Journal of Chemistry

Journal of Chemistry / 2021 / Article

Research Article | Open Access

Volume 2021 |Article ID 8840998 |

H. El hassouni, M. Bouhrim, R. El hajji, M. Bnouham, A. Ziyyat, A. Romane, "Characterization of an Endemic Plant Origanum grosii from Morocco: Trace Element Concentration and Antihyperglycemic Activities", Journal of Chemistry, vol. 2021, Article ID 8840998, 10 pages, 2021.

Characterization of an Endemic Plant Origanum grosii from Morocco: Trace Element Concentration and Antihyperglycemic Activities

Academic Editor: Murat Senturk
Received11 Sep 2020
Revised31 Mar 2021
Accepted17 Apr 2021
Published26 Apr 2021


Origanum genus is one of the most widely used herbs in folk medicine for its biological properties. The present investigation aims to characterize, for the first time, endemic Origanum grosii collected from the Taounate region, Morocco. This characterization was realized by determining the concentration of metals in different parts of the plant (flowers, leaves, and stems) by ICP-MS, and the results were studied statistically by Principal Component Analysis (PCA). Phytochemical screening with the dosage of polyphenols and flavonoids has been conducted. To know more about this species, antihyperglycemic tests have been performed to highlight the presence or absence of the antidiabetic effect for this plant. An Oral Glucose Tolerance Test (OGTT) has been performed on normal mice which were divided into two groups of six mice each. Group 1 (control group) was treated with distilled water, and group 2 was treated with an aqueous extract of O. grosii by gavage at 150 mg/kg. Digestive enzyme α-amylase inhibition assay has also been evaluated to study the inhibition effect of the studied extract using acarbose as a control. The results showed that the leaves exhibited a high concentration of trace elements (Ca, Mg, and K) and total absence of heavy metals, which were found in small quantities (Cr, Ni, and B) on the stems, and this makes the plant safe to use. On the other hand, tannins, flavonoids, triterpenes, and steroids were the major families strongly present in this species. The antidiabetic results showed that O. grosii have significantly reduced postprandial hyperglycemia after glucose loading in normal rats. It showed also that this species has a significant antihyperglycemic activity reflected by the inhibition of α-amylase. The one responsible for this property could be the synergy between the trace elements and the nature of the chemical families of O. grosii species, which can make this plant useful in the management of postprandial hyperglycemia.

1. Introduction

Medicinal plants have been used in folk medicine against a lot of diseases for thousands of years [13]. It has been confirmed by the World Health Organization (WHO) that approximately 80% of people traditionally use medicinal and aromatic herbs for the treatment of many diseases [4].

The herbals unfortunately also have side effects, such as nature and concentration of the mineral components. Some metals as As, Cd, Hg, Pb, or Se are not essential for plant growth. Others such as Co, Cu, Fe, Mn, Mo, Ni, and Zn are essential elements required for normal growth and metabolism of plants, but when their concentration is greater than optimal values, these elements can easily lead to poisoning [59]. On the other hand, there are the wild dumps that constitute chemical contamination, especially of heavy metals, and accumulates in the soil and under certain biogeochemical conditions can pass into the soil solution [10, 11] and, therefore, become bioavailable and absorbed by plants [12].

In this sense, scientific researchers have been obliged to fix norms in terms of plant mineral composition; for example, the WHO declared that the presence of heavy metals should be checked for some medicinal plants used as ingredients in herbal formulations (teas, tinctures, etc.) [13]. Therefore, we should check the heavy metal concentrations in medicinal plants and their products to ensure the safety and efficacy of herbal products [2, 14].

On the other hand, the advantages of medicinal plants are enormous, especially in the pharmacological sector by discovering new components coming from natural sources to fight against several diseases [1518]. Besides, to determine the chemical profile and composition of medicinal plants, several studies show the complexity and variety of compounds that all contribute to the various uses of plants in the processing of many foods, including life-threatening diseases such as AIDS, cancer, and diabetes [2, 19].

Diabetes is one of the oldest diseases whose devastating effect is increasing day by day and severely at an epidemic level [20]. Generally, there are two types of diabetes: type 1 diabetes is an autoimmune disease in which the β cells of the pancreas do not produce sufficient insulin (a hormone that helps use blood sugar (glucose) for energy). Type 2 diabetes is the interaction between several genetic and environmental factors that results in a heterogeneous and progressive disorder with variable degrees of insulin resistance and pancreatic β-cell dysfunction. When β cells are not longer able to secrete sufficient insulin to overcome insulin resistance, impaired glucose tolerance progresses to type 2 diabetes [21].

This disease is the most frequent in the world affecting 7% of the population or 285 million people worldwide. It is predicted that this number will exceed 435 million in 2030 [22].

Despite the use of hypoglycemic as antidiabetic drugs, diabetes and its complications constitute a major problem in the therapeutic management of diabetics and the success of treatment would be more interesting. Despite the progress of new therapeutic molecules, modern drugs, including insulin and oral hypoglycemic agents, have shown an unwanted effect when administered regularly [23, 24]. Recently, diabetologists conclude that a therapeutic complement consisting of plant extracts is necessary to optimize the treatment of diabetes [25, 26] due to their perceived effectiveness, safety, affordability, and acceptability, with minimal side effects in clinical experience and relatively low cost [27, 28]. The World Health Organization recommends the use of traditional and plant-based medicines for the management of diabetes mellitus [29].

The Origanum genus is among the plants whose antidiabetic properties are well known [30, 31]. This genus is presented in five species in Morocco; three of them are endemic, O. compactum, O. elongatum, and O. grosii, which are our interest in this paper [32]. To the best of our knowledge, no pharmacological work was carried out on the species O. grosii to characterize and evaluate this species. This work has two objectives: firstly, determining, by ICP-MS, its mineral proportions, trace elements, and heavy metals to ensure the safe and efficient use of the plant in therapeutic medicine. After determining the chemical families of the studied plant via photochemical screening and the dosage of polyphenols and flavonoids, our second objective will aim to evaluate the plant by studying its antihyperglycemic activities by two tests: an Oral Glucose Tolerance Test (OGTT), in normal mice, and α-amylase inhibition assay.

2. Materials and Methods

2.1. Plant Materiel

The aerial part of O. grosii was harvested during the flowering period when it produces normally maximal biomass. It was collected in July 2015 from the Taounate region (Taher souk), Morocco. The species was identified in the scientific institute of Rabat in Morocco; the Voucher specimens (99125) were deposited in its herbarium.

2.2. The Analysis of Metals by ICP-MS Methods
2.2.1. Devices and Reagents

In this study, a Thermo Fisher X Series II (Thermo Fisher Scientific, Bremen, Germany) with an autosampler ASX-510 (Cetac, Omaha, Nebraska, USA) was used in standard configuration. The instrument was equipped with a standard monobloc torch with a quartz injector tube (internal diameter: 1.5 mm).

The introduction system is composed of a Micromist microcentric nebulizer (Glass Expansion, USA) associated with a so-called Scott double passage nebulization chamber cooled to 2°C by the Peltier effect.

The instrument was optimized (daily performance) to give maximum sensitivity to M+ ions and double ionization and oxides, controlled by rations between Ba2+/Ba+ and Ce2+/CeO+ respectively, these being always less than 2%. The experimental conditions were argon debit on a nebulizer (0.8 L·min−1), auxiliary gas debit 0.84 L·min−1, argon debit in plasma 4.5 L·min−1, lens voltage 7.30 V, power RF in plasma 1100 W, and the sampling depth (cone-torch distance) of 9 mm.

All reagents are of analytical quality. For the preparation of the solutions and the cleaning of the materials, we used ultrapure water with a conductivity <1 μs·cm−1 obtained by purifying the demineralized water with Milli-QTM PLUS and nitric acid (67% v/v) purified.

2.2.2. Sample Digestion Procedure

Acid digestion on a hot plate was performed following the protocol of Schwartz [33, 34]; each sample was digested in a mixture of nitric acid, sulfuric acid, and oxygenated water. The samples are then heated slowly to 95°C following a temperature ramp of 2°C·min−1 using a digestion block (SCP Science, Montreal, QC) to avoid too strong reactions. The temperature of 95°C was maintained for 40 min until the appearance of the samples became constant. The residues were washed with nitric acid at 50% v/v. The supernatants were filtered using Whatman filter paper to minimize the number of microparticles during the analysis that could block the liquid sample intake or interfere with the nebulization of the solution by the plasma used for the ICP-MS methods. The solutions are filtered and eviolated in a plastic flask. Internal standards are added to the samples at a concentration of 5 μg·L−1.

2.3. Statistical Study: PCA

To treat the results of metals analysis, we used statistical studies by the software R for chemometric analysis. The loading plot tool in PCA was used to show the relationship between variables (metals) and how significant each variable was for each principal component. Also, the plot of variables (correlation plot) was used to study the dimensions and their correlation with metals. Also, the plot of individuals was used to identify groups of individuals (three parts of the plant) with similarity [9, 35, 36].

2.4. Characterization of Chemical Families
2.4.1. Phytochemical Screening

The objective of phytochemical screening tests is to determine the presence or absence of some chemical families in the studied plants such as alkaloids, tannins, flavonoids, anthocyanins, leucoanthocyanines, coumarins, quinones, terpenoids, steroids, triterpenoids, carotenoids, and saponins [37, 38].

2.4.2. Polyphenol and Flavonoid Dosage

To determine the total content of polyphenols, we used the Folin–Ciocalteu method. 100 μL of the diluted extract was mixed with 2.5 mL of Folin–Ciocalteu reagent and 2.5 mL of Na2CO3 solution. The mixture was incubated in darkness for 1 h, and then, the absorbance was measured at 515 nm. As a standard, we used gallic acid. The results were expressed as mg of gallic acid equivalent per gram of dry weight (mg GAE/g DW) [39, 40].

Concerning the flavonoid content, we used the colorimetric method of aluminum trichloride. We mixed 100 µL of extract with 0.4 mL of distilled water, 0.003 mL of NaNO2 solution (5%), and 0.02 mL of AlCl3 solution (10%); after 5 min, we added to the mixture 0.2 mL of Na2CO3 solution (1 M) and 0.25 mL of distilled water. The absorbance was measured at 510 nm, and quercetin was used as standard. The results were expressed as mg of quercetin equivalent per gram of extract weight (mg QE/g DW) [41].

2.5. Antidiabetic Activities
2.5.1. Oral Glucose Tolerance Test (OGTT), in Normal Mice

The antihyperglycemic effect of aqueous extract was evaluated as described by several others [27, 42, 43]. Normal mice (180–250 g) fasted for 14 h before experimentation but were allowed free access to water. The animals were divided into two groups of six mice each. Group 1 (control group) was treated with distilled water (10 mL/kg). Group 2 was treated with an aqueous extract of O. grosii by gavage at 150 mg/kg. All animals were orally loaded with glucose (2 g/kg of body weight) 30 minutes after treatment. Afterward, the blood glucose variation was monitored for 2 hours.

2.5.2. Inhibitory Effect of the Plant of Pancreatic Alpha-Amylase Enzyme Activity

The α-amylase inhibition assay was conducted according to some reporters [44, 45], with some modifications. Briefly, 200 μL of the sample (dissolved in phosphate buffer solution, the concentrations have been prepared from 3.33 to 1.66 mg/ml) was mixed with 200 μL of α-amylase (13 IU/ml, in 0.02 M phosphate buffer solution (PBS), pH 6.9). After incubating at 37°C for 10 min, 200 μL of 1% (w/v) soluble starch (in 0.02 M PBS, pH 6.9) was added and the mixture was further incubated at 37°C for 15 min, followed by adding 250 μL of dinitrosalicylic acid color reagent (DNS 1 g in 40 mL of distilled water, 30 g Na-K tartrate, 2 N NaOH), and stopped by heating in a boiling water bath for 8 min. After cooling to room temperature, the mixture has been diluted with 1 mL of PBS and the absorbance was measured at 540 nm.

The inhibition percentage (%) was calculated by the following equation:

Absorbances are abbreviated as follows: (control), (control blank), (sample), and (sample blank).

3. Results and Discussion

3.1. The Mineral Composition Analyzed by ICP-MS

All results are summarized in Table 1. The results showed that Ca, K, and Mg present higher mineral values in the species.

Mean (mg/kg)S.D (mg/kg)Mean (mg/kg)S.D (mg/kg)Mean (mg/kg)S.D (mg/kg)


To understand and treat these results, we used the statistical study (PCA).

3.2. Principal Component Analysis (PCA)

Table 2 shows that only the first two components have eigenvalues greater than 1. This implies that these two components can be considered for the explanation of the data variability.

Component numberEigenvaluePercentage of variance explained (%)Cumulative percentage (%)

Dimension 19.9008255.0045555.00456
Dimension 22.6275314.5974369.60199
Dimension 30.995235.5291175.13110
Dimension 40.862804.7933479.92444
Dimension 50.784314.3573284.28176
Dimension 60.558073.1004087.38217
Dimension 70.484692.6927290.07489
Dimension 80.401402.2300292.30492
Dimension 90.298461.6581393.96305

Figure 1 reveals the existence of correlations between most metals that are positively correlated with CP1 such as Ca, Fe, Zn, Al, Na, Mn, and Sr and Ba, As, Pb, and Si which are positively correlated with CP2, although, Cr, B, and, maybe, Ni are negatively correlated with CP2.

3.2.1. Study of Individuals

From Figure 2, it is very clear that there is a birth of three groups, the leaves are presented on the right of the first component as the first group and the stems are formed as the second group on the left of the first component, while the flowers which are in the third group are placed at the bottom of the second component.

For a better and clear explication of these separations, we associated the variables (metals) and individuals (three parts of the plant) into a single figure:

By superposing the score and loading plots, we have obtained the biplot (Figure 3).

According to this graph and Figure 4 which shows the distribution of metals by size, we find that the majority of metals, especially trace elements that are positively correlated to CP1, are concentrated at the leaves and they are completely absent from the toxic metals. On the other hand, these heavy metals (As and Cr) were presented at the stems.

From these figures, it is clear that the leaves are the richest part in trace elements which makes them the most important part in the plant. It is also necessary to mention that the concentration of heavy metals in the stems did not exceed the optimal values declared by the WHO, which does not make this plant toxic for human.

3.3. Characterization of Chemical Families

To have a better view of the chemical families present in this plant, we carried out some phytochemical screening tests summarized in Table 3.




O-hétérosides à génine réduite

According to the table, tannins, flavonoids, triterpenes, and steroids are the most chemical families present in the leaves. However, tannins, triterpenes, and steroids were also present in the steams but in lesser quantities. Our results were not very different comparing with several studies conducted on other species [46, 47].

According to these results, we will be focused on the leaves’ composition. Table 4 presents its content of polyphenols and flavonoids.

Polyphenols (mgGAE/g)Flavonoids (mgQE/g)

136.5 ± 1.250.1 ± 2.0

This work was compared to other studies conducted on the same genus studied by Bouyahya et al. who declared that O. compactum had less concentration of polyphenols and flavonoids compared to our results, 117.6 mg EAG/g and 27.6 mg EQ/g, respectively [46].

3.4. Antidiabetic Activities
3.4.1. Glucose Tolerance and Antihyperglycemic Effect

The results presented in Figure 5 showed that, in the control group, the postprandial hyperglycemia level caused by 2 mg/kg of glucose at 30 min loading reached 180 mg/dL after glucose administration. At 90 min, it increased to 140 mg/dL and then decreased to reach an average of 118 mg/dL at 150 min after loading. However, O. grosii extract at a dose of 150 mg/kg suppressed significantly the postprandial hyperglycemia level compared with the normal control group as indicated in Figure 5. The area under the curve of glucose tolerance (AUC glucose) for the O. grosii-extract-treated group was significantly lower than that of the normal control group; this result presents an antihyperglycemic effect of this species. These results were similar compared to another study conducted on Mexican oregano for normal and diabetic fasting mice [48] and also another study conducted on another plant which was less than 125 mg/dL [49]. According to several works [50, 51], this may be due to the presence of a large hypoglycemic chemical family such as flavonoids, terpenes, and tannins which are present in our species (phytochemical screening results). Those components improve the performance of pancreatic tissues by increasing insulin secretion or decreasing the intestinal absorption of glucose [52]. For this reason, our study needs more advanced research. Overall, for some authors, Lamiaceae is among the families of plants with the most potent hypoglycemic effects included [53, 54].

3.4.2. Alpha-Amylase Inhibitor Activity

Percent alpha-amylase inhibition of the studied species was plotted as a function of concentration in comparison with acarbose, as shown in Figure 6. The inhibitory effect of the studied plant was inferior to that of acarbose. The results indicate that the plant extract (3.33 mg/ml) had a good exhibition anti-alpha-amylase activity compared to that of the lower concentration (1.66 mg/ml).

To control postprandial glycemic levels for the management of diabetes, the inhibition of digestive enzymes is a great strategy for glucose control [55], α-amylase, which results in a significant reduction in postprandial blood glucose, presenting an important goal in diabetes management [56]. In addition, a microbial pseudotetrasaccharide, acarbose, inhibits the brush border enzymes glucoamylase, dextrinase, maltase, and sucrase, as well as pancreatic α-amylase [55]. Despite the effectiveness of acarbose as an antidiabetic drug, alternative foods are necessary. Moreover, due to the side effects of acarbose and rare cases of hepatotoxicity which have been recorded as a result of long-term consummation [44], scientists are interested in nutritional therapies and functional foods with preventive effects on diabetes and obesity [56]. Few articles have described the inhibitory activities of the Origanum genus [30, 57]. Yet, none of the previous studies have been recorded on the O. grosii species. As is known, Origanum leaves are currently used for the treatment of type 1 and type 2 diabetes mellitus [30, 31, 58]. The dose of Origanum used (20 mg/kg) is effective for 2 weeks to normalize blood glucose levels in severely diabetic rats. We can report that the antihyperglycemic effect of Origanum is very potent and cumulative. The plant extract also can be effective as an inhibitor of renal tubular glucose reabsorption [58, 59].

The present study indicated that Origanum grosii species could be useful in the management of postprandial hyperglycemia. The antienzymatic activity of the species is probably due to its phenolic content, which necessitates a deep study on this activity, as well as a chemical separation that will allow the extraction of compounds responsible for this property.

Minerals and trace elements are important agents for biochemical reactions. They are considered to be a stabilizer of enzymes and proteins as cofactors. Many trace elements affected the biological processes by binding the receptor site of the cell membrane or preventing the entry of particular molecules into the cell by changing the shape of the receptor [60]. Macroelements, primarily calcium (Ca), potassium (K), magnesium (Mg), chloride (Cl), phosphorous (P), sodium (Na), and iron (Fe), and certain trace elements such as cobalt (Co), boron (B), chromium (Cr), copper (Cu), sulfur (S), iodine (I), zinc (Zn), and molybdenum (Mo), enhance insulin action by activating insulin receptor sites [6163].

Several works explained the relation between the trace elements (Zn, Cr, and Mg) and the antidiabetic activity. They explained also the deficiency of some trace elements in diabetic patients that play a great role in the development of diabetes mellitus [6467]. Ahmed et al. reported that several trace elements are significantly reduced in people with diabetes mellitus [67, 68]. Also, other work reported that the trace elements Ca and K regulate voltage-dependent channels in pancreatic β-cells, which are essential for insulin exocytosis [6971]. Ekmekcioglu et al. indicated that potassium’s role in the control of blood glucose is grounded in its function at a cellular level where potassium-induced cell depolarization results in insulin secretion from pancreatic β cells [72]. Similarly, Stone reported that the appropriate potassium intake may influence the control of glucose, limiting, therefore, the risk of diabetes, especially in those on thiazide diuretic treatment and those already at higher risk from the development of additional comorbidities [73]. Also, Helderman et al. confirm the impact of potassium on the thiazide administration used to decrease glucose [74]. Other studies have shown a complex association between calcium levels and the pathogenesis of diabetes. The decreased β-cells’ function was related to abnormal calcium regulation [63, 75].

The research mentioned above proved the principal protective role of trace elements against diabetes mellitus. Then, the plants which have insulin-mimetic, hypoglycemic, and antidiabetic properties may conduct them by helpful effects of trace element contents.

4. Conclusions

In conclusion, the mineral composition of O. grosii did not exceed the limit values required by the WHO, which makes it safe for human use. Origanum is one of the natural herbal medicines rich in antidiabetic compounds (flavonoids, tannins, and phenolic) that improve the performance of pancreatic tissues by increasing the insulin secretion or decreasing the intestinal absorption of glucose, and the antihyperglycemic action of this plant can be partially attributed to the inhibition of α-amylase or other enzymes. The chemical families of the Origanum plant could act separately or in synergy to cause the hypoglycemic effect of the genus. Besides, other studies are necessary to determine the chemical composition and separate the active components of plants, to identify the compounds responsible for this activity. Moreover, because of trace element variations between the studied plants, the hypoglycemic effect of these herbs is not due to a unique element present in the herbs, rather a synergic effect of several elements that might account for the hypoglycemic nature of these plants. Other works are necessary to evaluate this phenomenon. Hence, based on the found results, it is approved to say that the studied species might be used in diabetes treatments without ignoring testing its toxicity on humans.

Data Availability

No data were used in this study.

Conflicts of Interest

The authors declare that they have no conflicts of interest.


  1. N. H. Rakotoarivelo, F. Rakotoarivony, A. V. Ramarosandratana et al., “Medicinal plants used to treat the most frequent diseases encountered in Ambalabe rural community, Eastern Madagascar,” Journal of Ethnobiology and Ethnomedicine, vol. 11, p. 68, 2015. View at: Publisher Site | Google Scholar
  2. R. A. Street and G. Prinsloo, “Commercially important medicinal plants of South Africa: a review,” Journal of Chemistry, vol. 2013, Article ID 205048, 16 pages, 2013. View at: Publisher Site | Google Scholar
  3. W. Abdelli, F. Bahri, A. Romane et al., “Chemical composition and anti-inflammatory activity of Algerian thymus vulgaris essential oil,” Natural Product Communications, vol. 12, no. 4, pp. 611–614, 2017. View at: Publisher Site | Google Scholar
  4. A. Shah, A. Niaz, N. Ullah et al., “Comparative study of heavy metals in soil and selected medicinal plants,” Journal of Chemistry, vol. 2013, Article ID 621265, 5 pages, 2013. View at: Publisher Site | Google Scholar
  5. I. Khan, J. Ali, and H. Tullah, “Heavy metals determination in medicinal plant Withania somnifera growing in various areas of Peshawar, NWFP,” Journal of the Chemical Society of Pakistan, vol. 30, pp. 69–74, 2008. View at: Google Scholar
  6. J. Singh and A. S. Kalamdhad, “Effects of heavy metals on soil, plants, human health and aquatic life,” International Journal of Research in Chemistry and Environment, vol. 1, pp. 15–21, 2011. View at: Google Scholar
  7. M. Y. Arjouni, M. A. Bennouna, M. A. El Alaoui El Fels, and A. Romane, “Assessment of mineral elements and heavy metals in leaves of indigenous cypress of High Atlas Mountains,” Natural Product Research, vol. 29, no. 8, pp. 764–767, 2015. View at: Publisher Site | Google Scholar
  8. F. A. Ababneh, “The hazard content of cadmium, lead, and other trace elements in some medicinal herbs and their water infusions,” International Journal of Analytical Chemistry, vol. 2017, Article ID 6971916, 8 pages, 2017. View at: Publisher Site | Google Scholar
  9. M. Ouknin, A. Romane, M. Y. Arjouni, and L. Majid, “Mineral composition, multivariate analysis of some oligo-elements and heavy metals in some species of genus thymus,” Journal of Materials and Environmental Science, vol. 9, pp. 980–985, 2018. View at: Publisher Site | Google Scholar
  10. M. J. Mench, A. Manceau, J. Vangronsveld, H. Clijsters, and B. Mocquot, “Capacity of soil amendments in lowering the phytoavailability of sludge-borne zinc,” Agronomie, vol. 20, no. 4, pp. 383–397, 2000. View at: Publisher Site | Google Scholar
  11. D. Zmirou, P. D. C. Beausoleil, I. Deportes et al., Environnement et Santé Publique Fondements et Pratiques, University of Montreal, Montreal, Canada, 2003.
  12. S. Belabed, B. Lotmani, and A. Romane, “Assessment of metal pollution in soil and in vegetation near the wild garbage dumps at Mostaganem region,” Journal of Materials and Environmental Science, vol. 5, pp. 1551–1556, 2014. View at: Google Scholar
  13. A. Stanojkovic-sebic, R. Pivic, D. Josic, Z. Dinic, and A. Stanojković, “Heavy metals content in selected medicinal plants commonly used as components for herbal formulations,” Tarim Bilimleri Dergisi, vol. 21, pp. 317–325, 2014. View at: Publisher Site | Google Scholar
  14. K. A. Steindor, I. J. Franiel, W. M. Bierza, B. Pawlak, and B. F. Palowski, “Assessment of heavy metal pollution in surface soils and plant material in the post-industrial city of Katowice, Poland,” Journal of Environmental Science and Health, Part A, vol. 51, no. 5, pp. 371–379, 2016. View at: Publisher Site | Google Scholar
  15. H. A. E. Shaaban, A. H. El-Ghorab, and T. Shibamoto, “Bioactivity of essential oils and their volatile aroma components: review,” Journal of Essential Oil Research, vol. 24, no. 2, pp. 203–212, 2012. View at: Publisher Site | Google Scholar
  16. A. Ouarhach, J. Costa, and A. Romane, “Chemical profiling of Lavandula maroccana of Morocco,” Chemistry of Natural Compounds, vol. 56, no. 2, pp. 348–350, 2020. View at: Publisher Site | Google Scholar
  17. A. Sayout, A. Ouarhach, I. Dilagui, N. Soraa, and A. Romane, “Antibacterial activity and chemical composition of essential oil from Lavandula tenuisecta Coss.ex Ball. an endemic species from Morocco,” The European Journal of Integrative Medicine, vol. 33, p. 101017, 2019. View at: Publisher Site | Google Scholar
  18. A. Sayout, A. Ouarhach, R. Rabie, I. Dilagui, N. Soraa, and A. Romane, “Evaluation of antibacterial activity of Lavandula pedunculata subsp. atlantica (Braun-Blanq.) romo essential oil and selected terpenoids against resistant bacteria strains–structure–activity relationships,” Chemistry and Biodiversity, vol. 17, p. 1900496, 2020. View at: Publisher Site | Google Scholar
  19. E. P. Rybicki, R. Chikwamba, M. Koch, J. I. Rhodes, and J.-H. Groenewald, “Plant-made therapeutics: an emerging platform in South Africa,” Biotechnology Advances, vol. 30, no. 2, pp. 449–459, 2012. View at: Publisher Site | Google Scholar
  20. S. Wild, G. Roglic, A. Green, R. Sicree, and H. King, “Global prevalence of diabetes: estimates for the year 2000 and projections for 2030,” Diabetes Care, vol. 27, no. 5, pp. 1047–1053, 2004. View at: Publisher Site | Google Scholar
  21. A. A. Siddiqui, S. A. Siddiqui, S. Ahmad, S. Siddiqui, I. Ahsan, and K. Sahu, “Diabetes: mechanism, pathophysiology and management-a review,” International Journal of Drug Development & Research, vol. 5, pp. 1–23, 2013. View at: Google Scholar
  22. World Health Organization, Diabetes Fact Sheet No 312, World Health Organization, Geneva, Switzerland, 2011.
  23. P. J. Grant, “Beneficial effects of metformin on haemostasis and vascular function in man,” Diabetes & Metabolism, vol. 29, no. 4, pp. 6S44–6S52, 2003. View at: Publisher Site | Google Scholar
  24. C. J. Bailey, “Metformin: effects on micro and macrovascular complications in type 2 diabetes,” Cardiovascular Drugs and Therapy, vol. 22, no. 3, pp. 215–224, 2008. View at: Publisher Site | Google Scholar
  25. H. Pareek, S. Sharma, B. S. Khajja, K. Jain, and G. Jain, “Evaluation of hypoglycemic and anti-hyperglycemic potential of Tridax procumbens (Linn.),” BMC Complementary and Alternative Medicine, vol. 9, no. 1, p. 48, 2009. View at: Publisher Site | Google Scholar
  26. M. June, C. N. Kimani, J. M. Mbaria, M. Suleiman, D. Gakuya, and S. G. Kiama, “Antihyperglycemic activity of Zanthoxylum chalybeum stem bark extract in diabetic rats,” The Journal of Phytopharmacology, vol. 4, pp. 183–189, 2015. View at: Google Scholar
  27. H. Jouad, M. Haloui, H. Rhiouani, J. El Hilaly, and M. Eddouks, “Ethnobotanical survey of medicinal plants used for the treatment of diabetes, cardiac and renal diseases in the North centre region of Morocco (Fez-Boulemane),” Journal of Ethnopharmacology, vol. 77, no. 2-3, pp. 175–182, 2001. View at: Publisher Site | Google Scholar
  28. A. Arya, M. A. Abdullah, B. S. Haerian, and M. A. Mohd, “Screening for hypoglycemic activity on the leaf extracts of nine medicinal plants: in-vivo evaluation,” E-Journal of Chemistry, vol. 9, no. 3, pp. 1196–1205, 2012. View at: Publisher Site | Google Scholar
  29. World Health Organization, vol. 844, WHO, Geneva, Switzerland, 1994.
  30. A. Lemhadri, “Anti-hyperglycaemic activity of the aqueous extract of Origanum vulgare growing wild in Tafilalet region,” Journal of Ethnopharmacology, vol. 92, no. 2-3, pp. 251–256, 2004. View at: Publisher Site | Google Scholar
  31. N. A. Mohamed and O. A. Nassier, “The antihyperglycaemic effect of the aqueous extract of Origanium Vulgare leaves in streptozotocin-induced diabetic rats,” Jordan Journal of Biological Sciences, vol. 6, no. 1, pp. 31–38, 2013. View at: Publisher Site | Google Scholar
  32. L. Zenasni, “Etude de polymorphisme chimique des huiles essentielles de thymus satureioides Coss et d’Origanum compactum benth et du genre nepeta et évaluation de leur propriété antibactérienne,” Mohammed V University, Rabat, Morocco, 2014, Ph.D. Thesis. View at: Google Scholar
  33. C. Schwartz, “Phytoextraction des métaux des sols pollués par la plante hyperaccumulatrice Thalaspi caerulescens,” National Polytechnic Institute of Lorraine, Nancy, France, 1997, Ph. D. Thesis. View at: Google Scholar
  34. S. A. Khan, L. Khan, I. Hussain, K. B. Marwat, and N. Akhtar, “Profile of heavy metals in selected medicinal plants,” Journal of Weed Sciences and Research, vol. 14, pp. 101–110, 2008. View at: Google Scholar
  35. M. Fadil, A. Farah, B. Ihssane, T. Haloui, and S. Rachiq, “Optimisation des paramètres influençant l’hydrodistillation de Rosmarinus officinalis L. par la méthodologie de surface de réponse optimization of parameters influencing the hydrodistillation of Rosmarinus officinalis L. by response surface methodology,” Journal of Materials and Environmental Science, vol. 6, pp. 2346–2357, 2015. View at: Google Scholar
  36. M. Ouknin, A. Romane, J. Costa, and L. Majidi, “Comparative study of the chemical profiling, antioxidant and antimicrobial activities of essential oils of different parts of Thymus willdenowii Boiss & Reut,” Natural Product Research, vol. 33, no. 16, pp. 2398–2401, 2018. View at: Publisher Site | Google Scholar
  37. N. Savithramma, M. Linga Rao, and D. Suhrulatha, “Screening of medicinal plants for secondary metabolites,” Middle East Journal of Scientific Research, vol. 8, pp. 579–584, 2011. View at: Google Scholar
  38. S. M’sou, M. Alifriqui, and A. Romane, “Phytochemical study and biological effects of the essential oil of Fraxinus dimorpha Coss & Durieu,” Natural Product Research, vol. 31, no. 23, pp. 2797–2800, 2017. View at: Publisher Site | Google Scholar
  39. R. S. Abdul-jabbar, “Polyphenol and flavonoid contents and antioxidant activity in freshly consumed rocket (Eruca sativa),” IOP Conference Series Materials Science and Engineering, vol. 454, p. 012158, 2018. View at: Publisher Site | Google Scholar
  40. A. Romane and M. Trimeche, “Total phenolic content, antioxidant and anticorrosive activities of Olea europaea L. and Eucalyptus globulus cultivated in Tunisian arid zones on steel rebar’s in alkaline chloride solution,” International Journal of Electrochemical Science, vol. 14, p. 7530, 2019. View at: Google Scholar
  41. A. Arvouet-Grand, B. Vennat, A. Pourrat, and P. Legret, “Standardization of propolis extract and identification of principal constituents,” Journal de Pharmacie de Belgique, vol. 49, pp. 462–468, 1994. View at: Google Scholar
  42. S. Chakravarty and J. C. Kalita, “Antihyperglycaemic effect of flower of Phlogacanthus Thyrsiflorus Nees on streptozotocin induced diabetic mice,” Asian Pacific Journal of Tropical Biomedicine, vol. 2, no. 3, pp. S1357–S1361, 2012. View at: Publisher Site | Google Scholar
  43. H. Ouassou, T. Zahidi, S. Bouknana et al., “Inhibition of α-glucosidase, intestinal glucose absorption, and antidiabetic properties by Caralluma europaea,” Evidence-Based Complementary and Alternative Medicine, vol. 2018, Article ID 9589472, 8 pages, 2018. View at: Publisher Site | Google Scholar
  44. K. T. Kee, M. Koh, L. X. Oong, and K. Ng, “Screening culinary herbs for antioxidant and α-glucosidase inhibitory activities,” International Journal of Food Science & Technology, vol. 48, no. 9, pp. 1884–1891, 2013. View at: Publisher Site | Google Scholar
  45. I. Marmouzi, E. M. Karym, N. Saidi et al., “In vitro and in vivo antioxidant and antihyperglycemic activities of Moroccan oat cultivars,” Antioxidants, vol. 6, no. 4, p. 102, 2017. View at: Publisher Site | Google Scholar
  46. A. Bouyahya, J. Abrini, Y. Bakri, and N. Dakka, “Screening phytochimique et évaluation de l’activité antioxydante et antibactérienne des extraits d’Origanum compactum,” Phytothérapie, vol. 15, no. 6, pp. 379–383, 2017. View at: Publisher Site | Google Scholar
  47. R. Gutierrez, “Effect of Mexican oregano (Lippia graveolens kunth) on streptozotocin induced diabetic mice and its role in regulating carbohydrate metabolic enzymes and their inhibitory effect on the formation of advanced glycation end products,” Annual Research & Review in Biology, vol. 4, no. 23, pp. 3470–3491, 2014. View at: Publisher Site | Google Scholar
  48. S. Dhanabal, R. Vadivelan, V. Maithili, and S. Mahendran, “Antidiabetic activity of ethanolic extract of tubers of Dioscorea alata in alloxan induced diabetic rats,” Indian Journal of Pharmacology, vol. 43, no. 4, pp. 455–459, 2011. View at: Publisher Site | Google Scholar
  49. H. Oualili, H. Rchid, and R. Nmila, “Phytochemical screening and antioxidant activity of: Origanum elongatum and Cupressus atlantica two endemic plants of Morocco,” International Journal of Pharmacognosy and Phytochemical Research, vol. 10, pp. 196–200, 2018. View at: Publisher Site | Google Scholar
  50. D. Patel, S. Prasad, R. Kumar, and S. Hemalatha, “An overview on antidiabetic medicinal plants having insulin mimetic property,” Asian Pacific Journal of Tropical Biomedicine, vol. 2, no. 4, pp. 320–330, 2012. View at: Publisher Site | Google Scholar
  51. V. Sornalakshmi, P. Tresina Soris, K. Paulpriya, M. Packia Lincy, and V. R. Mohan, “Oral Glucose Tolerance Test (OGTT) in normal control and glucose induced hyperglycemic rats with Hedyotis leschenaultiana DC,” International Journal of Pharmacology and Toxicology, vol. 8, pp. 59–62, 2016. View at: Google Scholar
  52. W. Kooti, M. Farokhipour, Z. Asadzadeh, D. Ashtary-Larky, and M. Asadi-Samani, “The role of medicinal plants in the treatment of diabetes: a systematic review,” Electronic physician, vol. 8, no. 1, pp. 1832–1842, 2016. View at: Publisher Site | Google Scholar
  53. H. Bischoff, “Pharmacology of α-glucosidase inhibition,” European Journal of Clinical Investigation, vol. 24, pp. 3–10, 1994. View at: Google Scholar
  54. M. Bnouham, “Medicinal plants with potential antidiabetic activity-a review of ten years of herbal medicine research (1990–2000),” International Journal of Diabetes and Metabolism, vol. 14, pp. 1–25, 2006. View at: Google Scholar
  55. H. E. Lebovitz, “Alpha-glucosidase inhibitors,” Endocrinology and Metabolism Clinics of North America, vol. 26, no. 3, pp. 539–551, 1997. View at: Publisher Site | Google Scholar
  56. A. B. Evert, J. L. Boucher, M. Cypress et al., “Nutrition therapy recommendations for the management of adults with diabetes,” Diabetes Care, vol. 37, no. 1, pp. S120–S143, 2014. View at: Publisher Site | Google Scholar
  57. H. N. Gök, D. D. Orhan, I. E. Orhan, N. Orhan, and M. Aslan, “Evaluation of enzyme inhibitory and antioxidant activity of some Lamiaceae plants,” Journal of Research in Pharmacy, vol. 23, pp. 749–758, 2019. View at: Publisher Site | Google Scholar
  58. M. M. Soliman, M. A. Nassan, and T. A. Ismail, “Origanum majoranum extract modulates gene expression, hepatic and renal changes in a rat model of type 2 diabetes,” Iranian Journal of Pharmaceutical Research, vol. 15, pp. 45–54, 2016. View at: Google Scholar
  59. M. Maghrani, A. Lemhadri, H. Jouad, J.-B. Michel, and M. Eddouks, “Effect of the desert plant Retama raetam on glycaemia in normal and streptozotocin-induced diabetic rats,” Journal of Ethnopharmacology, vol. 87, no. 1, pp. 21–25, 2003. View at: Publisher Site | Google Scholar
  60. V. R. Young, “Trace element biology: the knowledge base and its application for the nutrition of individuals and populations,” The Journal of Nutrition, vol. 133, no. 5, pp. 1581S–1587S, 2003. View at: Publisher Site | Google Scholar
  61. S. Praveeena, S. Pasula, and K. Sameera, “Trace elements in diabetes mellitus,” Journal of Clinical and Diagnostic Research: JCDR, vol. 7, no. 9, pp. 1863–1865, 2013. View at: Publisher Site | Google Scholar
  62. H. Derakhshanian, M. H. Javanbakht, M. Zarei, E. Djalali, and M. Djalali, “Vitamin D increases IGF-I and insulin levels in experimental diabetic rats,” Growth Hormone & IGF Research, vol. 36, pp. 57–59, 2017. View at: Publisher Site | Google Scholar
  63. P. Dubey, V. Thakur, and M. Chattopadhyay, “Role of minerals and trace elements in diabetes and insulin resistance,” Nutrients, vol. 12, no. 6, p. 1864, 2020. View at: Publisher Site | Google Scholar
  64. N. Wiernsperger and J. Rapin, “Trace elements in glucometabolic disorders: an update,” Diabetology & Metabolic Syndrome, vol. 2, no. 1, p. 70, 2010. View at: Publisher Site | Google Scholar
  65. N. Sanjeevi, J. Freeland-Graves, S. N. Beretvas, and P. K. Sachdev, “Trace element status in type 2 diabetes: a 
meta-analysis,” Journal of Clinical and Diagnostic Research, vol. 12, pp. OE01–OE08, 2018. View at: Publisher Site | Google Scholar
  66. P. Rajalakshmy, “Role of micronutrients on type II diabetes mellitus,” Acta Scientific Nutritional Health, vol. 3, pp. 44–47, 2019. View at: Publisher Site | Google Scholar
  67. A. Gholam hoseinian, B. Shahouzehi, and G. Mohammadi, “Trace elements content of some traditional plants used for the treatment of diabetes mellitus,” Biointerface Research in Applied Chemistry, vol. 10, no. 5, pp. 6167–6173, 2020. View at: Publisher Site | Google Scholar
  68. A. M. Ahmed, O. F. Khabour, A. H. Awadalla, and H. A. Waggiallah, “Serum trace elements in insulin-dependent and non-insulin-dependent diabetes: a comparative study,” Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy, vol. 11, pp. 887–892, 2018. View at: Publisher Site | Google Scholar
  69. C. H. Sales, L. F. C. Pedrosa, J. G. Lima, T. M. A. M. Lemos, and C. Colli, “Influence of magnesium status and magnesium intake on the blood glucose control in patients with type 2 diabetes,” Clinical Nutrition, vol. 30, no. 3, pp. 359–364, 2011. View at: Publisher Site | Google Scholar
  70. D. H. Bonfanti, L. P. Alcazar, P. A. Arakaki et al., “ATP-dependent potassium channels and type 2 diabetes mellitus,” Clinical Biochemistry, vol. 48, no. 7-8, pp. 476–482, 2015. View at: Publisher Site | Google Scholar
  71. P. N. B. Lima, G. B. D. Carvalho, R. K. F. Santos et al., “Intakes of zinc, potassium, calcium, and magnesium of individuals with type 2 diabetes mellitus and the relationship with glycemic control,” Nutrients, vol. 10, no. 12, p. 1948, 2018. View at: Publisher Site | Google Scholar
  72. C. Ekmekcioglu, I. Elmadfa, A. L. Meyer, and T. Moeslinger, “The role of dietary potassium in hypertension and diabetes,” Journal of Physiology and Biochemistry, vol. 72, no. 1, pp. 93–106, 2016. View at: Publisher Site | Google Scholar
  73. M. Stone, L. Martyn, and C. Weaver, “Potassium intake, bioavailability, hypertension, and glucose control,” Nutrients, vol. 8, no. 7, p. 444, 2016. View at: Publisher Site | Google Scholar
  74. J. H. Helderman, D. Elahi, D. K. Andersen et al., “Prevention of the glucose intolerance of thiazide diuretics by maintenance of body potassium,” Diabetes, vol. 32, no. 2, pp. 106–111, 1983. View at: Publisher Site | Google Scholar
  75. G. Sun, S. Vasdev, G. R. Martin, V. Gadag, and H. Zhang, “Altered calcium homeostasis is correlated with abnormalities of fasting serum glucose, insulin resistance, and -cell function in the newfoundland population,” Diabetes, vol. 54, no. 11, pp. 3336–3339, 2005. View at: Publisher Site | Google Scholar

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