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A Critical Overview on the Pharmacological and Clinical Aspects of Popular Satureja Species

Abstract

Throughout the world, various parts of most Satureja species are traditionally used to treat patients with various diseases and complications. As for the presence of different classes of metabolites in Satureja and their numerous ethnomedical and ethnopharmaco-logical applications, many species have been pharmacologically evaluated. The current work aimed to compile information from pharmacological studies on this savory for further investigations. The keyword Satureja was searched through Scopus and PubMed up to January 1, 2016. We found nearly 55 papers that dealt with the pharmacology of Satureja. We found that 13 species had been evaluated pharmacologically and that Satureja khuzestanica, Satureja bachtiarica, Satureja montana and Satureja hortensis appeared to be the most active, both clinically and phytopharmacologically. Regarding the content of rich essential oil, most evaluations were concerned with the antimicrobial properties. However, the antioxidant, antidiabetic and anticholesterolemic properties of the studied species were found to be good. In addition to the pharmacological activities that have been indentified for some species, opportunities still exist to assess the effectiveness of other well-known species. If different Satureja species are to have extensive ethnopharmacological applications, comprehensive assessments of the acute and chronic toxicities, as well as the teratogenicity, of those plants are needed.

1. Introduction

Almost 7,000 species belonging to more than 230 genera are reported within the family Lamiaceae [1]. Among those genera, Satureja (savory) encompasses over 200 different herbs or shrub species that are often aromatic and are broadly found in the Mediterranean area, Asia and some parts of the US [2]. All over the world, flowers, leaves, stem and seeds of most of the Satureja species are traditionally used for various diseases and complications such as gastrointestinal cramps, nausea, diarrhea, muscle pains, and infectious diseases [3]. Because of the aromatic characteristics, leaves and aerial parts of this genus possess distinctive but pleasant tastes [4]. In Iran, Satureja is represented by 14 species in Flora Iranica, of which 11 have been reported [5].

Most of the savory species contain essential oil in their botanical parts. The yield of essential oil often exceeds 5% in different species of this genus [6]. With reference to the presence of monoterpenes such as thymol, carvacrol and cymene in the total essential oils [7,8], these metabolites resulted in the indication of antimicrobial activities against food, plants and human pathogens [9]. Flavonoids, tannins, acids and exudates are other known compounds in savory [6]. Based on the presence of all these metabolites, pharmacological properties such as antioxidant [10], anti-inflammatory and analgesic [11], and anti-hypercholesterolemic [12] activity have also been demonstrated.

Several species of savory are extensively and continuously used in ethnomedical and ethnopharmacological approaches of different cultures around the world. Valuable reports have been released on the pharmacological and clinical applications of this genus. Based on this, the current study aimed to compile and outline a frame from critical and pharmacological studies on this savory for further investigations.

2. Methods

To collect the data for this study, an extensive search with the keyword, Satureja, was carried out via two main search engines (Scopus and PubMed) from the beginning to January 1, 2016. All irrelevant papers as well as those on genetics, botany, agriculture, and chemistry were excluded. Almost 70 papers based on clinical and pharmacological aspects of different Satureja species were selected.

3. Results

3.1. Antimicrobial activities

Due to the rich amount of essential oils, different Satureja species have been assessed for possible antimicrobial activities. Using disc diffusion assay, the essential oil of Satureja bachtiarica demonstrated antibacterial activity against Pseudomonas aeruginosa as compared to erythromycin. Utilizing the broth dilution method, minimum inhibitory concentration (MIC) of S. bachtiarica essential oil was calculated as 31 µg/mL [13]. The ethanol extract of this species was assessed against some Gram-positive bacteria (Escherichia coli, Klebsiella pneumoniae, Staphylococcus aureus and Streptococcus agalactiae) and was found to be effective [14]. In another investigation using disc diffusion and agar dilution methods, the antimicrobial activity of the essential oils of this species against 10 clinical isolates of Helicobacter pylori was observed. The oil presented potent inhibitory effects against clinical isolates (17.6 ± 1.1 mm and 0.035 ± 0.13 µL/mL) [15].

Satureja calamintha is an Eastern Algerian species with antimicrobial activities. The essential oil of this plant has been evaluated against a wide range of microorganisms such as Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus, Klebsiella pneumoniae, Enterobacter aerogenes, Proteus mirabilis and Streptococcus entero-coccus. MIC values of the concerned essential oil against those microorganisms were 20 µg/mL, 40 µg/mL, 80 µg/mL, 80 µg/mL, 40 µg/mL, 20 µg/mL, and 40 µg/mL, respectively [16]. The essential oil of this species was also effective against certain fungi (MIC = 2 µL/mL) [17].

The essential oil of Satureja hortensis has also been evaluated as an antimicrobial agent against various Gram-positive and Gram-negative microorganisms. The outcome of that study revealed the activity of the essential oil [18].

The essential oil of Satureja intermedia, an endemic species from Iran, has also been assessed for possible antimicrobial activities against different pathogenic bacteria and fungi such as K. pneumoniae, Escherichia coli, Enterococcus faecalis, Staphylococcus aureus, Staphylococcus epidermidis, Bacillus subtilis, and Bacillus pumulis, respectively. The oil was also active against Candida albicans and Saccharomyces cerevisiae (MICs were at the range of 47–12 mg/mL for bacteria and 7.5–1.75 mg/mL for fungi). Standard antibiotic and antifungal agents were ampicillin (10 mg/disc) and nystatine (30 mg/disc) in that study [19]. Another study revealed a considerable antimicrobial effect from S. intermedia essential oil against Staphylococcus aureus (MIC = 125 µg/mL) [20].

Three antimicrobial studies have been carried out on the essential oil and methanol of Satureja khuzestanica. Methanol extract of a native sample of S. khuzestanica demonstrated more active antimicrobial properties against Staphylococcus aureus and Candida albicans as compared to a cultivated sample [21]. Moreover, the antimicrobial activities of S. khuzestanica essential oil have been evaluated against a wide range of pathogenic bacteria and fungi [22]. In another investigation, S. khuzestanica essential oil containing carvacrol (90.8%) as the main constituent in full- flowering stage exerted maximum antimicrobial effects against studied pathogens as compared to other collection stages. MICs for pathogens sensitive to S. khuzestanica essential oil were in the range of 19–312 µg/mL [23]. The ethanol extract of S. khuzestanica fresh leaves were assessed for antifungal activity against some saprophytic fungi in comparison with amphotericin B by utilizing agar well diffusion method (MIC values in the range of 625–5,000 µg/mL) [24]. Similarly, the hydroalcoholic extract of S. khuzestanica demonstrated antifungal activity against Cryptococcus neoformans isolates (MIC and minimal fungicidal concentration values in the range of 62.5–2,000 µg/mL and 125–4,000 µg/mL, respectively) [25].

Satureja kitaibelii is another medicinal species that has been evaluated for antimicrobial activities. The essential oil of this herb demonstrated potent activity (broth microdilution assay, MIC 0.97–15.6 mg/mL) when applied in a form of lozenge (0.2%). The MIC value for the essential oil was calculated as 0.10–25 µg/mL [26].

Using broth dilution method, minimum bactericidal concentration and MIC values for Satureja montana ethanol extract against Staphylococcus aureus, Escherichia coli, Proteus morgani, Candida tropicalis and Trichophyton mentagrophytes were determined at the range of 4.1–6.3% and 3.1–4.1%, respectively. In contrast, hole-plate diffusion method demonstrated the strongest activity of the aforementioned extract against Bacillus subtilis, Sarcina flava, Candida tropicalis and Candida krusei [27]. The antifungal activity of S. montana essential oil was studied against eight different fungi and two phytopathogens. Using a disc diffusion method, the maximum effectiveness of essential oil (carvacrol at around 60%) was demonstrated against Trichophyton violaceum, Trichophyton rubrum, Trichophyton tonsurans, Trichophyton mentagrophytes and Pyricularia oryzae (inhibition zone > 70%) [28].

Satureja sahendica is another species with antibacterial activities. Disk diffusion method demonstrated that the essential oil containing thymol (40%), γ-terpinene (28%), and ρ-cymene (22%) possesses considerable antimicrobial activities on tested bacteria and fungi [29].

Another similar study on Satureja thymbra essential oil demonstrated the effectiveness of this species against different Gram-positive and Gram-negative strains [30], and some of those were multiple resistant. These sensitive strains were Stenotrophomonas maltophilia and Chryseomonas luteola [31].

A Satureja species from Mediterranean region, namely Satureja parnassica has been evaluated for possible antimicrobial activities. The extracted essential oil from this species was collected before flowering, just before flowering, full flowering, and after flowering periods. A comparative determination on samples revealed the maximum antimicrobial effects of the herb against Salmonella enterica and Listeria monocytogenes at full flowering period. The MIC values at two levels of bacterial inoculation (105 CFU/mL and 102 CFU/mL) on Salmonella enterica were 64 µg/mL and 56 µg/mL on Salmonella enterica and 49 µg/ mL and 35 µg/mL on Listeria monocytogenes, respectively [32].

Satureja wiedemanniana essential oil has been assessed for antibacterial effects against Bacillus species isolated from raw meat samples [33].

3.2. Antiparasitic effects

There is a report on the amebicidal activity of Satureja cuneifolia methanol extract (1.0–32.0 mg/mL) on Acanthamoeba castellanii cysts and trophozoites. The extract demonstrated both time- and dose-dependent amebistatic and amebicidal activities. No viable trophozoites were found within 24 hours in the presence of 32 mg/mL extract (p < 0.05) [34].

The trypanocidal activity of Satureja macrantha essential oil, diethyl ether extract and respective fractions on Trypanosoma cruzi epimastigotes was assessed in a study. In vitro trypanocidal assay resulted in minimum lethal concentrations of 12.5 µg/mL and 25 µg/mL for essential oil and diethyl ether extract, as compared to that of Gentian violet (positive control 6.25 µg/mL). Responsible constituents for such activity were found as thymol and carvacrol [35].

Satureja thymbra essential oil has been evaluated for acaricidal activity against field-collected unfed adult Hyalomma marginatum in an experimental study. The total volatile oil (5 µl/L, 10 µl/L, 20 µl/L, and 40 µl/L) as well as its major constituents, carvacrol (40 µl/L) and γ-terpinene (40 µl/L) were examined for possible tick mortality effect. Ticks exposed to vapors from cotton wicks with 40 µl/L produced 100% mortality in 3 hours. In contrast, only carvacrol and γ-terpinene produced knockdown in the evaluated species [36].

Hydroalcoholic extract of S. khuzestanica, an endemic species to Iran, has been examined against hydatid cyst protoscolices for possible scolicidal activity. The extract at the concentration of 1% was highly potent for in exposure time of 30 minutes, 1 hour and 2 hours. It was observed that by reducing the concentration or increasing the exposure time, mortality rate was reduced [37].

In a similar experimental assessment, scolicidal effects of S. khuzestanica essential oil were evaluated against protoscolices collected aseptically from hydatid cyst within affected sheep livers. The scolicidal effects of 3 mg/mL of the oil were found as 28.58%, 32.71%, 37.20% and 42.02% after 10 minutes, 20 minutes, 30 minutes, and 1 hour, respectively. Total scolicidal activity was found at 10 mg/ mL after 10 minutes [38].

In another assessment, S. khuzestanica essential oil exerted antiparasitic activities against Leishmania major promastigotes inoculated in an animal model. In that study, the oil (0.01%) could reduce the progress of lesion size and decrease the mortality rate, as compared to the controls [39].

In addition to those studies on S. khuzestanica, the hydroalcoholic extract from their leaves demonstrated inhibitory activity against Giardia lamblia cysts, as compared to metronidazole. Fatality rate on cysts in vitro was determined as 32.52 ± 9.07% for the extract in comparison with that of metronidazole (28.75 ± 10.30%) [40].

3.3. Antiviral effects

Among Satureja species, it seems that only S. montana has been evaluated for antiviral activities (human immunodeficiency virus-1 induced cytopathogenicity in MT-4 cells). The aqueous extract of this plant exerted strong anti-human immunodeficiency virus-1 activity (effective dose = 16 µ/mL) against the virus and also respective reverse transcriptase [41].

3.4. Antioxidant and radical scavenging activities

With reference to high phenolic and flavonoid contents in Satureja species, different studies on the antioxidant and radical scavenging properties have been carried out on those species.

The methanol extract from two S. bachtiarica samples, wild and cultivated, has been assessed for those aforementioned activities through 2,2-diphenyl-1-picrylhydrazyl (DPPH) and ferric ion reducing antioxidant power (FRAP) methods of assay. Higher levels of antioxidant and radical scavenging effect (29.04 mg/g and 58.25 mg/g Trolox via FRAP and DPPH, respectively) were observed for wild samples, which may be due to the higher phenolic compounds (24.50 mg caffeic acid/g sample) and total flavonoids (87.99 mg catechin/g sample) [42].

By using FRAP and thiobarbituric acid reactive substances (TBARS) assays, total antioxidant power and lipid peroxidation of S. khuzestanica essential oil were determined in rats. Regarding treatment with the essential oil, normal blood lipid peroxidation level was reduced (1.66 ± 0.25 nmol/mL treated with essential oil vs. 2.1 ± 0.33 nmol/mL untreated) and total antioxidant power was increased (98.25 ± 4.81 mmol/m treated with essential oil vs. 32 ± 2.86 mmol/m untreated) [43]. The essential oil extracted from S. khuzestanica also possessed antioxidant activities (225 mg/kg per day, orally) in reprotoxicity induced by cyclosporine in adult male Wistar rats. In that study, reduced sperm count, viability, fertilization, and blastocyst development rates were corrected via pre-treatment with the essential oil [44]. Also in alloxan-induced type I diabetic rats, the essential oil of this species was assessed for possible antioxidant enzyme activity (500 ppm in drinking water). Following 8 weeks of intervention, serum level of glutathione, glutathione peroxidase serum activity, superoxide dismutase, and catalase in the essential oil group was increased, as compared to the controls [45].

With reference to antibacterial and antibiofilm activities against periodontopathogens, S. hortensis essential oil was evaluated for antioxidant properties in oxidative stress and excessive matrix metalloproteinase (MMP) expression/activity. Treatment with 1 µL/mL and 5 µL/mL of S. hortensis inhibited MMP activity and H2O2-induced cell death [46].

In an investigation, Satureja macrostema methanol extract was assessed for antioxidant properties through various antioxidant assays DPPH, superoxide, NO, hydroxyl radical scavenging, and iron-chelating activity. Compared to those of ascorbic acid (100 µg/mL), DPPH radical scavenging ability of the extract (100 mg/mL) was found in lesser amounts (89.87% vs. 97%). Compared to quercetin (50 µg/mL), the NO scavenging and superoxide anion of the extract (same amount) were not accepted (69.79 ± 4.17% and 66.12 ± 0.25% vs. 93.8 ± 0.98% and 90.87 ± 0.43%, respectively). In contrast, methanol extract showed highest activity on hydroxyl radical [50% inhibitory concentration (IC50) = 49.65 µg/mL] [47].

Because of the presence of polyphenolic compounds, ethyl acetate fraction of S. montana methanol extract as well as the total essential oil demonstrated radical scavenging activity via DPPH assay [84.9% and 94.4% respectively as compared to Trolox, 98.2%, 50% effective concentration (EC50) = 44 ± 1.63 µg/mL and 128 ± 2.26 µg/mL, respectively) [48]. In a similar study, DPPH assay and 2, 2’-azino-bis (3-ethylbenzothiazoline-6-sulphonic acid method (ABTS) on S. montana methanol extract resulted in EC50 values of 116.36 ± 12.83 µg/mL and 106.59 ± 1.41 µmol Trolox equivalents/g dry sample, respectively [49].

The spray-dried hydroalcoholic extract of S. montana in combination with 10% maltodextrin as carrier and drying agent resulted in a potent radical scavenging activity (IC50 = 5.24 µg/mL) via DPPH assay [50].

The antioxidant effects of S. hortensis essential oil on safflower oil oxidation has been studied through different related methods, such as DPPH, ABTS, ferric thiocyanate, and β-carotene bleaching. The oils exerted considerable activities in different concentrations [51]. A similar study on the hydroalcoholic extract of this plant revealed positive antioxidant and radical scavenging activities (IC50 DPPH < 300 µg/mL) [52]. Another study demonstrated that both essential oil (1 µL/mL and 2.5 µL/mL) and ethanol extract (2.5 mg/mL) of S. hortensis may decrease the rat lymphocytes oxidative damage induced by hydrogen peroxide [53].

3.5. Anti-inflammatory, antinociceptive and healing activities

Essential oil, hydroalcoholic and polyphenolic extracts of S. hortensis seeds have been evaluated for possible antiinflammatory and analgesic activities. Acetic acid and formalin (analgesic methods) and carrageenan-induced rat paw edema (anti-inflammatory) tests were used. In that study, pretreatment with those extracts decreased acetic-acid-induced abdominal twitches and paw edema [54]. Another investigation demonstrated that an aqueous extract of this herb (200 mg/kg) could diminish the morphine withdrawal syndrome signs [55]. A similar study revealed that both hydroalcoholic and essential oil of this plant could inhibit the mice writhing responses caused by acetic acid [56]. To assess the therapeutic effects of S. hortensis in periodontal inflammation, a study revealed that the herb essential oil can reduce the ratio of live/dead bacteria and increase the membrane permeability [57].

Satureja horvatii essential oil has demonstrated antimicrobial effects against certain bacteria (MIC 0.03–0.57 mg/mL) and yeast strains (MIC 0.56–2.23 mg/ mL) [58].

S. khuzestanica has been studied for analgesic and antiinflammatory activities. The hydroalcoholic extract of S. khuzestanica has been evaluated for anti-inflammatory and antinociceptive effects by means of carrageenan-induced rat paw edema and formalin test, respectively. The extract [150 mg/kg; intraperitoneally (i.p.)] was as effective as indomethacin (4 mg/kg; i.p.) based on antiinflammatory activities. The antinociceptive effect was found to be dose-dependent (10–150 mg/kg; i.p.) as compared to morphine (3 mg/kg; i.p.) [11]. Another study confirmed the antinociceptive activities of S. khuzestanica ethanol extract utilizing different tests such as tail-flick, hot-plate, and acetic acid (writhing test). Regarding tail-flick and hot-plate tests, the extract (100 mg/kg; i.p.) demonstrated analgesic effect at 15 minutes following the injection and peak at about 30 minutes after injection. The effect was permanent for almost 45 minutes. Through the acid acetic test, the extract demonstrated the effectiveness at 100 mg/kg and 150 mg/kg [59].

In another investigation, it was observed that S. khuzestanica (25 mg/kg, 50 mg/kg, and 100 mg/kg, i.p., simultaneously with morphine) may dose-dependently have preventive effects on opioid analgesic tolerance in adult male Wistar rats. The outcomes were of significant increase in glial fibrillary acidic protein and tumor necrosis factor α levels, which were reversed to control levels when subjected to 100 mg/kg of the extract [60].

Furthermore, it has been revealed that S. khuzestanica possess protective effects in patients with recurrent aphthous stomatitis. In a placebo-controlled randomized clinical trial, both S. khuzestanica essential oil (Group A) and hydroalcoholic extract (Group B) were evaluated in comparison with a hydroalcoholic solution as placebo. Mean time of pain elimination in both S. khuzestanica groups showed significant differences as compared to placebo (3.40 ± 0.50 days and 3.20 ± 0.41 days for S. khuzestanica groups vs. 5.70 ± 1.12 days) in the placebo group. The mean duration of complete healing in S. khuzestanica groups (5.90 ± 1.24 days and 6.85 ± 1.30 days) were also significantly different from that of the placebo (10.40 ±1.66 days) [61].

Compared to prednisolone as the standard drug, S. khuzestanica essential oil was evaluated for possible effectiveness against acetic-acid-induced inflammatory bowel disease in a mouse model. According to the outcomes of that study, lipid peroxidation, a marker for evaluating oxidative stress, was restored in prednisolone and essential oil groups (500 ppm, 1,000 ppm, and 1,500 ppm). In contrast, myeloperoxidase activity was significantly reduced with both 1,000 ppm and 1,500 ppm of the oil as well as prednisolone. Furthermore, score values of macroscopic and microscopic characters were reduced in essential oil (1,000 ppm and 1,500 ppm) and prednisolone groups [62].

3.6. Antidiabetic, hepatoprotective, anticholesterolemic and allied activities

Via an animal study, it was concluded that administration of S. cuneifolia tea (80 mg/kg) to the affected rats may have antihypercholesterolemic effects as compared to the control and cholesterol groups (2% cholesterol-containing pellet feed) [63].

The different preparations of S. khuzestanica have been assessed for possible antidiabetic, hypoglycemic and antihyperlipidemic activities. In an assessment, S. khuzestanica essential oil significantly decrease the level of glucose (258 ±18.1 mg/dL vs. 325 ± 21.5 mg/dL in the control group), total cholesterol (146 ± 9.6 mg/dL vs. 156 ± 14.1 mg/dL in the control group) and triglyceride (166 ± 14.9 mg/dL vs. 201 ± 17.6 mg/dL in the control group) in streptozocin-induced diabetic rats as well as those rats receiving a lipid regimen [43]. In a similar study on alloxan-induced type I diabetic rats, the oil significantly inhibited the activities of liver enzymes and decrease fasting blood glucose, triglyceride, low-density lipoprotein (LDL) and very low-density lipoprotein (VLDL) [64].

Another investigation on serum glucose levels and lipid profile in male streptozotocin-induced diabetic rats revealed that S. khuzestanica ethanol extract (100 mg/kg) could significantly reduce the LDL, VLDL, and triglyceride levels. Moreover, doses of 100 mg/kg and 300 mg/kg of the extract reduced the fasting blood sugar after 1 month of administration [65].

Regarding the association of liver in body glucose metabolism, a study demonstrated that S. khuzestanica essential oil (1,000 ppm added to drinking water of rats for 2 weeks) could alter the key enzymes of glycogenosis and gluconeogenesis, glycogen phosphorylase (24% increased) and phosphoenol pyruvate carboxy kinase (26% decreased), as compared to controls. Nevertheless, the oil had no impact on blood sugar concentrations [66].

S. khuzestanica has been traditionally accepted as a liver tonic herb. It has been proven that hyperthyroidism is often associated with liver oxidative stress and thus may lead to liver dysfunction. Accordingly, S. khuzestanica essential oil was investigated for possible hepatoprotective activities in hyperthyroid rats. The oil (225 mg/kg) was effective on serum aspartate transaminase, alanine transaminase, and hepatic malondialdehyde when administered in combination with vitamin E (200 mg/kg) [67].

In a double-blinded randomized controlled trial on patients with type II diabetes mellitus, S. khuzestanica crude leaves powder (250 mg/day for 2 months) was assessed for possible effectiveness on some metabolic parameters. Treatment of patients with crude leaves powder revealed significant decrease in total cholesterol and LDL levels as well as increase in high-density lipoprotein-cholesterol, total antioxidant power, and TBARS. On the contrary, the plant exhibited no impacts on serum glucose level, triglyceride, creatinine, and TBARS [68]. Despite the positive results on the antidiabetic activities of S. khuzestanica in animal models, outcomes of this study showed that the antidiabetic activities of this plant in human have not yet been confirmed [69].

S. khuzestanica essential oil could significantly ameliorate the progress of diabetic nephropathy in alloxan-induced diabetic rats as compared to control and diabetic untreated groups. The oil (250 ppm or 500 ppm added to drinking water for 8 weeks) inhibited the progression of glomerular hypertrophy, glomerulosclerosis, glomerular number loss, lipid peroxidation, serum creatinine, and urea in comparison with diabetic untreated group [70].

Methanol extract of S. macrostema possessed hepatoprotective activity as it could ameliorate lipid peroxidation in carbon tetrachloride and paracetamol-induced hepatic damaged rats [47].

Using a standard method [71], the spray-dried hydro-alcoholic extract of S. montana in combination with different concentrations of maltodextrin as carriers was evaluated experimentally for possible angiotensin-I-converting enzyme (ACE) inhibition activity. The extract in three samples (associated maltodextrin as 10%, 30% and 50%) exhibited similar ACE inhibition (IC50 values of 0.33 mg, 0.33 mg, and 0.49 mg, respectively) [50].

3.7. Anticancer and cytotoxic effects

Using MTT (3-[4,5-dimethylthiazol-2-yl]-2,5 diphenyltetrazolium bromide) assay, cytotoxic activities of S. intermedia essential oil were assessed on two human cancerous cells (esophageal squamous cell carcinoma and human bladder carcinoma cell lines). The results revealed a considerable activity ranging from 39 µg/mL to 1,000 µg/mL (IC50 = 156 µg/mL) [19].

Using brine shrimp lethality assay (BSLA), diethyl ether, methanol, and water extracts of S. macrantha as well as column chromatography-isolated terpenoids were evaluated for possible cytotoxic activity against water life brand brine shrimp (Artemia salina) eggs. Seawater and a well-known cytotoxic alkaloid, berberine hydrochloride (LC50 = 26 µM) were selected as controls. Results from BSLA showed that three isolates especially oleanolic acid (LC50 = 17 µM) were effective [72].

Brine shrimp lethality as well as four cancerous cell lines, HT29/219, Caco2, NIH-3T3, and T47D (human breast ductal carcinoma) were selected to evaluate the possible cytotoxic activities of isolated chalcone and flavanones from aerial parts of Satureja spicigera. Among those isolates, 5, 7, 3′, 5′-tetrahydroxy flavanone and 5,4′-dihydroxy-3′-methoxyflavanone-7-(6″-O-α-L-rhamnopyranosyl)-β-D-glucopyranoside were effective against Artemia salina larva (LC50 = 2 µg/mL) and T47D (IC50 = 98.7 µg/mL), respectively. The controls were seawater and berberine hydrochloride (LC50 = 26 µM) and the methods were BSLA and MTT cytotoxicity assays [73].

MTT cytotoxicity assay was used to evaluate the S. sahendica essential oil cytotoxic activities against human cancer cell lines. According to the outcomes of that study, cell viability of MCF7, Vero, SW480 and JET 3 cancerous cells (IC50 values were calculated as 15.6 µg/mL, 15.6 µg/ mL, 125 µg/mL, and 250 µg/mL, respectively) were significantly reduced dose-dependently [29].

3.8. Cardiovascular effects

The inhibitory effects of S. hortensis methanol extracts on adhesion of the activated human platelet to laminin-coated plates as well as aggregation and protein secretion were assessed. The extract could inhibit the platelet adhesion to laminin-coated wells by 48% [74].

3.9. Diuretic activity

The extracted essential oil of S. montana has demonstrated diuretic activity in an animal model when compared with an infusion and water—alcohol extract. Nevertheless, both essential oil (0.1%) and infusion (10%) solutions were effective in 3 days of experimentation [75].

3.10. Fertility effects

S. khuzestanica essential oil (75 mg/kg per day, 150 mg/kg per day, and 225 mg/kg per day for 45 days in drinking water) was revealed to have positive male fertility effects in male rates. With reference to the outcomes, potency, fecundity, fertility index, and litter size as well as testosterone level, weights of testes, seminal vesicles were significantly improved. Higher doses (150 mg/kg and 225 mg/kg) of the oil could also increase the number of spermatogonia and spermatozoids [76].

In an animal study, the improvement effects of S. montana hydroalcoholic extract on premature ejaculation and copulatory behavior in rats were examined. The extract was orally administered for eight consecutive days (25 mg/kg and 50 mg/kg). In comparison to control, acute administration of the extract in both doses as well as sub-acute use of the extract at lower dose resulted in a significant increase in ejaculation. In addition, the extract could decrease the intromission frequency with the same administration condition. In addition, testosterone serum level in rats acutely treated with 50 mg/kg of the extract was significantly elevated as compared to that of the control [77].

3.11. Gastrointestinal activities

S. hortensis essential oil was assessed for antispasmodic activity on contractions of isolated ileum compared with the effect of atropine and dicyclomine. The oil (0.1 mL/ 100 g) could also inhibit castor-oil-induced diarrhea in mice [78]. Another species, Satureja obovata has also been evaluated for possible spasmolytic effects against acetyl-choline. Total terpene content of this essential oil was responsible for the studied activity [79].

3.12. Immunostimulant effects

The effect of S. bachtiarica ethanol extract (200 mg/kg and 400 mg/kg) on immunological parameters in Wistar rats was assessed. The extract demonstrated a significant increase in albumin levels (200 mg/kg), phagocytosis number (400 mg/kg) and neutrophil count (400 mg/kg). Accordingly, the herb can be introduced as an immunostimulant without causing hematological side effects [80]. Solely and in combination with another medicinal herb, the effectiveness of S. khuzestanica on lysozyme activity and hematological factors was assessed in common carp. Serum lysozyme activities were significantly different in various treatments. S. khuzestanica, in both conditions, increased the resistance of common carp [81].

3.13. Respiratory-related activities

Different concentrations of S. hortensis hydroalcoholic extract have been evaluated for their relaxant effect on guinea pig trachea. Compared to theophylline, the plant demonstrated a potent activity in higher concentrations [82]. The aqueous extract (250 mg/kg) of S. hortensis could exert anti-inflammatory effects on induced rhinosinusitis in rabbits. Topical application of this extract could decrease both NO synthase enzyme and concentration of NO radical metabolites [83].

3.14. Other pharmacological properties

In an investigation on Satureja viminea, hippocratic screening showed that the respective aqueous extract (500 mg/kg and 1,000 mg/kg) decreased the motor activity of nonfasted SpragueeDawley female rats. In contrast, doses of 500 mg/kg and 750 mg/kg of S. viminea essential oil produced a higher decrease in motor activity. To assess the exploratory behavior and curiosity of animals under oral administration of S. viminea essential oil, 1,000 mg/kg of the oil significantly reduced the numbers of holes (from 60 ± 2.6 to 2.2 ± 1.1) explored by albino mice, as compared to that of the vehicle (from 61 ± 4.2 to 43 ± 7.5). These two tests simply showed the sedative effects of S. viminea [84].

The protective effects of S. montana hydroalcoholic extract were evaluated against cyclophosphamide-induced testicular damage in rats. The extract was administered orally (50 mg/kg per day) for 7 days before and after cyclophosphamide injection (200 mg/kg i.p.). The extract could restore and increase the relative testicular weight, serum testosterone level, and alkaline phosphatase activity as well as testicular acid phosphatase and sorbitol dehydrogenase activities. Improving the total antioxidant capacity, the extract could also reduce the lipid peroxidation. In contrast, testicular DNA fragmentation was mitigated in the extract group. The protective effects of the extract were also confirmed by histopathological assessments. Antiapoptotic and antioxidant activities were mentioned as main mechanisms of the extract in that study [85].

3.15. Toxicity

An animal study demonstrated that application of S. cuneifolia (80 mg/kg) could be responsible for granular degeneration in the liver of Wistar albino rats [63].

4. Conclusions and future perspectives

The current study aimed to compile studies carried out pharmacological activities of most popular Satureja species. According to the outcomes, most of the performed studies focused on the antibacterial and antifungal activities that are closely related to the presence of rich monoterpenes in those species [86]. Nevertheless, antiviral effects of the mentioned species should be given consideration. Among those species, the anti-inflammatory and analgesic activities, mostly related to S. khuzestanica, were found. In this regard, it could be interesting to study the respective properties on other well-known species. In addition to these findings, there was only one study on the possible toxicity of a certain Satureja species (S. cuneifolia). Regarding the extensive ethnopharmacological application of different Satureja species, comprehensive assessments on acute and chronic toxicity as well as teratogenicity of those medicinal plants are recommended (Fig. 1).

Figure 1
figure 1

Different Satureja species and related proved properties.

References

  1. Zarshenas MM, Krenn L. Phytochemical and pharmacological aspects of Salvia mirzayanii Rech. f. & Esfand. J Evid Based Complementary Altern Med. 2015;20:65–72.

    Google Scholar 

  2. Rustaiyan A, Feizbakhsh A, Masoudi S, Ameri N. Comparison of the volatile oils of Satureja atropatana Bung. and Satureja mutica Fisch. et C.A. Mey. from Iran. J Essent Oil Res. 2004; 16:594–596.

    Google Scholar 

  3. Gulluce M, Sokmen M, Daferera D, Agar G, Ozkan H, Kartal N, et al. In vitro antibacterial, antifungal, and antioxidant activities of the essential oil and methanol extracts of herbal parts and callus cultures of Satureja hortensis L. J Agric Food Chem. 2003;51:3958–3965.

    Google Scholar 

  4. Eminagaoglu O, Tepe B, Yumrutas O, Akpulat HA, Daferera D, Polissiou M, et al. The in vitro antioxidative properties of the essential oils and methanol extracts of Satureja spicigera (K. Koch.) Boiss. and Satureja cuneifolia ten. Food Chem. 2007; 100:339–343.

    Google Scholar 

  5. Rechinger KH, ed. Flora Iranica. Wien: Akademische Druck und Verlagsanstalt; 1982.

  6. Momtaz S, Abdollahi M. An update on pharmacology of Satureja species; from antioxidant, antimicrobial, antidiabetes and anti-hyperlipidemic to reproductive stimulation; 2010. Available at: http://hdl.handle.net/2263/15298.

    Google Scholar 

  7. Ghannadi A. Composition of the essential oil of Satureja hortensis L. Seeds from Iran. J Essent Oil Res. 2002;14:35–36.

    Google Scholar 

  8. Kurkcuoglu M, Tumen G, Baser K. Essential oil constituents of Satureja boissieri from Turkey. Chem Nat Compd. 2001;37:329–331.

    Google Scholar 

  9. Bonnafé E, Drouard F, Hotier L, Carayon JL, Marty P, Treilhou M, et al. Effect of a thymol application on olfactory memory and gene expression levels in the brain of the honeybee Apis mellifera. Environ Sci Pollut Res. 2015;22:8022–8030.

    Google Scholar 

  10. Četković G, Čanadanović-Brunet J, Djilas S, Tumbas V, Markov S, Cvetković D. Antioxidant potential, lipid peroxidation inhibition and antimicrobial activities of Satureja montana L. subsp. kitaibelii extracts. Int J Mol Sci. 2007;8:1013–1027.

    Google Scholar 

  11. Amanlou M, Dadkhah F, Salehnia A, Farsam H, Dehpour AR. An anti-inflammatory and anti-nociceptive effects of hydroalcoholic extract of Satureja khuzistanica Jamzad extract. J Pharm Pharm Sci. 2005;8:102–106.

    Google Scholar 

  12. Mchedlishvili D, Kuchukashvili Z, Tabatadze T, Davitaia G. Influence of flavonoids isolated from Satureja hortensis L. on hypercholesterolemic rabbits. Ind J Pharmacol. 2005;37:259.

    Google Scholar 

  13. Pirbalouti AG, Dadfar S. Chemical constituents and antibacterial activity of essential oil of Satureja bachtiarica (Lamiaceae). Acta Pol Pharm. 2013;70:933–938.

    Google Scholar 

  14. Zareii B, Seyfi T, Movahedi R, Cheraghi J, Ebrahimi S. Antibacterial effects of plant extracts of Alcea digitata L., Satureja bachtiarica L. and Ferulago angulata L. J Babol Univ Med Sci. 2014;16:31–37.

    Google Scholar 

  15. Falsafi T, Moradi P, Mahboubi M, Rahimi E, Momtaz H, Hamedi B. Chemical composition and anti-Helicobacter pylori effect of Satureja bachtiarica Bunge essential oil. Phytomedicine. 2015;22:173–177.

    Google Scholar 

  16. Bensouici C, Benmerache A, Chibani S, Kabouche A, Abuhamdah S, Semra Z, et al. Antibacterial activity and chemical composition of the essential oil of Satureja calamintha ssp. sylvatica from Jijel, Algeria. Der Pharmacia Lettre. 2013;5:224–227.

    Google Scholar 

  17. Labiod R, Aouadi S, Bouhaddouda N. Chemical composition and antifungal activity of essential oil from Satureja calamintha nepeta against phytopathogens fungi. Int J Pharmacy Pharm Sci. 2015;7:208–211.

    Google Scholar 

  18. Mahboubi M, Kazempour N. Chemical composition and antimicrobial activity of Satureja hortensis and Trachyspermum copticum essential oil. Iran J Microbiol. 2011;3:194–200.

    Google Scholar 

  19. Sadeghi I, Yousefzadi M, Behmanesh M, Sharifi M, Moradi A. In vitro cytotoxic and antimicrobial activity of essential oil from Satureja intermedia. Iran Red Crescent Med J. 2013;15:70–74.

    Google Scholar 

  20. Shahnazi S, Khalighi-Sigaroodi F, Ajani Y, Yazdani D, Taghizad- Farid R, Ahvazi M, et al. The chemical composition and antimicrobial activity of essential oil of Satureja intermedia C. A. Mey. J Medicinal Plants. 2008;7:85–92.

    Google Scholar 

  21. Amanlou M, Fazeli MR, Arvin A, Amin HG, Farsam H. Antimicrobial activity of crude methanolic extract of Satureja khuzistanica. Fitoterapia. 2004;75:768–770.

    Google Scholar 

  22. Yousefzadi M, Riahi-Madvar A, Hadian J, Rezaee F, Rafiee R, Biniaz M. Toxicity of essential oil of Satureja khuzistanica:in vitro cytotoxicity and anti-microbial activity. J Immunotoxicol. 2014;11:50–55.

    Google Scholar 

  23. Pirbalouti AG, Moalem E. Variation in antibacterial activity of different ecotypes of Satureja khuzestanica Jamzad, as an Iranian endemic plant. Ind J Tradit Knowl. 2013;12:623–629.

    Google Scholar 

  24. Sadeghi-Nejad B, Shiravi F, Ghanbari S, Alinejadi M, Zarrin M. Antifungal activity of Satureja khuzestanica (Jamzad) leaves extracts. Jundishapur J Microbiol. 2007;3:36–40.

    Google Scholar 

  25. Zarrin M, Amirrajab N, Sadeghi-Nejad B. In vitro antifungal activity of Satureja khuzestanica Jamzad against Cryptococcus neoformans. Pak J Med Sci. 2010;26:880.

    Google Scholar 

  26. Kundakovic T, Milenkovic M, Zlatkovic S, Kovacevic N, Goran N. Composition of Satureja kitaibelii essential oil and its antimicrobial activity. Nat Prod Commun. 2011;6:1353–1356.

    Google Scholar 

  27. Pepeljnjak S, Stanić G, Potoćki P. Antimicrobial activity of the ethanolic extract of Satureja montana ssp. montana. Acta Pharmaceutica. 1999;49:65–69.

    Google Scholar 

  28. Entela Haloc I, Toska V, Baldisserotto A, Goci E, Vertuani S, Manfredini S. Evaluation of antifungal activity of Satureja montana essential oil before and after inclusion in betacyclodextrine. Int J Pharmacy Pharm Sci. 2014;6:189–191.

    Google Scholar 

  29. Yousefzadi M, Riahi-Madvar A, Hadian J, Rezaee F, Rafiee R. In vitro cytotoxic and antimicrobial activity of essential oil from Satureja sahendica. Toxicol Environ Chem. 2012;94:1735–1745.

    Google Scholar 

  30. Capone W, Mascia C, Spanedda L, Chiappini M. Chemical composition and antibacterial activity of the essential oil from Sardinian Satureja thymbra. Fitoterapia. 1989;60:90–92.

    Google Scholar 

  31. Sarac N, Ugur A. Antimicrobial activities of the essential oils of Origanum onites L., Origanum vulgare L. subspecies hirtum (Link) Ietswaart, Satureja thymbra L., and Thymus cilicicus Boiss. & Bal. growing wild in Turkey. J Med Food. 2008;11:568–573.

    Google Scholar 

  32. Chorianopoulos N, Evergetis E, Mallouchos A, Kalpoutzakis E, Nychas GJ, Haroutounian SA. Characterization of the essential oil volatiles of Satureja thymbra and Satureja parnassica:influence of harvesting time and antimicrobial activity. J Agric Food Chem. 2006;54:3139–3145.

    Google Scholar 

  33. Yucel N, Aslim B, Ozdogan H. In vitro antimicrobial effect of Satureja wiedemanniana against Bacillus species isolated from raw meat samples. J Med Food. 2009;12:919–923.

    Google Scholar 

  34. Malatyali E, Tepe B, Degerli S, Berk S. In vitro amoebicidal activities of Satureja cuneifolia and Melissa officinalis on Acanthamoeba castellanii cysts and trophozoites. Parasitol Res. 2012;110:2175–2180.

    Google Scholar 

  35. Saeidniaa S, Goharia A, Hadjiakhoondib A. Trypanocidal activity of the essential oil of Satureja macrantha and its main volatile components. Int J Essent Oil Ther. 2007;1:184–186.

    Google Scholar 

  36. Cetin H, Cilek JE, Oz E, Aydin L, Deveci O, Yanikoglu A. Acaricidal activity of Satureja thymbra L. essential oil and its major components, carvacrol and gamma-terpinene against adult Hyalomma marginatum (Acari: Ixodidae). Vet Parasitol. 2010;170:287–290.

    Google Scholar 

  37. Zibaei M, Sarlak A, Delfan B, Ezatpour B, Azargoon A. Scolicidal effects of Olea europaea and Satureja khuzestanica extracts on protoscolices of hydatid cysts. Kor J Parasitol. 2012;50:53–56.

    Google Scholar 

  38. Moazeni M, Saharkhiz MJ, Hoseini AA, Alavi AM. In vitro scolicidal effect of Satureja khuzistanica (Jamzad) essential oil. Asian Pac J Trop Biomed. 2012;2:616–620.

    Google Scholar 

  39. Kheirandish F, Delfan B, Farhadi S, Ezatpour B, Khamesipour A, Kazemi B, et al. The effect of Satureja khuzestanica essential oil on the lesions induced by Leishmania major in BALB/c mice. Afr J Pharmacy Pharmacol. 2011;5:648–653.

    Google Scholar 

  40. Fallahi S, Rostami A, Delfan B, Pournia Y, Rashidipour M. Effect of olive leaf, Satureja khuzestanica, and Allium sativum extracts on Giardia lamblia cysts compared with metronidazole in vitro. J Parasit Dis; 2015. Available at: http://link.springer.com/article/10.1007%2Fs12639-015-0650-8#/page-1.

    Google Scholar 

  41. Yamasaki K, Nakano M, Kawahata T, Mori H, Otake T, Ueba N, et al. Anti-HIV-1 activity of herbs in Labiatae. Biol Pharm Bull. 1998;21:829–833.

    Google Scholar 

  42. Salehi-Arjmand H, Mazaheri D, Hadian J, Majnoon Hosseini N, Ghorbanpour M. Essential oils composition, antioxidant activities and phenolics content of wild and cultivated Satureja bachtiarica Bunge plants of Yazd origin. J Medicinal Plants. 2014;13:6–14.

    Google Scholar 

  43. Abdollahi M, Salehnia A, Mortazavi SH, Ebrahimi M, Shafiee A, Fouladian F, et al. Antioxidant, antidiabetic, antihyperlipidemic, reproduction stimulatory properties and safety of essential oil of Satureja khuzestanica in rat in vivo: a oxicopharmacological study. Med Sci Monit. 2003;9:331–335.

    Google Scholar 

  44. Najafi G, Farokhi F, Shalizar Jalali A, Akbarizadeh Z. Protection against cyclosporine-induced reprotoxicity by Satureja khuzestanica essential oil in male rats. Int J Fertil Steril. 2016;9:548–557.

    Google Scholar 

  45. Ahmadvand H. Amelioration of altered antioxidant enzyme activity by Satureja khuzistanica essential oil in alloxan-induced diabetic rats. Chin J Nat Med. 2014;12:672–676.

    Google Scholar 

  46. Zeidan-Chulia F, Neves de Oliveira BH, Gursoy M, Kononen E, Fonseca Moreira JC, Gursoy UK, et al. MMPREDOX/NO interplay in periodontitis and its inhibition with Satureja hortensis L. essential oil. Chem Biodivers. 2013;10:507–523.

    Google Scholar 

  47. Gutierrez RM, Navarro YT. Antioxidant and hepatoprotective effects of the methanol extract of the leaves of Satureja macrostema. Pharmacogn Mag. 2010;6:125–131.

    Google Scholar 

  48. Hassanein HD, Ahl Hah SA, Abdelmohsen MM. Antioxidant polyphenolic constituents of Satureja montana L. growing in Egypt. Int J Pharmacy Pharm Sci. 2014;6:578–581.

    Google Scholar 

  49. López-Cobo A, Gómez-Caravaca AM, Švarc-Gajić J, Segura- Carretero A, Fernández-Gutiérrez A. Determination of phenolic compounds and antioxidant activity of a Mediterranean plant: The case of Satureja montana subsp. kitaibelii. J Funct Food. 2015;18(B):1167–1178.

    Google Scholar 

  50. Vidović SS, Vladić JZ, Vaštag ŽG, Zeković ZP, Popović ZP, Popović LM. Maltodextrin as a carrier of health benefit compounds in Satureja montana dry powder extract obtained by spray drying technique. Powder Technol. 2014;258:209–215.

    Google Scholar 

  51. Fathi A, Sahari M, Barzegar M, Naghdi Badi H. Antioxidant activity of Satureja hortensis L. essential oil and its application in safflower oil. J Medicinal Plants. 2013;1:51–67.

    Google Scholar 

  52. Bahramikia S, Yazdanparast R, Nosrati N. A comparision of antioxidant capacities of ethanol extracts of Satureja hortensis and Artemisia dracunculus leaves. Pharmacol Online. 2008;2:694–704.

    Google Scholar 

  53. Behravan J, Mosaffa F, Karimi G, Iranshahi M. In vitro protective effects of Satureja hortensis L. essential oil and ethanolic extract on lymphocytes DNA. J Medicinal Plants. 2007;2:64–70.

    Google Scholar 

  54. Hajhashemi V, Zolfaghari B, Yousefi A. Antinociceptive and anti-inflammatory activities of Satureja hortensis seed essential oil, hydroalcoholic and polyphenolic extracts in animal models. Med Princ Pract. 2012;21:178–182.

    Google Scholar 

  55. Vafaei AA, Miladi-Gorji H, Taherian AA, Bagerian M. Effects of Valeriane officinalis, Satureja hortensis, and Mentha piperita extracts on the withdrawal syndrome signs in mice. Koomesh. 2011;12:342–347.

    Google Scholar 

  56. Hajhashemi V, Ghannadi A, Pezeshkian SK. Antinociceptive and anti-inflammatory effects of Satureja hortensis L. extracts and essential oil. J Ethnopharmacol. 2002;82:83–87.

    Google Scholar 

  57. Zeidan-Chulia F, Keskin M, Kononen E, Uitto VJ, Soderling E, Moreira JC, et al. Antibacterial and antigelatinolytic effects of Satureja hortensis L. essential oil on epithelial cells exposed to Fusobacterium nucleatum. J Med Food. 2015;18:503–506.

    Google Scholar 

  58. Bukvicki D, Stojkovic D, Sokovic M, Vannini L, Montanari C, Pejin B, et al. Satureja horvatii essential oil: in vitro antimicrobial and antiradical properties and in situ control of Listeria monocytogenes in pork meat. Meat Sci. 2014;96:1355–1360.

    Google Scholar 

  59. Saberi A, Sepehrib G, Mahani SE, Rasoulian B, Sheibani V, Esmaeilpour K, et al. Satureja khuzestanica extract elicits antinociceptive activity in several model of pain in rats. J Appl Sci. 2013;13:729–735.

    Google Scholar 

  60. Esmaeili-Mahani S, Ebrahimi B, Abbasnejad M, Rasoulian B, Sheibani V. Satureja khuzestanica prevents the development of morphine analgesic tolerance through suppression of spinal glial cell activation in rats. J Nat Med. 2015;69:165–170.

    Google Scholar 

  61. Amanlou M, Babaee N, Saheb-Jamee M, Salehnia A, Farsam H. Efficacy of Satureja khuzistanica extract and its essential oil preparations in the management of recurrent aphthous stomatitis. DARU J Pharm Sci. 2007;15:231–235.

    Google Scholar 

  62. Ghazanfari G, Minaie B, Yasa N, Nakhai LA, Mohammadirad A, Nikfar S, et al. Biochemical and histopathological evidences for beneficial effects of Satureja khuzestanica Jamzad essential oil on the mouse model of inflammatory bowel diseases. Toxicol Mech Methods. 2006;16:365–372.

    Google Scholar 

  63. Akdogan M, Kisioglu AN, Ciris M, Koyu A. Investigating the effectiveness of different tea types from various thyme kinds (Origanum onites, Thymbra spicata and Satureja cuneifolia) on anemia and anticholesterolemic activity. Toxicol Ind Health. 2014;30:938–949.

    Google Scholar 

  64. Ahmadvand H, Tavafi M, Khalatbary AR. Hepatoprotective and hypolipidemic effects of Satureja khuzestanica essential oil in alloxan-induced type 1 diabetic rats. Iran J Pharmaceutical Res. 2012;11:1219–1226.

    Google Scholar 

  65. Hafezi H, Vahdati A, Sepehrimanesh M. Effect of Satureja khuzestanica Jamzad extract on serum lipid profile, blood glucose level and body weight gain in diabetes mellitus: a Rattus norvegicus model. Comp Clin Pathol. 2015;24:1033–1037.

    Google Scholar 

  66. Saadat M, Pournourmohammadi S, Donyavi M, Khorasani R, Amin G, Nazar Salehnia A, et al. Alteration of rat hepatic glycogen phosphorylase and phosphoenolpyruvate carboxykinase activities by Satureja khuzestanica Jamzad essential oil. J Pharm Pharm Sci. 2004;7:310–314.

    Google Scholar 

  67. Assaei R, Zal F, Mostafavi-Pour Z, Dabbaghmanesh MH, Geramizadeh B, Ranjbar Omrani GH, et al. Hepatoprotective effect of Satureja khuzestanica essential oil and vitamin E in experimental hyperthyroid rats: evidence for role of antioxidant effect. Iran J Med Sci. 2014;39:459–466.

    Google Scholar 

  68. Vosough-Ghanbari S, Rahimi R, Kharabaf S, Zeinali S, Mohammadirad A, Amini S, et al. Effects of Satureja khuzestanica on serum glucose, lipids and markers of oxidative stress in patients with type 2 diabetes mellitus: a double-blind randomized controlled trial. Evid Based Complement Alternat Med. 2010;7:465–470.

    Google Scholar 

  69. Sarkhail P, Rahmani P. Hypoglycemic property of Satureja khuzestanica in human still in doubt. Mol Cell Biochem. 2011; 7:745–746.

    Google Scholar 

  70. Tavafi M, Ahmadvand H, Tamjidipoor A, Delfan B, Khalatbari AR. Satureja khozestanica essential oil ameliorates progression of diabetic nephropathy in uninephrectomized diabetic rats. Tissue Cell. 2011;43:45–51.

    Google Scholar 

  71. Yoshie-Stark Y, Wada Y, Wäsche A. Chemical composition, functional properties, and bioactivities of rapeseed protein isolates. Food Chem. 2008;107:32–39.

    Google Scholar 

  72. Gohari AR, Hadjiakhoondi A, Sadat-Ebrahimi E, Saeidnia S, Shafiee A. Cytotoxic terpenoids from Satureja macrantha CA Mey. DARU J Pharm Sci. 2005;13:177–181.

    Google Scholar 

  73. Gohari AR, Ostad SN, Moradi-Afrapoli F, Malmir M, Tavajohi S, Akbari H, et al. Evaluation of the cytotoxicity of Satureja spicigera and its main compounds. Scis World J. 2012;2012:203861.

    Google Scholar 

  74. Yazdanparast R, Shahriyary L. Comparative effects of Artemisia dracunculus, Satureja hortensis and Origanum majorana on inhibition of blood platelet adhesion, aggregation and secretion. Vasc Pharmacol. 2008;48:32–37.

    Google Scholar 

  75. Stanic G, Samarzija I. Diuretic activity of Satureja montana Subsp. montana extracts and oil in rats. Phytotherapy Res. 1993;7:363–366.

    Google Scholar 

  76. Haeri S, Minaie B, Amin G, Nikfar S, Khorasani R, Esmaily H, et al. Effect of Satureja khuzestanica essential oil on male rat fertility. Fitoterapia. 2006;77:495–499.

    Google Scholar 

  77. Zavatti M, Zanoli P, Benelli A, Rivasi M, Baraldi C, Baraldi M. Experimental study on Satureja montana as a treatment for premature ejaculation. J Ethnopharmacol. 2011;133:629–633.

    Google Scholar 

  78. Hajhashemi V, Sadraei H, Ghannadi AR, Mohseni M. Antispasmodic and anti-diarrhoeal effect of Satureja hortensis L. essential oil. J Ethnopharmacol. 2000;71:187–192.

    Google Scholar 

  79. Cruz T, Cabo M, Jimenez J, Zarzuelo A. Composition and pharmacological activity of the essential oil of Satureja obovata ii. spasmolytic activity. Fitoterapia. 1990;61:247–251.

    Google Scholar 

  80. Dehkordi HS, Dehkordi MJ, Chaleshtori MR, Khamesipour F, Katsande S. Effect of alcohol extract of Zataria multiflora (Boiss), Satureja bachtiarica (Bunge) and Zaravschanica membranacea (Boiss) on immuno-hematologic factors in rats. Trop J Pharm Res. 2015;14:1999–2004.

    Google Scholar 

  81. Khansari A, Yavari V, Alishahi M, Mousavi SM, Ghorbanpoor M, Bastami KD, et al. Effects of Oliviera decumbens and Satureja khuzestanica extract on some immunological and haematological parameters of Cyprinus carpio. Comp Clin Pathol. 2012;22:339–342.

    Google Scholar 

  82. Boskabady M, Aslani M, Mansuri F, Amery S. Relaxant effect of Satureja hortensis on guinea pig tracheal chains and its possible mechanism. DARU J Pharm Sci. 2007;15:199–204.

    Google Scholar 

  83. Uslu C, Karasen RM, Sahin F, Taysi S, Akcay F. Effects of aqueous extracts of Satureja hortensis L. on rhinosinusitis treatment in rabbit. J Ethnopharmacol. 2003;88:225–228.

    Google Scholar 

  84. Suarez A, Echandi MM, Ulate G, Ciccio JF. Pharmacological activity of the essential oil of Satureja viminea (Lamiaceae). Rev Biol Trop. 2003;51:247–252.

    Google Scholar 

  85. Abd El Tawab AM, Shahin NN, AbdelMohsen MM. Protective effect of Satureja montana extract on cyclophosphamideinduced testicular injury in rats. Chem Biol Interact. 2014; 11(224C):196–205.

    Google Scholar 

  86. Tepe B. Inhibitory effect of Satureja on certain types of organisms. Rec Nat Prod. 2015;9:1–18.

    Google Scholar 

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Jafari, F., Ghavidel, F. & Zarshenas, M.M. A Critical Overview on the Pharmacological and Clinical Aspects of Popular Satureja Species. Innov. Acupunct. Med. 9, 118–127 (2016). https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.jams.2016.04.003

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