Antioxidant, Antidiabetic, and Antibacterial Potentials and Chemical Composition of <i>Salvia officinalis</i> and <i>Mentha suaveolens</i> Grown Wild in Morocco

Al-Mijalli, Samiah Hamad; Assaggaf, Hamza; Qasem, Ahmed; El-Shemi, Adel G.; Abdallah, Emad M.; Mrabti, Hanae Naceiri; Bouyahya, Abdelhakim

doi:https://doi.org/10.1155/2022/2844880

Advances in Pharmacological and Pharmaceutical Sciences

On this page

Abstract Introduction Materials and Methods Results Discussion Conclusion Abbreviations Data Availability Conflicts of Interest Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2022 | Article ID 2844880 | https://doi.org/10.1155/2022/2844880

Antioxidant, Antidiabetic, and Antibacterial Potentials and Chemical Composition of Salvia officinalis and Mentha suaveolens Grown Wild in Morocco

Samiah Hamad Al-Mijalli,¹Hamza Assaggaf,²Ahmed Qasem,²Adel G. El-Shemi,²Emad M. Abdallah,³Hanae Naceiri Mrabti,⁴and Abdelhakim Bouyahya⁵

Academic Editor: Chita Ranjan Sahoo

Received25 Feb 2022

Revised24 May 2022

Accepted31 May 2022

Published15 Jun 2022

Abstract

This work evaluated in vitro antioxidant, antidiabetic, and antibacterial properties of Salvia officinalis (S. officinalis) and Mentha suaveolens (M. suaveolens) essential oils (EO). The EOs were extracted, and their chemical composition was determined using GC-MS analysis. The in vitro antioxidant, antidiabetic, and antibacterial activities of S. officinalis and M. suaveolens EO were shown to be remarkable. Furthermore, S. officinalis EO demonstrated better antioxidant findings (using DPPH, ABTS, and FRAP test) than M. suaveolens EO (). There were no significant differences in the inhibitory effects of the EOs on α-amylase and α-glucosidase activities in the antidiabetic assays. All of the examined bacterial strains (10 different strains), with the exception of P. aeruginosa, demonstrated significant sensitivity to the tested EOs, with M. suaveolens EO exhibiting better activity than S. officinalis EO. Thus, the research indicated that EO from these two medicinal plants has considerable potential for application in the formulation of antibacterial, antioxidant, and antidiabetic pharmaceuticals. However, more research studies are required to interpret the pharmacologic action of the studied EOs and their principal constituents and to confirm their safety.

1. Introduction

About 80% of rural people in developing countries use traditional medicine made from plants. Even people in developed countries are becoming more interested in medicinal plants [1]. Indeed, over 25% of medications used in the previous two decades are typically extracted from plants, while the remaining 25% are chemically altered natural substances. Despite this, only around 5%–15% of the roughly 250,000 higher plants have ever been studied for pharmacological activities [2]. Numerous studies conducted over the last few decades have shown that research on therapeutic plants is critical and bioactive phytochemicals or bionutrients are abundant in medicinal plants; these phytochemicals have a critical role in avoiding chronic illnesses such as cancer [3–5], diabetes [6–9], and coronary heart disease [10–12]. Dietary fiber, detoxifying agents, antioxidants, anticancer, neuropharmacological agents, and immune-stimulating agents are the key groups of phytochemicals having disease-preventive properties [13].

There is now strong evidence that oxidative stress caused by free radicals or reactive oxygen species is the main cause of a number of human neurological diseases. Antioxidant compounds found in foods and medicinal plants can be used as chemo-preventive agents [14]. Also, oxidative stress is a significant factor for development of diabetes mellitus. Natural antioxidants are abundant in plant-based foods. Numerous epidemiological and clinical research, as well as in vivo and in vitro studies, have shown that fruits with varying phytochemical profiles have the capacity to normalize blood glucose levels [15]. Diabetes mellitus is becoming a severe hazard to human health in all regions of the globe due to its fast-rising prevalence. Additionally, during the last several years, some novel bioactive compounds derived from plants have shown superior anti-diabetic action than commonly used oral hypoglycemic medications [16].

Antibiotics’ capacity to treat microbial infections has deteriorated over the last several decades, and multidrug resistant bacteria have arisen; as a result, medicinal plants are recommended as a source of novel antibacterial compounds such as coumarin molecules which were reported as promising antibacterial agents [17]. It is believed that taking corrective and preventive action now through collaborative and innovative approaches in the field of novel antibacterial drug discovery and development is critical for preparing for future pandemics caused by multidrug-resistant bacteria, a target that truly deserves our full attention [18]. Interestingly, numerous studies revealed that there are hundreds of medicinal plants that documented antibacterial effectiveness which may be turned into effective medications [19]. According to scientific reports, the antibacterial activity of some medicinal plants is a consequence of their phytochemical constituents, which include sulfur-containing compounds, alkaloids, terpenoids, carotenoids, and polyphenols [20].

Sage (Salvia officinalis L.) is an aromatic and medicinal plant that belongs to the Lamiaceae family. This family has about 900 species that are found around the globe, with some of them having a high economic value due to their usage in the cosmetic industry and perfumery [21]. Salvia is extensively used in traditional medicine as an antiseptic, antiscabies, antibacterial, antisyphilis, and anti-inflammatory medication, and it was reportedly used to cure fever and some digestive disorders in several locations of the Middle East [22].

Apple mint (Mentha suaveolens Ehrh.) is a perennial rhizomatous plant, the genus Mentha is a member of the Labiatae family and is well-known for its high essential oil concentration, and this herb is widespread in a number of Mediterranean countries [23]. Labiatae family has over 260 genera and more than 7000 species, and it has been widely known since ancient civilizations [24]. It has been used in traditional medicine in Mediterranean countries for a wide variety of purposes, including cardiovascular effects, antibacterial properties, analgesic properties, anti-inflammatory properties, and antiviral properties [25].

Although various studies on the bioactive properties of S. officinalis and M. suaveolens have been conducted worldwide, the essential oils (EOs) of these plants that grow wild in Morocco have received little attention in terms of their biological effects. Moreover, the current investigation aimed to determine the chemical composition of S. officinalis EOs (SOEO) and M. suaveolens EOs (MSEO) and to evaluate their antioxidant, antidiabetic, and antibacterial potentials.

2. Materials and Methods

2.1. Chemicals and Reagents

Acarbose, ascorbic acid, 2, 2′-diphenyl-1-picrylhydrazyl (DPPH), 6-hydroxy2, 5, 7, 8-tetramethylchroman-2-carboxylic acid (Trolox), 2, 2-azino-bis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS), p-nitrophenyl-α-D–D-glucopyranoside (p-NPG), and 3, 4-dihydroxy phenylalanine (L-DOPA) were procured from Sigma-Aldrich (France). α-Amylase (from Bacillus licheniformis) and α-glucosidase (from Saccharomyces cerevisiae) were purchased from Roche Diagnostics (USA). All other reagents used were of analytical grade.

2.2. Plant Materials and EOs Extraction

During April 2021, the aerial parts of S. officinalis and M. suaveolens were manually collected from their natural habitat in the Taza region of Morocco. The plants were identified according to the procedure described by González-Tejero et al. [26] and confirmed by the botanists at the Botany Department of the Scientific Institute of Rabat, University of Mohammed V Rabat, Morocco. Voucher specimens of each plant were deposited in the herbarium under the voucher specimen code RAB61862 for S. officinalis and RAB611848 for M. suaveolens. The extraction process of the EOs was carried out by hydrodistillation in a Clevenger-type apparatus. Briefly, 100 g of the dry powder of each plant were placed in a flask filled to 2/3 with water; the whole is brought to the boil for 3 hours. The oil is recovered and then stored at a temperature of 4°C.

2.3. Chemical Composition Analysis

The chemical components of SOEO and MSEO were determined by using gas chromatography/mass spectrometry (GC/MS) analysis conditions as described in our latterly published study [27].

2.4. In Vitro Antioxidant Assays

The antioxidant activity of the two tested EOs (solubilized in Tween 20 (5%)) was evaluated using the following three commonly used in vitro complementary assays: DPPH and ABTS radical scavenging assays, and ferric reducing/antioxidant power (FRAP) assay, and following the same procedures as described previously by our research group [28, 29] and by others. Each assay was carried out in triplicate, and Trolox and ascorbic acid were used as positive controls. In each assay, the concentrations of the EOs that provided 50% inhibition (IC₅₀) were determined, and their values were presented in μg/mL.

2.5. In Vitro Assessment of Antidiabetic Activity

The in vitro antidiabetic effects of SOEO and MSEO ((solubilized in Tween 20 (5%)) were determined by measuring their capacity to inhibit α-amylase and α-glucosidase enzymatic activity, following the same methods as we previously described [30], and the IC₅₀ (μg/mL) values were determined.

2.6. In Vitro Evaluation of Antibacterial Activity

2.6.1. Bacterial Strains

In the present study, the antibacterial activity of SOEO and MSEO was carried out on ten referenced pathogenic bacterial strains divided as five Gram-positive strains including Staphylococcus aureus, Staphylococcus epidermidis, Enterococcus faecalis, Listeria monocytogenes, and Bacillus cereus, and five Gram-negative strains including Escherichia coli, Salmonella typhimurium, Klebsiella pneumoniae, Proteus mirabilis, and Pseudomonas aeruginosa. All the bacterial strains were brought from the Microbiology Lab at Mohammed V University in Rabat, after their identification using the standard microbiological procedures [31].

2.6.2. Disc-Diffusion Test

The disc-diffusion test was employed to determine the preliminary antibacterial potential of SOEO and MSEO against the selected 10 bacterial pathogens, according to the protocol described previously by our research group [27]. Briefly, the tested EOs were mixed with 10% dimethyl sulfoxide (DMSO) to enhance their diffusion into the agar. Subsequently, a 0.5 McFarland (10⁸ CFU/mL) suspension of each studied bacterium was prepared in normal saline (0.9% NaCl) and inoculated through swabbing on Mueller–Hinton agar plates (Biokar, Beauvais, France). Then, 10 μL of each EO was placed onto sterile paper discs with a diameter of 6 millimeters. Another disc holding 10 μL of 10% DMSO was used as a negative control, and another disc containing chloramphenicol (30 g/disc) was employed as a referenced drug (positive control). Following that, all plates were incubated at 37°C for 24 hours, and the inhibition diameter was measured in millimeters (disk included) and reported as the mean ± standard deviation of three replicates.

2.6.3. Determination of Minimum Inhibitory Concentration (MIC)

The broth dilution technique was used to determine the MIC values for SOEO and MSEO using a 96-well microtitration plate [32, 33]. Decreasing quantities of EOs were generated in microplates (final concentrations ranged between 20 and 0.039 mg/mL) in 10% DMSO. After adding 20 μL of bacterial suspensions adjusted to 0.5 McFarland standard and 140 μL of Mueller–Hinton broth, the microplates were incubated at 37°C for 24 hours. After incubation, 40 μL of 2, 3, 5-diphenyltetrazolium chloride (TTC) (Sigma-Aldrich, Buchs, Switzerland) at a concentration of 0.2 g/mL was added and incubated for 30 minutes at 37°C. The existence of living bacteria is indicated by the presence of a red hue on TTC.

2.6.4. Determination of Minimum Bactericidal Concentration (MBC)

The minimum bactericidal concentration (MBC) was determined for the two EOs against the examined bacteria as follows: 100 mL from each of the MIC tubes that exhibited no growth was subcultured on Mueller–Hinton agar plates and incubated at 37°C for 24 hours. MBC was defined as the lowest concentration that demonstrated no single colony of bacteria. Moreover, MBC/MIC values were calculated to classify the antibacterial agent as bacteriostatic or bactericidal [33].

2.7. Statistical Analysis

All tests were performed in triplicate and the obtained results are expressed as mean ± SD. Data were analyzed using SPSS software version 21, and comparisons of the means were determined by one-way analysis of variance (one-way ANOVA) followed by the Tukey test. Values with were considered statically significant.

3. Results

3.1. In Vitro Antioxidant Activity of SOEO and MSEO

The two EOs were investigated for their antioxidant capacity using three complementary tests: DPPH, ABTS radical scavenging capacity, and FRAP. As given in Table 1, both SOEO and MSEO had potent antioxidant activity, and SOEO showed the highest antioxidant ability as compared with MSEO (IC₅₀ = 53.19 ± 1.12 μg/mL, 69.48 ± 2.05 μg/mL and 75.19 ± 1.80 μg/mL vs. 93.67 ± 2.17 μg/mL, 112.41 ± 3.18 μg/mL, and 129.74 ± 2.11 μg/mL for DPPH, FRAP, and ABTS assay, respectively; ).

3.2. In Vitro Antidiabetic Activities of SOEO and MSEO

The antidiabetic activities of SOEO and MSEO were determined using the inhibitory effects on α-amylase and α-glucosidase enzymatic activities. The results are expressed as IC₅₀ and given in Table 2. The two EOs inhibited the activities of the two tested enzymes at low concentrations compared with the used standard drug (acarbose). However, no significant differences were detected between the inhibitory effects of the two EOs (IC₅₀ of S. officinalis EO = 81.91 ± 0.03 μg/mL and 113.17 ± 0.02 μg/mL vs. IC₅₀ of M. suaveolens EO = 94.30 ± 0.06 μg/mL and 141.16 ± 0.21 μg/mL, for inhibiting α-amylase and α-glucosidase enzymatic activity, respectively) (Table 2).

3.3. In Vitro Antibacterial Activity of SOEO and MSEO

As given in Table 3, the 10 examined bacterial strains were significantly () susceptible to the antibacterial activity of both SOEO and MSEO, with the exception of Pseudomonas aeruginosa which demonstrated weak susceptibility toward the two EOs and complete resistance to the reference antibiotic (chloramphenicol at 30 μg/disc). It was noted also that MSEO had showed comparably greater antibacterial activity than SOEO (Table 3). Moreover, the examined Gram-positive bacteria were more susceptible to the antibacterial activity of the two EOs than the tested Gram-negative bacteria. Next, the antibacterial efficacies of the two EOs were determined by using MIC and MBC assays. As given in Table 4, the overall MIC and MBC values for MSEO against all the tested bacteria were significantly lower than those for SOEO, reflecting its higher bactericidal activity than the latter one. Finally, the MBC/MIC ratios for both EOs were between 1 and 2, and Pseudomonas aeruginosa showed sensitivity to chloramphenicol only at its high concentration of 64 μg/mL (Table 4), indicating the high antimicrobial-resistance property of this pathogenic bacterial strain.

3.4. Chemical Composition of SOEO and MSEO

As given in Table 5 and Figures 1 and 2, the principal compounds detected in SOEO were thujone (33.77%), caryophyllene (12.28%), humulene (12.19%), camphor (11.52%), naphthalene (9.94%), eucalyptol (8.11%), α- and β-pinene (3.31% and 1.8%, respectively), β-myrcene (1.49%), germacrene D (1.36%), and borneol (1.18%). In comparison, the major chemical constituents for MSEO were pulegone (37.16%), pyrazines (33.81%), limonene (11.19%), umbellulone (6.09%), camphor (4.27%), 3-carene (1.34%), 2-bornanone (1.2%), menthone (0.98%), 1-octen-3-ol (0.97%), α-pinene (0.88%), and thujone (0.60%) (Table 5).

4. Discussion

The present in vitro study showed the remarkable antioxidant, antidiabetic, and antibacterial properties of SOEO and MSEO, and it also showed the comparable antioxidant and antidiabetic superiorities of SOEO but the antibacterial superiority of MSEO. These observed favourable antibacterial, antidiabetic, and antioxidant potentials of the two tested EOs, as well as the variance in their levels, could largely be attributed to the synergistic effects of their bioactive principal constituents [34, 35].

MSEO and SOEO chemical compounds were reported by numerous studies [36–39]. These investigations showed the richness of SOEO by thujone, caryophyllene camphor, eucalyptol, α-pinene, β-myrcene, borneol, and γ-terpinene as main compounds and MSEO by pulegone, limonene, camphor, menthone, α-pinene, and thujone as main compounds.

For instance, pulegone, which herein is one of the major components detected in MSEO, has been recently described as a potential and novel inhibitor of bacterial growth and biofilm formation in multidrug resistant (MDR) bacteria by suppressing specific genes in susceptible bacteria [40]. Similarly, pyrazines are well-known as volatile organic compounds with broad-spectrum antimicrobial activity mediated by their diffusion into various bacterial structures and result in cell envelope disintegration and DNA destructing in susceptible bacteria [41]. Additionally, due to their high efficacy in combating MDR-bacterial pathogens at lower concentrations and minimal mammalian toxicity, pyrazines are prone to be applied in various aspects of food industry to prevent microbial spoilage and contaminations [41–44]. Some recent studies have also explored the unique bactericidal mechanism for each of 3-carene [45] and 1-octen-3-ol [46] by disintegrating cell membranes integrity and metabolic functionality of food- and nonfood-related virulent pathogenic Gram-positive and Gram-negative bacteria. At a constant line, naphthalene, which herein was among the major components of SOEO, is a well-known aromatic compound with potent antibacterial, antiviral, and antituberculous activities mediated by its covalent interactions with pathogen cellular proteins to produce potent cytotoxic and lytic effects on these pathogens [47, 48]. Most importantly, several naphthalene containing drugs with a broad spectrum of biological activities are approved by the FDA and are available as therapeutics [47]. Closely, eucalyptol has been latterly proposed as an excellent natural replacer for antibiotics due to its powerful bactericidal activity against a wide range of potential pathogenic Gram (+) and Gram (−) bacteria [49]. Moreover, eucalyptol has also shown remarkable synergistic interaction with traditional antibiotics such as amoxicillin and gentamicin, suggesting its combination therapeutic benefit in cases of MDR and mixed-bacterial infections [49]. Recently, α-pinene has also faced a specific attention in antimicrobial therapy. Besides its predominant bactericidal activities against antibiotic resistant Staphylococci, Streptococci, Enterococci, Salmonella, Escherichia coli, and Pseudomonas species, α-pinene has been identified as potential inhibitors for the bacterial efflux’s pumps, which extrudes antibiotics out of bacterial cells and represents one of the main mechanisms contributing to MDR pathogenic bacteria [50–52]. Finally, the promising antimicrobial properties of thujone, caryophyllene, humulene, umbellulone, camphor, limonene, menthane, germacrene D, myrcene, and borneol, particularly against antibiotics-resistant microbial pathogens, have also been documented [53–55].

Diabetes mellitus (DM) is a highly complexed, chronic, metabolic disease caused by failure of pancreatic β-cells to produce sufficient insulin hormone alongside peripheral insulin resistance (IR) and characterized by persistent hyperglycemia and progressive metabolic and cellular changes [56, 57]. Nowadays, it has become more evident that progressive oxidative stress and mass production of reactive oxygen species (ROS) are among the ultimate contributors for pancreatic β-cell impairment and destruction, as well as in development of IR and multiple organ injury in diabetic patients [58]. Moreover, uncontrolled hyperglycemia, particularly postprandial hyperglycemia, is known as the most important risk factor for the generation of ROS and inflammation and act synergistically with oxidative stress to exacerbate β-cell failure, peripheral IR, and multimicro and macrovascular complications of DM. Hence, simultaneous controlling of hyperglycemia and oxidative stress is a paramount demand in DM therapy [59]. Despite the availability and the therapeutic benefits of several classes of antidiabetic-hypoglycemic agents, they are expensive, and their use is often associated with a wide range of side effects and nonproper control of patient’s hyperglycemia. Therefore, the search for alternative antidiabetic therapeutic options, specifically for approaches based on medical plants products with potential antidiabetic and antioxidant properties, has gained specific importance to overcome the disadvantages of currently used synthetic antidiabetic compounds [60]. Herein, the antidiabetic potentialities of SOEO and MSEO were identified by their potent inhibitory effects on α-amylase and α-glucosidase enzymatic activities, in addition to their potent antioxidant capacity. Inhibition of α-glucosidase and α-amylase activities, which are the main enzymes responsible for gastrointestinal carbohydrates digestion and for starch hydrolysis into glucose preabsorption, is one of the most hopeful therapeutic targets in DM therapy to reduce postprandial hyperglycemia and prevent the absorption of dietary starch [60, 61]. Moreover, SOEO, which is rich in thujone, is known for its metformin-like antidiabetic effect, and oral administration of the leaves of Mentha plant was found to markedly suppress the blood indices of lipid peroxidation and increase the levels of enzymatic and nonenzymatic antioxidant variables, in patients with type II DM [62]. Such previous clinical observations of the antidiabetic usefulness of SOEO and MSEO, alongside our current findings, could also be primarily mediated by the augmenting interactions between their biological active components [63, 64]. In this regard, and as presented here, the chemical composition of the two EOs (Table 5) showed an enrichment in monoterpenoids compounds, such as pulegone, thujone, umbellulone, limonene, camphor, α- and β-pinene, menthone, borneol, and bornanone, which collectively have well-documented potent antihyperglycaemic, antioxidant, and anti-inflammatory properties [65, 66]. Additionally, monoterpenes have been reported to stimulate insulin release from pancreatic β-cells, reduce cellular oxidative stress, and modulate enzymes, proteins, and pathways that contribute to the development of IR and other pathological events, and thus, they were emerged as promising natural molecules to treat DM and a vast range of metabolic disorders [65]. Likewise, both humulene and caryophyllene have been documented as pluripotent free radical scavengers and α-glucosidase and α-amylase inhibitors [67, 68].

4.1. Study Limitations

In addition to the study’s main findings, important limitations were inevitably identified, that should be addressed in the future. First, these findings are at the in vitro level, and to be more convinced, future in vivo studies in experimental rat and mice models of DM [59] and bacterial diseases [69] are essentially required, in which a second level of biochemical, molecular, and mechanistic analyses will be added. Second, the safety and toxicity profile and therapeutic index of these two EOs need to be determined in normal experimental animals to confirm the reliability of their clinical application in the future.

5. Conclusion

Findings of the present study revealed the chemical composition and antioxidant, antidiabetic, and antibacterial activities of SOEO and MSEO. The two tested essential oils inhibited α-amylase and α-glucosidase activities and showed potent in vitro antioxidant capacity. In addition, they exhibited significant bactericidal activity at lower concentrations against Staphylococcus aureus, Staphylococcus epidermidis, Enterococcus faecalis, Listeria monocytogenes, Bacillus cereus, Escherichia coli, Salmonella typhimurium, Klebsiella pneumoniae, and Proteus mirabilis bacterial strains, but weak activity against Pseudomonas aeruginosa. The observed favourable biological activities of these oils may primarily be attributed to the synergistic and/or additive effects of their bioactive chemical constituents. However, further studies are required to elucidate the present findings at the molecular and pharmaceutical levels and support their reliability for medical applications.

Abbreviations

ABTS:	2,2′-Azino-bis(3-ethylbenzothiazoline-6-sulphonic acid
ANOVA:	One-way analysis of variance
β-cell:	Beta cells in pancreatic islets
CFU:	Colony forming unit
DM:	Diabetes mellitus
DMSO:	Dimethyl sulfoxide
DPPH:	2,2′-Diphenyl-1-picrylhydrazyl
FDA:	U.S. Food and Drug Administration
FRAP:	Ferric reducing/antioxidant power
GC/MS:	Gas chromatography/mass spectrometry
IR:	Insulin resistance
EO:	Essential oil
IC₅₀:	The half-maximal inhibitory concentration
MDR:	Multidrug resistant
MBC:	Minimum bactericidal concentration
MIC:	Minimum inhibitory concentration
MSEO:	Mentha suaveolens essential oil
ROS:	Reactive oxygen species
SOEO:	Salvia officinalis essential oil
TTC:	2, 3, 5-Diphenyltetrazolium chloride
VS:	Versus.

Data Availability

The data used to support the findings of this study are included within the article.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

This study was supported by the Princess Nourah Bint Abdulrahman University Researchers Supporting Project number (PNURSP2022R158) Princess Nourah Bint Abdulrahman University, Riyadh, Saudi Arabia.

References

T. De Silva, “Industrial utilization of medicinal plants in developing countries,” Medicinal Plants for Forest Conservation and Health Care, FAO, Rome, Italy, pp. 34–44, 1997.
View at: Google Scholar
A. Amin, H. Gali-Muhtasib, M. Ocker, and R. Schneider-Stock, “Overview of major classes of plant-derived anticancer drugs,” International Journal of Biomedical Science: IJBS, vol. 5, no. 1, pp. 1–11, 2009.
View at: Google Scholar
J. Sharifi-Rad, A. Ozleyen, T. Boyunegmez Tumer et al., “Natural products and synthetic analogs as a source of antitumor drugs,” Biomolecules, vol. 9, no. 11, p. 679, 2019.
View at: Publisher Site | Google Scholar
A. Balahbib, N. El Omari, N. E. Hachlafi et al., “Health beneficial and pharmacological properties of p-cymene,” Food and Chemical Toxicology, vol. 153, Article ID 112259, 2021.
View at: Publisher Site | Google Scholar
N. El Omari, S. Bakrim, M. Bakha et al., “Natural bioactive compounds targeting epigenetic pathways in cancer: a review on alkaloids, terpenoids, quinones, and isothiocyanates,” Nutrients, vol. 13, no. 11, p. 3714, 2021.
View at: Publisher Site | Google Scholar
A. Bouyahya, I. Chamkhi, F.-E. Guaouguaou et al., “Ethnomedicinal use, phytochemistry, pharmacology, and food benefits of thymus capitatus,” Journal of Ethnopharmacology, vol. 259, Article ID 112925, 2020.
View at: Publisher Site | Google Scholar
A. Bouyahya, N. El Omari, N. Elmenyiy et al., “Moroccan antidiabetic medicinal plants: ethnobotanical studies, phytochemical bioactive compounds, preclinical investigations, toxicological validations and clinical evidences; challenges, guidance and perspectives for future management of diabetes worldwide,” Trends in Food Science & Technology, vol. 115, pp. 147–254, 2021.
View at: Publisher Site | Google Scholar
A. Bouyahya, I. Chamkhi, T. Benali et al., “Traditional use, phytochemistry, toxicology, and pharmacology of Origanum majorana L,” Journal of Ethnopharmacology, vol. 265, Article ID 113318, 2021.
View at: Publisher Site | Google Scholar
B. Abdelaali, N. El Menyiy, N. El Omari et al., “Phytochemistry, toxicology, and pharmacological properties of Origanum elongatum,” Evidence-Based Complementary and Alternative Medicine, vol. 2021, Article ID 6658593, 12 pages, 2021.
View at: Publisher Site | Google Scholar
A. Bouyahya, H. Mechchate, T. Benali et al., “Health benefits and pharmacological properties of carvone,” Biomolecules, vol. 11, no. 12, p. 1803, 2021.
View at: Publisher Site | Google Scholar
A. Bouyahya, N. El Omari, M. Hakkur et al., “Sources, health benefits, and biological properties of zeaxanthin,” Trends in Food Science & Technology, vol. 118, pp. 519–538, 2021.
View at: Publisher Site | Google Scholar
N. El Omari, F. Ezzahrae Guaouguaou, N. El Menyiy et al., “Phytochemical and biological activities of Pinus halepensis mill., and their ethnomedicinal use,” Journal of Ethnopharmacology, vol. 268, Article ID 113661, 2021.
View at: Publisher Site | Google Scholar
M. Saxena, J. Saxena, R. Nema, D. Singh, and A. Gupta, “Phytochemistry of medicinal plants,” Journal of Pharmacognosy and Phytochemistry, vol. 1, no. 6, 2013.
View at: Google Scholar
S. E. Atawodi, “Antioxidant potential of African medicinal plants,” African Journal of Biotechnology, vol. 4, no. 2, pp. 128–133, 2005.
View at: Google Scholar
C. Sun, Y. Liu, L. Zhan et al., “Anti-diabetic effects of natural antioxidants from fruits,” Trends in Food Science & Technology, vol. 117, pp. 3–14, 2021.
View at: Publisher Site | Google Scholar
S. Malviya, S. Rawat, A. Kharia, and M. Verma, “Medicinal attributes of Acacia nilotica Linn.—a comprehensive review on ethnopharmacological claims,” Life Sciences, vol. 2, no. 6, p. 8, 2011.
View at: Google Scholar
C. R. Sahoo, J. Sahoo, M. Mahapatra et al., “Coumarin derivatives as promising antibacterial agent (s),” Arabian Journal of Chemistry, vol. 14, no. 2, Article ID 102922, 2021.
View at: Publisher Site | Google Scholar
M. Miethke, M. Pieroni, T. Weber et al., “Towards the sustainable discovery and development of new antibiotics,” Nature Reviews Chemistry, vol. 5, no. 10, pp. 726–749, 2021.
View at: Publisher Site | Google Scholar
P. Saranraj and S. Sivasakthi, “Medicinal plants and its antimicrobial properties: a review,” Global Journal of Pharmacology, vol. 8, no. 3, pp. 316–327, 2014.
View at: Google Scholar
R. Barbieri, E. Coppo, A. Marchese et al., “Phytochemicals for human disease: an update on plant-derived compounds antibacterial activity,” Microbiological Research, vol. 196, pp. 44–68, 2017.
View at: Publisher Site | Google Scholar
K. L. Lemle, “Salvia officinalis used in pharmaceutics,” in Proceedings of the IOP Conference Series: Materials Science and Engineering, IOP Publishing, Nanjing, China, August 2018.
View at: Google Scholar
M. S. Abu-Darwish, C. Cabral, I. V. Ferreira et al., “Essential oil of common sage (Salvia officinalis L.) from Jordan: assessment of safety in mammalian cells and its antifungal and anti-inflammatory potential,” BioMed Research International, vol. 2013, Article ID 538940, 9 pages, 2013.
View at: Publisher Site | Google Scholar
L. Moreno, R. Bello, E. Primo-Yifera, and J. Esplugues, “Pharmacological properties of the methanol extract from Mentha suaveolens Ehrh,” Phytotherapy Research, vol. 16, no. 1, pp. 10–13, 2002.
View at: Publisher Site | Google Scholar
F. Brahmi, M. Khodir, C. Mohamed, and D. Pierre, “Chemical composition and biological activities of Mentha species,” Aromatic and Medicinal Plants—Back to Nature, IntechOpen Limited, London, UK, vol. 10, pp. 47–79, 2017.
View at: Google Scholar
M. Sevindik, “Pharmacological properties of mentha species,” Journal of Traditional Medicine & Clinical Naturopathy, vol. 7, no. 1, p. 2, 2018.
View at: Publisher Site | Google Scholar
M. R. González-Tejero, M. Casares-Porcel, C. P. Sánchez-Rojas et al., “Medicinal plants in the mediterranean area: synthesis of the results of the project Rubia,” Journal of Ethnopharmacology, vol. 116, no. 2, pp. 341–357, 2008.
View at: Publisher Site | Google Scholar
M. Mekkaoui, H. Assaggaf, A. Qasem et al., “Ethnopharmacological survey and comparative study of the healing activity of moroccan thyme honey and its mixture with selected essential oils on two types of wounds on albino rabbits,” Foods, vol. 11, no. 1, p. 28, 2021.
View at: Publisher Site | Google Scholar
A. Ed-Dra, F. Rhazi Filali, Lo Presti et al., “Evaluation of chemical composition, antioxidant and anti listeria monocytogenes and Salmonella enterica activity of the essential oil of Mentha pulegium and Mentha suaveolens collected in Morocco,” Article ID 2019050017, 2019.
View at: Google Scholar
N. El Omari, K. Sayah, S. Fettach et al., “Evaluation of in vitro antioxidant and antidiabetic activities of Aristolochia longa extracts,” Evidence-Based Complementary and Alternative Medicine, vol. 2019, Article ID 7384735, 9 pages, 2019.
View at: Publisher Site | Google Scholar
H. N. Mrabti, K. Sayah, N. Jaradat et al., “Antidiabetic and protective effects of the aqueous extract of Arbutus unedo L. in streptozotocin-nicotinamide-induced diabetic mice,” Journal of Complementary and Integrative Medicine, vol. 15, no. 3, 2018.
View at: Publisher Site | Google Scholar
M. Cheesbrough, District Laboratory Practice in Tropical Countries, Cambridge University Press, Cambridge, UK, 2005.
A. Aghraz, Q. Benameur, T. Gervasi et al., “Antibacterial activity of Cladanthus arabicus and Bubonium imbricatum essential oils alone and in combination with conventional antibiotics against Enterobacteriaceae isolates,” Letters in Applied Microbiology, vol. 67, no. 2, pp. 175–182, 2018.
View at: Publisher Site | Google Scholar
A. Ed-Dra, F. R. Filali, V. L. Presti et al., “Effectiveness of essential oil from the Artemisia herba-alba aerial parts against multidrug-resistant bacteria isolated from food and hospitalized patients,” Biodiversitas Journal of Biological Diversity, vol. 22, no. 7, 2021.
View at: Publisher Site | Google Scholar
M. G. Carranza, M. B. Sevigny, D. Banerjee, and L. Fox-Cubley, “Antibacterial activity of native California medicinal plant extracts isolated from Rhamnus californica and Umbellularia californica,” Annals of Clinical Microbiology and Antimicrobials, vol. 14, no. 1, p. 29, 2015.
View at: Publisher Site | Google Scholar
A. L. Demain and A. Fang, “The natural functions of secondary metabolites,” History of Modern Biotechnology, vol. 69, pp. 1–39, 2000.
View at: Google Scholar
M. Božović, A. Pirolli, and R. Ragno, “Mentha suaveolens Ehrh. (Lamiaceae) essential oil and its main constituent piperitenone oxide: biological activities and chemistry,” Molecules, vol. 20, no. 5, pp. 8605–8633, 2015.
View at: Publisher Site | Google Scholar
M. Grdiša, M. Jug-Dujaković, M. Lončarić et al., “Dalmatian sage (Salvia officinalis L.): a review of biochemical contents, medical properties and genetic diversity,” Agriculturae Conspectus Scientificus, vol. 80, no. 2, pp. 69–78, 2015.
View at: Google Scholar
F. Z. El Hassani, “Characterization, activities, and ethnobotanical uses of Mentha species in Morocco,” Heliyon, vol. 6, no. 11, Article ID e05480, 2020.
View at: Publisher Site | Google Scholar
S. Miraj and S. Alesaeidi, “A review study of therapeutic effects of Salvia officinalis L,” Electronic Physician, vol. 8, no. 9, pp. 3024–3031, 2016.
View at: Publisher Site | Google Scholar
H. Gong, L. He, Z. Zhao, X. Mao, and C. Zhang, “The specific effect of (R)-(+)-pulegone on growth and biofilm formation in multi-drug resistant Escherichia coli and molecular mechanisms underlying the expression of pgaABCD genes,” Biomedicine & Pharmacotherapy, vol. 134, Article ID 111149, 2021.
View at: Publisher Site | Google Scholar
T. K. S. Janssens, O. Tyc, H. Besselink, W. de Boer, and P. Garbeva, “Biological activities associated with the volatile compound 2, 5-bis (1-methylethyl)-pyrazine,” FEMS Microbiology Letters, vol. 366, no. 3, 2019.
View at: Publisher Site | Google Scholar
P. Kusstatscher, T. Cernava, S. Liebminger, and G. Berg, “Replacing conventional decontamination of hatching eggs with a natural defense strategy based on antimicrobial, volatile pyrazines,” Scientific Reports, vol. 7, no. 1, pp. 1–8, 2017.
View at: Google Scholar
V. B. Rychen, M. de Lourdes Bastos, G. Bories, P. S. Cocconcelli, G. Flachowsky, and J. Gropp, “Safety and efficacy of pyrazine derivatives including saturated ones belonging to chemical group 24 when used as flavourings for all animal species,” EFSA Journal, vol. 15, no. 2, Article ID e04671, 2017.
View at: Google Scholar
M. Schöck, S. Liebminger, G. Berg, and T. Cernava, “First evaluation of alkylpyrazine application as a novel method to decrease microbial contaminations in processed meat products,” AMB Express, vol. 8, no. 1, pp. 1–7, 2018.
View at: Google Scholar
H. Shu, H. Chen, X. Wang et al., “Antimicrobial activity and proposed action mechanism of 3-Carene against Brochothrix thermosphacta and Pseudomonas fluorescens,” Molecules, vol. 24, no. 18, p. 3246, 2019.
View at: Google Scholar
C. Xiong, Q. Li, S. Li, C. Chen, Z. Chen, and W. Huang, “In vitro antimicrobial activities and mechanism of 1-octen-3-ol against food-related bacteria and pathogenic fungi,” Journal of Oleo Science, vol. 66, no. 9, pp. 1041–1049, 2017.
View at: Publisher Site | Google Scholar
S. Makar, T. Saha, and S. K. Singh, “Naphthalene, a versatile platform in medicinal chemistry: sky-high perspective,” European Journal of Medicinal Chemistry, vol. 161, pp. 252–276, 2019.
View at: Publisher Site | Google Scholar
S. Nencetti, L. Ciccone, A. Rossello, E. Nuti, C. Milanese, and E. Orlandini, “Synthesis and cycloxygenase inhibitory properties of new naphthalene-methylsulfonamido, naphthalene-methylsulfonyl and tetrahydronaphthalen-methylsulfonamido compounds,” Journal of Enzyme Inhibition and Medicinal Chemistry, vol. 30, no. 3, pp. 406–412, 2015.
View at: Publisher Site | Google Scholar
W. Mączka, A. Duda-Madej, A. Górny, M. Grabarczyk, and K. Wińska, “Can eucalyptol replace antibiotics?” Molecules, vol. 26, no. 16, p. 4933, 2021.
View at: Publisher Site | Google Scholar
P. R. Freitas, A. C. J. de Araújo, C. R. Barbosa et al., “Inhibition of efflux pumps by monoterpene (α-pinene) and impact on Staphylococcus aureus resistance to tetracycline and erythromycin,” Current Drug Metabolism, vol. 22, no. 2, pp. 123–126, 2021.
View at: Publisher Site | Google Scholar
J. Kovač, K. Šimunović, Z. Wu et al., “Antibiotic resistance modulation and modes of action of (-)-α-pinene in campylobacter jejuni,” PLoS One, vol. 10, no. 4, Article ID e0122871, 2015.
View at: Publisher Site | Google Scholar
W. K. Shiu, J. P. Malkinson, M. M. Rahman et al., “A new plant-derived antibacterial is an inhibitor of efflux pumps in Staphylococcus aureus,” International Journal of Antimicrobial Agents, vol. 42, no. 6, pp. 513–518, 2013.
View at: Publisher Site | Google Scholar
S. S. Dahham, Y. M. Tabana, M. A. Iqbal et al., “The anticancer, antioxidant and antimicrobial properties of the sesquiterpene β-caryophyllene from the essential oil of Aquilaria crassna,” Molecules, vol. 20, no. 7, pp. 11808–11829, 2015.
View at: Publisher Site | Google Scholar
A. Mathlouthi, N. Saadaoui, and M. Ben-Attia, “Essential oils from Artemisia species inhibit biofilm formation and the virulence of Escherichia coli EPEC 2348/69,” Biofouling, vol. 37, no. 2, pp. 174–183, 2021.
View at: Publisher Site | Google Scholar
S. Tariq, S. Wani, W. Rasool et al., “A comprehensive review of the antibacterial, antifungal and antiviral potential of essential oils and their chemical constituents against drug-resistant microbial pathogens,” Microbial Pathogenesis, vol. 134, Article ID 103580, 2019.
View at: Publisher Site | Google Scholar
A. D. Association, “4. Lifestyle management: standards of medical care in diabetes—2018,” Diabetes Care, vol. 41, no. 1, pp. S38–S50, 2018.
View at: Google Scholar
L. I. Hudish, J. E. Reusch, and L. Sussel, “β Cell dysfunction during progression of metabolic syndrome to type 2 diabetes,” Journal of Clinical Investigation, vol. 129, no. 10, pp. 4001–4008, 2019.
View at: Publisher Site | Google Scholar
N. Eguchi, N. D. Vaziri, D. C. Dafoe, and H. Ichii, “The role of oxidative stress in pancreatic β cell dysfunction in diabetes,” International Journal of Molecular Sciences, vol. 22, no. 4, p. 1509, 2021.
View at: Publisher Site | Google Scholar
A. G. El-Shemi, O. A. Kensara, A. Alsaegh, and M. H. Mukhtar, “Pharmacotherapy with thymoquinone improved pancreatic β-cell integrity and functional activity, enhanced islets revascularization, and alleviated metabolic and hepato-renal disturbances in streptozotocin-induced diabetes in rats,” Pharmacology, vol. 101, no. 1-2, pp. 9–21, 2018.
View at: Publisher Site | Google Scholar
S. Kumar, A. Mittal, D. Babu, and A. Mittal, “Herbal medicines for diabetes management and its secondary complications,” Current Diabetes Reviews, vol. 17, no. 4, pp. 437–456, 2021.
View at: Publisher Site | Google Scholar
N. Nazir, M. Zahoor, F. Uddin, and M. Nisar, “Chemical composition, in vitro antioxidant, anticholinesterase, and antidiabetic potential of essential oil of Elaeagnus umbellata Thunb,” BMC Complementary Medicine and Therapies, vol. 21, no. 1, p. 73, 2021.
View at: Publisher Site | Google Scholar
R. Ullagaddi, P. Mahendrakar, and A. Bondada, “Efficacy of mint (Mentha spicata L.) leaves in combating oxidative stress in type 2 diabetes,” Life Sciences, vol. 1, pp. 1–7, 1999.
View at: Google Scholar
M. Bayani, M. Ahmadi-Hamedani, and A. J. Javan, “Study of hypoglycemic, hypocholesterolemic and antioxidant activities of Iranian Mentha spicata leaves aqueous extract in diabetic rats,” Iranian Journal of Pharmaceutical Research: Iranian Journal of Pharmaceutical Research, vol. 16, pp. 75–82, 2017.
View at: Google Scholar
M. S. Hooda, R. Pal, A. Bhandari, and J. Singh, “Antihyperglycemic and antihyperlipidemic effects of Salvadora persica in streptozotocin-induced diabetic rats,” Pharmaceutical Biology, vol. 52, no. 6, pp. 745–749, 2014.
View at: Publisher Site | Google Scholar
L. T. Al Kury, A. Abdoh, K. Ikbariah, B. Sadek, and M. Mahgoub, “In vitro and in vivo antidiabetic potential of monoterpenoids: an update,” Molecules, vol. 27, no. 1, p. 182, 2021.
View at: Publisher Site | Google Scholar
M. Zielińska-Błajet and J. Feder-Kubis, “Monoterpenes and their derivatives—recent development in biological and medical applications,” International Journal of Molecular Sciences, vol. 21, no. 19, p. 7078, 2020.
View at: Publisher Site | Google Scholar
I. W. G. Gunawan, A. A. B. Putra, and I. A. G. Widihati, “The response to oxidative stress α-Humulene compounds Hibiscus Manihot L. leaf on the activity of 8-Hydroxy-2-Deoksiquanosin levels pancreatic β-cells in diabetic rats,” Biomedical and Pharmacology Journal, vol. 9, no. 2, pp. 433–441, 2016.
View at: Publisher Site | Google Scholar
H. P. T. Wathsara, H. D. Weeratunge, M. N. A. Mubarak, P. I. Godakumbura, and P. Ranasinghe, “In vitro antioxidant and antidiabetic potentials of Syzygium caryophyllatum L. Alston,” Evidence-Based Complementary and Alternative Medicine, vol. 2020, Article ID 9529042, 15 pages, 2020.
View at: Publisher Site | Google Scholar
F. B. Saraiva, A. C. C. de Araújo, A. de Araújo, and J. P. M. Senna, “Monoclonal antibody anti-PBP2a protects mice against MRSA (methicillin-resistant Staphylococcus aureus) infections,” PLoS One, vol. 14, no. 11, Article ID e0225752, 2019.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2022 Samiah Hamad Al-Mijalli et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies

Views

1296

Downloads

981

Citations