Biological Activities of Some Species of Genus Eryngium

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Biological Activities of Some Species of Genus Eryngium

This entry is adapted from the peer-reviewed paper 10.3390/molecules28104094

There are approximately 250 species of Eryngium L. distributed throughout the world, with North America and South America being centers of diversity on this continent. In the central-western region of Mexico there may be around 28 species of this genus. Some Eryngium species are cultivated as leafy vegetables, ornamental, and medicinal plants. In traditional medicine they are used to treat respiratory and gastrointestinal conditions, diabetes, and dyslipidemia, among others.

Eryngium Apiaceae medicinal plants traditional uses

1. Biological and Pharmacological Activity

The use of plants in medicines ranges from crude preparations or extracts, to refined extracts and single molecular species. In terms of categories of use, these encompass food supplements, herbal medicines, botanical drugs, and prescription medicines. There is an increasing interest in plants as a source of novel pharmacophores ^[1].

In this context, pharmacological studies of medicinal plants have been carried out, addressing various extract evaluation strategies in vitro or in vivo, using different extractive solvents or following traditional preparation practices. The plants of the genus Eryngium have not been the exception; thus, the evaluation of the extracts of Eryngium spp. distributed around the world, have shown multiple beneficial effects ^[2], such as anti-inflammatory ^[3], against snake and scorpion venoms ^[4]^[5], antibacterial, antioxidant ^[6], antihyperglycemic ^[7], and cytotoxic against human tumor cell lines ^[8], among others.

Regarding the Eryngium spp. reported in the central-western region of Mexico, records of its use in traditional medicine were found for eight species, but reports of biological activities were found only for five of these species.

2. Eryngium carlinae

There has been great interest in learning about its effects on diabetes control; thus, Noriega-Cisneros et al. (2012) ^[9] investigated the effect of chronic administration of ethanolic extract of E. carlinae on glucose, creatinine, uric acid, total cholesterol, and triglyceride levels in the serum of streptozotocin (STZ)-induced diabetic rats. Treatment with ethanolic extract of E. carlinae prevented the increase in glucose, triglycerides, total cholesterol, and uric acid in serum; it also reduced the levels of creatinine, uric acid, total cholesterol, and triglycerides in healthy rats compared to those with diabetes. Additionally, ethanolic extract significantly decreased glycosylated hemoglobin (HbA1c) in the serum of diabetic rats. The authors concluded that administration of E. carlinae reduced cardiovascular-risk-related hyperlipidemia in diabetes mellitus. Subsequently, Noriega-Cisneros (2013) ^[10] analyzed the chemical composition of the ethanolic extract of E. carlinae and studied the effect of its consumption in STZ-induced diabetic rats, and its antioxidant activity was assayed. The results showed that ethanolic extract had no hypoglycemic effect when administered orally to diabetic rats (45 mg/kg); however, it did reduce cholesterol and triglyceride levels, improving the lipid profile and reducing the cardiovascular risk index. The in vitro analysis showed antioxidant activity and a considerable amount of flavonoids and phenolic compounds related to it; however, the in vivo analysis did not have a significant effect on lipid peroxidation, and antioxidant enzymatic activity of the superoxide dismutase (SOD) and catalase (CAT) only showed an effect on reducing the nitric oxide levels. Histological analysis of the kidney showed that although the ethanolic extract of E. carlinae did not control hyperglycemia, it may offer benefits on lipid profile and progression of renal damage. Later, Noriega-Cisneros et al. (2020) ^[11] investigated the mechanism of action of the hypolipidemic effect of the ethanolic extract of E. carlinae, analyzing its composition and lipid-lowering activity. The extract was administered orally to STZ-induced diabetic rats (30 mg/kg) for more than 40 days, and its effect was compared with that of atorvastatin (a drug used to lower cholesterol levels). The analyzed extract reduced total cholesterol and non-high-density lipoprotein cholesterol (C-HDL) levels and increased the C-HDL levels reduced in diabetes, decreasing the atherogenic index and, therefore, the risk of suffering cardiovascular disease risk at the same level as atorvastatin. The results demonstrated the hypolipidemic potential of ethanolic extract of E. carlinae and support its use in traditional medicine as a hypolipidemic agent. On the other hand, García-Cerrillo et al. (2018) ^[12] demonstrated that the hexanic extract of E. carlinae had in vitro and in vivo antioxidant activity associated with the decrease in glucose and triacylglyceride levels during hyperglycemia and suggested that this effect could reduce the risk of developing diabetic cardiomyopathy. The authors administered hexanic extract of E. carlinae (30 mg/kg) to STZ-induced diabetic rats for seven weeks and found that serum levels of glucose, triacylglycerides, and TBARS (thiobarbituric acid reactive substances) were significantly reduced in diabetic rats supplemented with the extract. Peña-Montes et al. (2019) ^[13] also evaluated the in vitro antioxidant activity of the hexanic extract of E. carlinae inflorescences in Saccharomyces cerevisiae under stress induced by hydrogen peroxide, and later, they tested the extract in STZ-induced diabetic male Wistar rats. The hexanic extract showed in vitro antioxidant activity at different concentrations compared to ascorbic acid (positive control). Oral administration (30 mg/kg) of the hexanic extract reduced blood glucose levels; lipid peroxidation in the liver, kidney, and brain; protein carbonylation; and reactive oxygen species (ROS) production in normoglycemic and hyperglycemic rats. CAT activity in the brain, kidneys, and liver also increased. These findings showed the antioxidant properties of the hexanic extract of E. carlinae inflorescences.

Regarding active metabolites, Castro-Torres et al. (2017) ^[14] determined the hypocholesterolemic activity of the hydroalcoholic extract of aerial parts of E. carlinae and demonstrated the presence of hexa-O-acetyl-d-mannitol and its acetylated derivatives by gas chromatography coupled with mass spectrometry (GC-MS) analysis. The authors concluded that mannitol promoted osmotic diuresis, which may favor cholesterol transport, preventing it from accumulating in enterocytes and the development of hypercholesterolemia; in this sense, mannitol-based drugs are used to promote diuresis (before irreversible renal failure) and urinary excretion of toxic substances as an antiglaucoma agent, and as an aid in the diagnosis of renal function ^[15]. In the same way the diuretic effect and the excretion of toxic substances, the renoprotective activity of E. carlinae has been reported by Pérez-Ramírez et al. (2016) ^[16]. The authors studied the effect of plant decoctions on renal dysfunction in high-fructose and high-fat fed rats. Decoction consumption reduced serum uric acid, urine albumin and urea, and increased creatinine clearance, which was associated with reduced hyperglycemia, renal lipid accumulation, and oxidative stress. These results suggested that E. carlinae could be used as an ingredient of functional beverages with renoprotective effects.

The only clinical study of E. carlinae found during this research was reported by Montes-Moreno (2017) ^[17]. The authors evaluated the effect of consuming aqueous extracts of toad grass on serum triglycerides, body composition, and anthropometric values in adults. A randomized, parallel blind clinical trial was carried out, and anthropometric measurements, body composition, and blood biochemistry were taken. Individuals with triglycerides >150 mg/dL were selected to determine the effect of drinking the aqueous extract on the baseline parameters of the participants after four weeks. The consumption of the extract reduced weight and body fat (approx. 1 kg) and triglycerides and VLDL cholesterol (21%). The results obtained suggested that drinking the infusion at a 1% concentration at least once a day could reduce and/or control high serum triglyceride levels and be an adjuvant in reducing the percentage of body fat and weight.

Another reported use of Eryngium spp. is the treatment of cholelithiasis; therefore, Valdivia-Mares (2021) ^[18] evaluated the effectiveness of a 50% hydroalcoholic extract of E. carlinae to treat cholelithiasis by an in vitro dissolution model using 30 stones formed by ≥70% cholesterol selected from 1597 stones obtained by cholecystectomy. To improve solubility and resemble gallbladder conditions, the test temperature was between 35 and 37 °C, and the extract was renewed every hour for 20 h. Solutions of 50% ethanol and 99% ethyl ether were used as negative and positive controls, respectively. The dissolution rate of the media was estimated as the reduction in the mass of the treated stones (g/mL/h). The extract showed a higher dissolution rate (0.00280–0.00285 g/mL/h) than that shown by ethanol (0.00255 g/mL/h) and six times lower than that shown by ethyl ether (0.00715 g/mL/h). The authors suggested that these results could contribute to the development of a safer, cheaper, and less invasive therapy, such as a product containing E. carlinae.

Another of the benefits attributed to E. carlinae is its antispasmodic activity, which was confirmed in vivo by Pérez-Gutiérrez et al. (2006) ^[19]. This activity was attributed to the presence of two γ-lactones from the methanol fraction isolated and characterized by the authors.

Regarding the antimicrobial activity of E. carlinae, tests performed in vitro have not shown significant growth inhibition of human pathogenic bacteria ^[20]. On the other hand, Galindo-Hernández (2018) ^[21] evaluated the antifungal activity of the acetonic extract of E. carlinae against Candida spp. strains isolated from pediatric dental patients. The extract did not show strong antimicrobial activity against C. albicans (ATCC 90029). In contrast to the above antimicrobial studies, Espino-Garibay (2010) ^[22] evaluated the antimicrobial effect of E. carlinae metabolites, identifying 21 metabolites in ethanolic extracts (leaves, peduncles, and flowers) by GC-MS. Regarding the volatile compounds, germacrene showed antifungal activity against Colletotrichum lindemuthianum (49.6%) and Botrytis cinerea (39.1%). The highest antifungal activity against C. lindemuthianum (almost 100%) was shown by spathulenol (50 mg/mL) and piperitone oxide (500 mg/mL). While spathulenol, piperitone oxide, and menthol (100 mg/mL) exerted a less inhibitory effect against B. cinerea (37.8%), only piperitone oxide (250 mg/mL) had an inhibitory effect against Fusarioum oxysporum (28.8%). On the other hand, the antimicrobial activity of E. carlinae terpenoids was lower; thus, pulegone and borneol, with a dose of 500 mg/mL, inhibited the oomycete Phytophthora cinammomis 32.1 and 30.8%, respectively. Meanwhile, spathulenol (500 mg/mL) and myrcene (250 mg/mL) exerted an inhibitory effect of 18.1 and 15.3%, respectively. The crude extracts showed higher activity against P. cinnamomi (34%).

3. Eryngium comosum

There are few scientific reports on the biological activities of Eryngium comosum, Delaroche F.; for example, the work of Ronquillo de Jesús (2013) ^[23] who determined the antioxidant activity of ethanolic, aqueous, hexanic, and ether of petroleum extracts of E. comosum using the DPPH assay. In addition, the extracts cytotoxicity was assayed in vitro in peripheral blood mononuclear cells and in vivo in Artemia salina. Ethanolic and aqueous extracts at a concentration of 1000 ppm showed IC50 values of 4.93 µg/mL and 49.52 µg/mL, respectively. None of the extracts showed toxicity in mononuclear cells, while the extract with petroleum ether did show a cytotoxic effect in A. salina (IC50 2.92 ppm).

The antimicrobial activity has also been studied in E. comosum, in addition to the antioxidant activity. Díaz-Alvarado et al. (2020) ^[24] evaluated the antibacterial activity by the disk diffusion method (DDM), using reference strains of equine pathogenic bacteria: Listeria monocytogenes ATCC 19115, Staphylococcus sp., Escherichia coli ATCC 25922, and Salmonella enterica serotype Enteritidis ATCC 13076. Ethanolic extract of E. comosum (50%) prepared with dried tissue (125 mg/mL) inhibited the growth of Staphylococcus sp., S. enterica, and L. monocytogenes, showing a greater effect on the latter strain. The results suggested the extract of E. comosum as a source of antimicrobial agents to treat equine infections, although further in vitro and in vivo research is required to achieve its application. In the same way, Díaz-Alvarado (2020) ^[25] analyzed the bioactive compounds in aqueous and ethanolic extracts (50 and 70%) of E. comosum, and assayed antioxidant capacity and antimicrobial activity in 50% ethanolic extracts of this medicinal plant. The 50% ethanolic extract of E. comosum showed antioxidant capacity (1973.42 μM ETCA/g) and antibacterial activity against Enterococcus sp. and Salmonella sp. (inhibition zone diameter = 11.3 mm).

Regarding in vivo studies, Pérez-Reyes (2016) ^[26] reported that the aqueous extract of E. comosum reduced cholesterol and triglyceride levels in rats with dyslipidemia, induced with a hypercholesterolemic and hypertriglyceridemic diet. The extract was administered intragastrically for 3 weeks, testing three doses: 100, 200, and 400 mg/kg. After the treatment, the influence of the aqueous extract on the weight of adipose and muscle tissues was observed; however, a body weight reduction was not reported. On the other hand, the decrease in serum cholesterol levels was recorded at a dose of 100 mg/kg, with a serum concentration of 189.45 mg/dL in the control group and 99.16 mg/dL in the treated group; while the serum concentration of triglycerides decreased only with the 200 mg/kg dose, being 403.1 mg/dL in the control group and 337.8 mg/dL in the treated group.

4. Eryngium cymosum

One of the most widespread traditional uses of Eryngium ssp. is the treatment of type 2 diabetes (T2D), and there are some reports about its hypoglycemic effect. For example, the study carried out by Espinoza-Hernández et al. (2021) ^[27], in which the aqueous extract of aerial parts of the E. cymosum plant was administered via gavage to Wistar rats with streptozotocin-nicotinamide-induced hypoglycemia (STZ-NA). The authors reported the antihyperglycemic effect of the extract in the pyruvate tolerance test and the significant reduction of postprandial hyperglycemia in the maltose tolerance tests. As the main mechanism of action, the extract suppressed gluconeogenesis by inhibition (almost 100%) of the enzymes glucose-6-phosphatase (G6Pase) and fructose-1,6-bisphosphatase (FBPase), which is the altered pathway that causes fasting and postprandial hyperglycemia in patients with T2D; the extract also reduced the activity of a-glucosidases by 32%. In addition, it decreased insulin levels when it was administered orally in healthy rats in both nutritional states, without affecting normoglycemia in normal curves and reducing the postprandial peak in glucose load curves. The authors concluded that the traditional form of consumption of E. cymosum is safe and regulates glucose levels both fasting and in the postprandial state.

Subsequently, the same research group published a study that evaluated the chronic effects of traditional extracts on hyperglycemia and hypertriglyceridemia of some Mexican medicinal plants, including E. cymosum ^[28]. The aqueous extract was administered via gavage to hyperglycemic STZ-NA Wistar rats, daily for 42 days. For the preparation of the extract, 20 g of dried and ground plant material (aerial parts) were added to 500 mL of boiling, distilled water for 15 min. Non-fasting blood glucose (NFBG), HbA1c, and blood triglycerides were determined. The authors confirmed the long-term efficacy of the extract, as E. cymosum prevented the worsening of hyperglycemia by avoiding the significant increase in glucose levels shown by the negative control group and the increase in HbA1c (2.98%). Despite its antihyperglycemic effects, the extract was less effective in controlling triglycerides. The authors generated evidence of the antihyperglycemic effect of this Mexican medicinal plant, as well as its long-term efficacy in the control of T2D.

Research to reveal the mechanisms of action of the hypoglycemic effect of E. cymosum has led to the description of a new metabolite, acylated flavonol, and the isolation of known compounds both in aqueous extract and butanolic extract ^[29], whose chemical structures were elucidated using spectroscopic techniques, as described in the following section. Additionally, the role of the acylated flavonol glucoside on the inhibition of G6Pase and FBPase has been demonstrated.

5. Eryngium heterophyllum

Some studies have been carried out in E. heterophyllum to confirm its anti-inflammatory, hypoglycemic, and hypocholesterolemic activity. Navarrete et al. (1990) ^[30] reported the decrease in rat serum cholesterol when the aqueous extract of E. heterophyllum was administered orally. For his part, Miranda-Velásquez (2010) ^[31] tested the hypocholesterolemic activity of crude extracts dissolved in water or in a Tween 80/saline solution at two doses of 50 and 100 mg/kg of weight administered to hypercholesterolemic mice for five days, which at the end of this period were fasted for 12 h. The results showed that only the aqueous extracts of E. heterophyllum at 100 mg/kg showed a cholesterol reduction (20.7%). Therefore, this extract was subsequently evaluated in vitro using Vero cells to determine the inhibitory effect of the HMG-CoA enzyme. The results showed that indeed the mechanism of serum cholesterol reduction was related to the inhibition of said enzyme, as in the case of statin drugs. In the same way, García-Gómez et al. (2019) ^[32], in a 1-month clinical study, showed that combined treatment of E. heterophyllum and Amphipterygium adstringens with proven hypocholesterolemic activity tested in rats, reduced triglyceride levels by an average of 20%. On the other hand, Carreón-Sánchez et al. (2013) ^[33] showed that the ethanolic extract of E. heterophyllum, after being administered to mice by oral gavage in a single dose of 100 mg/kg of weight in a volume of 0.2 mL/30 g, had no hypoglycemic effect or acute or chronic anti-inflammatory effect; nor did it cause visible toxic effects in the acute poisoning model in mice.

Molina-Garza et al. (2014) ^[34] conducted a study to screen the trypanocidal activity of the Eryngium heterophyllum plants used in traditional Mexican medicine for the treatment of various diseases related to parasitic infections. Cultured Trypanosoma cruzi epimastigotes were incubated for 96 h with different concentrations of methanolic extract of E. heterophyllum, and the inhibitory concentration (IC50) was determined. The methanolic extracts exhibited the highest trypanocidal activity (88–100%) at a concentration of 150 µg/mL.

6. Eryngium longifolium

A dose-independent hypoglycemic effect has been reported for E. longifolium. Andrade-Cetto et al. (2021) ^[35] evaluated aqueous (30 and 310 mg/kg doses) and ethanolic (32 and 318 mg/kg doses) extracts of the aerial parts of the plant in hyperglycemic STZ-NA Wistar rats. Previously, the authors determined the basic phytochemical profiles (see next section) and acute toxicity tests, which did not show any physical problems or behavioral changes after oral administration of the maximum dose of 2000 mg/kg body weight (b.w.) of each extract; no deaths were reported and the LD50 was higher than the maximum dose used. In addition, they tested the inhibition of the G6Pase and FBPase enzymes involved in glucose metabolism. This study validated for the first time the traditional use of the aerial part of E. longifolium as a hypoglycemic agent in a hyperglycemic animal model; the results indicated that the in vitro inhibition of G6Pase and FBPase could be associated with the hypoglycemic effect in vivo. Therefore, the authors concluded that the ability to regulate hyperglycemia could involve inhibition of hepatic glucose production, which primarily controls fasting glucose levels, and that the doses traditionally consumed did not generate toxic effects.

According to the previous information, the main potential of the Mexican species of Eryngium to promote health, is related to lipid metabolism, which has been proven by the capacity of its extracts to decrease cholesterol, triglycerides, and body fat levels; this has also been reported for other species of Eryngium ^[36].

It is important to highlight the potential of the aqueous extracts of E. cymosum and E. longifolium for the control of diabetes, as reported for E. foetidum and E. billardieri ^[36]^[37]. The information found about hypoglycemic activity shows the differences between the biological and pharmacological activity that different Mexican species of Eryngium show; in addition, such differences could be associated with the type of extract evaluated since the content and nature of the active ingredients will also vary. For instance, the acetonic and methanolic extracts of E. foetidum did not show antibacterial activity against Escherichia coli, Salmonella infantis, Listeria monocytogenes, Staphylococcus aureus, or Bacillus cereus ^[38], while the essential oil of E. maritimum showed a significant antibacterial activity against L. monocytogenes and E.coli due to its content of oxygenated sesquiterpenes ^[39], and the leaf hydromethanolic extract of E. maritimun showed antimicrobial activity against S. aureus, B. cereus, Salmonella enterica, Pseudomonas aeruginosa, P. fluorescens, P. marginalis, E. coli, and Erwinia carotovora subsp. carotovora ^[40]. Although many species of Eryngium have shown antimicrobial activity against Gram-positive and Gram-negative bacteria, some species of fungi and yeasts, and viruses, it has been suggested that multi-target antimicrobial experiments should be carried out using extracts of Eymgium spp. as antimicrobial agents in order to expand the knowledge about its antimicrobial potential ^[41].

Additionally, it is important to point out that the study of the anticholelithiasis and trypanocidal activity shown by E. carlinae and E. heterophyllum, respectively, could extend to other species of Eryngium; likewise, other activities such as anticlastogenic, anticarcinogenic, antihelmintic, and larvicidal, amongst others reported for E. foetidum could be evaluated ^[2].

The biological activities reported for E. carlinae, E. comosum, E. cymosum, E. heterophyllum, and E. longifolium are summarized in Table 1.

Table 1. Confirmed biological activities in Eryngium species distributed in the central-western region of Mexico.

Eryngium sp.	Biological Activity Confirmed	Type of Extract	Plant Tissue	Model	Reference
E. carlinae	Hypolipidemic	Ethanolic	Plant	In vivo	^[9]^[11]
		Aqueous	Plant	Clinical trial	^[17]
		Hexanic	Inflorescence	In vitro and in vivo	^[12]
	Hypocholesterolemic	Ethanolic	Plant	In vivo	^[10]^[11]
	Hypocholesterolemic	Hydroalcoholic	Aerial parts	In vivo	^[14]
	Hypoglycemic	Hexanic	Inflorescence	In vivo	^[12]
	Hypoglycemic	Hexanic	Inflorescence	I vitro and in vivo	^[13]
	Antioxidant	Hydroalcoholic	Aerial parts	In vivo	^[14]
		Ethanolic	Plant	In vivo	^[10]
		Hexanic	Inflorescence	In vitro and in vivo	^[13]
	Diuretic-Renoprotective	Decoction	Plant	In vivo	^[16]
	Antimicrobiane (Pyhytophtora cinnamomi)	Ethanolic	Aerial parts	In vitro	^[22]
	Anticholelithiasis	Hydroalcoholic	Plant	In vitro	^[18]
	Antispasmodic	Methanolic	Aerial parts	In vivo	^[19]
E. comosum	Hypocholesterolemic	Aqueous	Plant	In vivo	^[26]
	Antioxidant	Aqueous and ethanolic	Plant	In vitro	^[23]
	Antioxidant	Ethanolic	Plant	In vitro	^[25]
	Antimicrobiane (Equine pathogens)	Ethanolic	Plant	In vitro	^[24]
	Cytotoxicity	Ethanolic	Plant	In vitro	^[25]
	Cytotoxicity	Aqueous and ethanolic	Plant	In vitro and in vivo	^[23]
E. cymosum	Hypoglycemic	Aqueous	Aerial parts	In vivo	^[27]
E. cymosum	Antihyperglycemic	Infusion	Plant	In vivo	^[42]
E. heterophyllum	Trypanocide	Methanolic	Aerial parts		^[34]
	Hypocholesterolemic	Aqueous	Plant	In vivo	^[31]
	Hypocholesterolemic	Decoction	Plant	Clinical trial	^[32]
E. longifolium	Hypoglycemic	Aqueous and ethanolic	Aerial parts	In vivo	^[35]

Plant—plant parts were not specified.

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Jeanette G. Cárdenas-Valdovinos

Ignacio García-Ruiz

María V. Angoa-Pérez

Hortencia G. Mena-Violante

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Update Date: 30 May 2023

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