPC with FRAP and ABTS) and strong (TPC with DPPH) positive correlation were revealed. Thus, the detected antioxidant activity could be attributed to total phenols content assessed in the EOs. These positive correlations between AOC and TPC have been already reported for plant species of the Mediterranean area [56].

3.4. Antimicrobial Activity

The antibacterial activity of the tested EOs against selected Gram-positive and Gram-negative bacteria was reported in Table 4. The strains were selected among spoiling (P. fluorescens, B. thermosphacta and E. faecium) and pathogenic (Salmonella enterica serotype Enteritidis and Salmonella enterica serotype Typhimurium, L. monocytogenes and S. aureus) bacteria commonly isolated from food products of different origins, to have an overview of the potentiality of the selected essential oils.

Table 4.

Minimum Inhibitory Concentration (MIC) (μL/mL) of selected essential oils against the different strains.

Strains Rosmarinus officinalis Origanum vulgare Salvia officinalis Mentha piperita Allium sativum Foeniculum vulgare Satureja montana Thymus vulgaris Coriandrum sativum
P. fluorescens P34 10 1.25 10 >20 10 >20 1.25 2.5 5
B. thermosphacta B2 >20 10 >20 >20 >20 >20 2.5 2.5 5
B. thermosphacta B1 >20 10 >20 >20 >20 >20 5 2.5 5
S. Enteritidis S2 20 2.5 >20 >20 >20 >20 1.25 1.25 5
S. Typhimurium S4 >20 2.5 >20 >20 >20 >20 5 2.5 5
E. faecium P14 >20 5 >20 >20 >20 >20 5 5 5
E. faecium ATCC 19434 10 5 >20 >20 10 >20 5 2.5 2.5
L. monocytogenes LM 4 >20 5 10 >20 >20 >20 2.5 1.25 0.625
L. monocytogenes ATCC 19144 10 5 5 20 2.5 >20 2.5 1.25 0.625
L. monocytogenes ATCC 7644 5 10 10 10 2.5 >20 5 1.25 0.625
S. aureus STA 32 10 5 >20 >20 10 >20 2.5 2.5 0.625
S. aureus STA 47 5 5 10 2.5 5 >20 5 1.25 1.25
S. aureus STA 39 >20 5 >20 >20 10 >20 5 1.25 1.25
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Generally, the results observed as MIC were also confirmed as MBC. In some cases, the MIC concentration had to be doubled to obtain a bactericidal activity (i.e., MBC of T. vulgaris and C. sativum EOs was respectively 5 and 10 µL/mL for both B. thermosphacta B1 and B2).

For F. vulgare EO, the results established that the obtained EO was unable to inhibit the tested microbial strains at concentrations lower or equal than 20 µL/mL. The results were in accordance with those reported by Çetin et al. [57], who assessed that for fennel EOs obtained from the aerial parts, as in our case, the different MIC values ranged from 31.25 to 500 µg/mL. Lower MIC values could be obtained from EOs extracted from seeds [42,58] and fruits [59] of the plant; in these cases, the EOs main compound is trans-anethol, present only in minor quantities in our EO.

Regarding R. officinalis, S. officinalis, M. piperita and A. sativum, the EO tested showed a limited spectrum of activity; good results (5 μL/mL) were obtained against different strains, however higher MIC values obtained for the other strains belonging to the same species seemed to underline a strain-dependent activity. Thus, for these EOs, a variable antimicrobial activity against the Gram-negative and Gram-positive bacteria tested, was generally recognized at concentrations higher than 10 μL/mL. Nevertheless, significant results were observed for A. sativum EO against the two Listeria monocytogenes type strains. Good results were also obtained for R. officinalis EO; in fact, it usually shows a good antioxidant activity [60] and a lower antimicrobial activity with respect to other EOs such as oregano, thyme or tea tree [43], while in our case it showed good inhibitory activity, particularly on L. monocytogenes ATCC7644 and S. aureus STA47. This activity is probably due to the presence of camphor and 1,8-cineol among the principal constituents, as reported in Table 2.

For O. vulgare, the MIC values showed a wide spectrum of activity, ranging from 1.25 to 10 μL/mL for both Gram-positive and Gram-negative bacteria. In this case, the antimicrobial activity could be related to the important presence of thymol and carvacrol in the volatile fraction, as described in Section 3.1 (Table 2); the high contents of thymol, in fact, results in good antimicrobial activities [39,61].

The most effective EOs were those obtained from S. montana, T. vulgaris and C. sativum. For these EOs the MIC values ranged from 0.625 to 5 μL/mL. For these EOs thymol, (S)-(+)-linalool, and carvacrol have been already confirmed to be responsible for their antimicrobial activity, with ranges similar to those obtained in the present study [43,62,63,64]. In particular, while the antimicrobial activity of O. vulgare and T. vulgaris EOs against L. monocytogenes is well known [65,66], very interesting results were observed for C sativum against Listeria, but also the other tested pathogens, such as S. aureus (especially strain STA32) and Salmonella strains. These results are particularly significant, as Gram-negative bacteria are usually less sensitive to EOs than Gram-positive, because of the presence of the lipopolysaccharide layer, that provides a higher resistance to hydrophobic compounds such as essential oils [67]. On the contrary, the Gram-positive B. thermosphacta strains B1 and B2 were among the most resistant strains, nevertheless, they were inhibited by low concentrations of T. vulgaris and S. montana EOs.

4. Conclusions

The results obtained from this study established that the essential oils obtained from Abruzzo region officinal plants, mainly from T. vulgaris, S. montana and C. sativum, showed interesting biological potentiality. The antimicrobial and antioxidant properties assessed are excellent bases for further in vitro assays that could be used to define these essential oils as potential candidates for natural biopreservatives in combination with or in substitution to synthetic chemical ones. Moreover, additional studies should be undertaken in order to understand their potentiality in model systems and in real food samples. Study should particularly aim to establish the most effective EO concentration depending on the food matrix, its organoleptic properties, and the microorganisms it should inhibit. Anyhow, these results represent a valid basis for future evaluations and enriched current understanding about the specificity of Abruzzo region plant species and their essential oils.

Acknowledgments

This research was supported by the grant of Regione Abruzzo, for the project “PSR 2017–2013 Misura 1.2.4” cod. CUA 2446850691, title “Sviluppo di sistemi convenzionali e innovazioni per la produzione di composti bioattivi da materie prime vegetali per l’impiego nel settore alimentare”.

Author Contributions

Claudio Lo Sterzo and Antonello Paparella conceived and designed the experiments; Marika Pellegrini, Giovanni Mazzarrino and Serena D’Amato performed the experiments; Marika Pellegrini, Antonella Ricci, Annalisa Serio and Clemencia Chaves-López analyzed the data and wrote the paper.

Conflicts of Interest

Authors declare no conflict of interest.

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