Salicornia europaea L. and Suaeda maritima (L.) Dumort: bioactive compounds and future perspectives

Figures & data

Figure 1. PRISMA 2020 flow diagram [20].

Table 1. Phytochemical composition of S. europaea L.

Biologically active compound	Plant part	References
Macroelements
Sodium	Leaves, Stems and Roots	[30]
Calcium	Leaves, Stems and Roots	[16,30]
Potassium	Leaves, Stems and Roots	[16,30]
Magnesium	Leaves and Stems	[16,30]
Phosphorus	Leaves and Stems	[30]
Microelements
Iron	Leaves and Stems	[16,30]
Copper	Leaves and Stems	[30]
Zinc	Leaves and Stems	[30]
Manganese	Leaves and Stems	[30]
Nickel	Leaves and Stems	[30]
Silicon	Leaves and Stems	[30]
Vitamins
Vitamin A	Leaves and Stems	[30]
Vitamin C	Leaves and Stems	[30]
Vitamin B1	Leaves and Stems	[30]
Vitamin B2	Leaves and Stems	[30]
Vitamin B3	Leaves and Stems	[30]
Vitamin B6	Leaves and Stems	[30]
Pigments
β-carotene	Leaves and Stems	[30]
Oleanane triterpenoid saponins
3b-Hydroxy-23-oxo-30-noroleana- 12,20(29)-diene-28-oic acid	Leaves and Stems	[28]
3-O-β-D-Glucuronopyranosyl-28-O-β-D-glucopyranoside	Leaves and Stems	[28]
30-Norhederagenin 3-O-b-D-glucuronopyranosyl-28-O-b-D-glucopyranoside	Leaves and Stems	[28]
30-Norhederagenin 3-O-b-D-glucuronopyranosyl-28-O-b-D-glucopyranoside	Leaves and Stems	[28]
Gypsogenin	Leaves and Stems	[31]
Gypsogenin 3-O-b-D-glucuronopyranoside	Leaves and Stems	[28,31]
Gypsogenin 3-O-b-D-glucuronopyranosyl-28-O-b-D-glucopyranoside	Leaves and Stems	[28]
3b,29-Dihydroxyolean-12-en-28-oic acid 28-O-b-D-glucopyranosyl ester	Leaves and Stems	[28]
Oleanolic acid 28-O-b-D-glucopyranoside	Leaves and Stems	[28]
Chikusetsusaponin IVa	Leaves and Stems	[31,32]
Chikusetsusaponin IVa methyl ester	Leaves and Stems	[28,32]
Calenduloside E	Leaves and Stems	[28,31]
Calenduloside E 60-methyl ester	Leaves and Stems	[28]
Caffeoylquinic acid derivatives
Tungtungmadic acid (3-caffeoyl-4-dihydrocaffeoyl quinic acid	Leaves and Stems	[28]
5-dicaffeoylquinic acid	Leaves and Stems	[28]
Methyl 3,5-dicaffeoylquinate	Leaves and Stems	[28]
3,4-Dicaffeoylquinic acid	Leaves and Stems	[28]
Methyl 4-caffeoyl-3-dihydrocaffeoylquinate	Leaves and Stems	[28]
4-Dihydrocaffeoyl quinic acid	Leaves and Stems	[33]
Flavonoids and flavanones
20-Hydroxy-67-methylenedioxyisoflavone	Leaves and Stems	[28]
(-)-(2S)-20-Hydroxy-6,7-methylenedioxyflavanone	Leaves and Stems	[28]
20,7-Dihydroxy-6-methoxyisoflavone	Leaves and Stems	[28]
5,7,2-Trihydroxy-6-methoxyisoflavone (Irilin B)	Leaves and Stems	[34]
Quercetin 3-O-(6″-O-malonyl)-β-D-glucoside	Leaves and Stems	[28]
Quercetin	Leaves and Stems	[26, 28,32]
Quercetin 3-O-β-D-glucopyranoside	Leaves and Stems	[26,28,31,35]
Quercetin-3′,4′-di-O-β-D-glucopyranoside	Leaves and Stems	[33]
Rutin	Leaves and Stems	[26,28,29,32]
Isorhamnetin 3-O-β-D-glucopyranoside	Leaves and Stems	[28,35]
Quercetin 3-O-(6”-O-malonyl)-b-D-glucoside	Leaves and Stems	[28]
Isoquercitrin 6”-O-methyloxalate	Leaves and Stems	[28]
2S-20,7-Dihydroxy-6-methoxyflavanone	Leaves and Stems	[28]
2S-20-Hydroxy-6,7-dimethoxy-flavanone	Leaves and Stems	[28]
2S-5,20-Dihydroxy-6,7-methylenedioxyflavanone	Leaves and Stems	[28]
Luteolin	Leaves and Stems	[26,28,31,32]
Acacetin	Leaves and Stems	[31]
Kaempferol	Leaves and Stems	[28,32]
Kaempferol-3-O-b-D-glucoside	Leaves and Stems	[28,31,32]
Hesperidin	Leaves and Stems	[26,31]
Hesperetin	Leaves and Stems	[31]
Rhamnetin	Leaves and Stems	[26]
Isorhamnetin	Leaves and Stems	[31]
Isorhamnetin-3-O-b-Dglucopyranoside	Leaves and Stems	[31]
Chromones
6,7-Methylenedioxychromone	Leaves and Stems	[28]
6,7-Dimethoxychromone	Leaves and Stems	[28]
7-Hydroxy-6-methoxychromone	Leaves and Stems	[28]
7-O-b-D-Glucopyranosyl-6-methoxychromone	Leaves and Stems	[28]
7-Hydroxy-6,8-dimethoxychromone	Leaves and Stems	[28]
Sterols
Stigmasterol	Leaves and Stems	[28,32]
Ergosterol	Leaves and Stems	[28]
β-Daucosterol	Leaves and Stems	[28,32]
Cerevisterol	Leaves and Stems	[28]
β-Sitosterol	Leaves and Stems	[28,32]
Lignans
Syringaresinol 4-O-b-D-glucopyranoside	Leaves and Stems	[28]
Erythro-1-(4-O-b-D-glucopyranosyl-3,5-dimethoxyphenyl)-2-syringaresinoxyl-propane-1,3-diol	Leaves and Stems	[28]
Ongifloroside B	Leaves and Stems	[28]
(-)-Syringaresinol	Leaves and Stems	[28,32]
Episyringaresinol-40′′-O-b-D-glucopyranoside	Leaves and Stems	[28]
Tortoside A	Leaves and Stems	[28]
Acanthoside B	Leaves and Stems	[17,28]
Fatty acids
Stearic acid	Leaves and Stems	[28,36,37]
γ-Linolenic acid	Leaves and Stems	[28,36,37]
Linoleic acid	Leaves and Stems	[28,36,37]
Palmitic acid	Leaves and Stems	[28,36,37]
Oleinic acid	Leaves and Stems	[36,37]
Myristic acid	Leaves and Stems	[37]
Phenolic acids
Vanillic aldehyde	Leaves and Stems	[26,28]
Catechol benzoic acid	Leaves and Stems	[28]
Tannic acid	Leaves and Stems	[26]
Quinic acid	Leaves and Stems	[26]
Hydroxycinnamic acids
Protocatechuic acid	Leaves and Stems	[28]
Ferulic acid	Leaves and Stems	[16,28,38]
Caffeic acid	Leaves and Stems	[28]
p-Coumaric acid	Leaves and Stems	[16,26,35]
Rosmarinic acid	Leaves and Stems	[26]
Chlorogenic acid	Leaves and Stems	[26,29]
Others
Uracil	Leaves and Stems	[28]
Icariside B2	Leaves and Stems	[28]
Phytol	Leaves and Stems	[28,31,32]
Dioctyl phthalate	Leaves and Stems	[28]
Dibutyl phthalate	Leaves and Stems	[28]
Pheophorbide A	Leaves and Stems	[28]
(13^2S)-Hydroxy-pheophorbide A	Leaves and Stems	[28]
Malic acid	Leaves and Stems	[26]
5-(Hydroxymethyl)furfural	Leaves and Stems	[16]
1-Octadecanol	Leaves and Stems	[28]
1-Octacosanol	Leaves and Stems	[28]

Table 2. Biological activities of S. europaea L.

Study objectives	Study design	Study duration	Main results	Ref.
Evaluation of the effects on memory of S. europaea L.	Fifty-three participants: 26 participants received 600 mg of S. europaea L.extract daily, 27 were in the placebo group.	12 weeks	Improvement of the cognitive function in the patients with mild cognitive impairment.	[39]
Assessment of the influence of S. europaea L. on progression of Alzheimer’s disease	Forty male mice divided into five groups: control group - intraperitoneal injection with 0.9% saline; 2^nd group − 2 mg/kg scopolamine intraperitoneally; 3rd group − 50 mg/kg S. europaea L. extract orally and 2 mg/kg scopolamine intraperitoneally; 4^th group − 100 mg/kg S. europaea L. extract orally and 2 mg/kg scopolamine intraperitoneally; 5^th group − 10 mg/kg tacrine orally and 2 mg/kg scopolamine intraperitoneally.	1 week	Antiamnesic effects, improved behavioural and cognitive deficits. Anti-cholinesterase, antioxidative and anti-neuroinflammatory activity.	[40]
Evaluation of the effects of S. europaea L. on vascular dysfunction and hypertension, caused by excessive salt intake.	Male rats randomly divided into six groups: Two control groups, Group 3 consumed high quantity of salt, Group 4 and 5 had intake of 1400 mg/kg S. europaea L. extract daily.	6 weeks	S. europaea L. did not cause dysfunction of the coronary artery even though it had a high salt content. Improved prevention of the occurrence of hypertension and vascular dysfunction.	[16]
Examination of the effects of S. europaea L. on prevention of atherosclerosis and postangioplasty restenosis.	Twenty-eight male mice divided into four groups: the 1^st, 2^nd and 3^rd group received orally desalted S. europaea L. extract 1.5, 15 and 150 mg/kg daily, respectively; the control group received orally an equivalent volume of 1% gum Arabic solution.	2 weeks	Suppressed vascular smooth muscle cells migration and proliferation.	[35]
Assessment of the influence of S. europaea L. on microglial inflammation.	Thirty-six male mice divided into 4 groups: the 1st group received orally 0.9% isotonic solution, the 2^nd (negative control) received orally neurotoxin. Groups 3 and 4 had also oral intake of S. europaea L. extract and the neurotoxin.	7 days	Anti-neuroinflammatory and antioxidant activity.	[34]
Evaluation of antidepressant effects of S. europaea L.	Sixty male mice divided into six groups: The 1^st and the 2^nd group had intake of distilled water. The 3^rd group received venlafaxine in a dose of 9.38 mg/kg. Groups 4, 5 and 6 received S. europaea L. extract in a dose of 1.8, 1.35 and 0.9 g/kg, respectively.	3 weeks	S. europaea L. extract demonstrated antidepressant effect.	[41]
Evaluation of the efficacy of S. europaea L. on obesity.	Fifty male rats divided equally into 5 groups: 1^st received saline, 2^nd received high-fat diet, 3^th group - high-fat diet and 250 mg/kg daily orally desalted S. europaea L. powder, 4^th group - high-fat diet and 500 mg/kg daily orally desalted S. europaea L. powder, 5^th group - high-fat diet and 200 mg/kg daily Garcinia cambogia.	12 weeks	Antiobesity activity.	[42]
Evaluation of the antimicrobial and antifungal effects of S. europaea L.	In vitro study: Escherichia coli, Klebsiella pneumonia, Bacillus subtilis and Staphylococcus aureus and two fungal strains including Candida albicans and Candida parapsilosis were used. For controls were used ampicillin for bacteria and fluconazole for fungal strains.	–	Antimicrobial and antifungal activity.	[43]
Assessment of the protective effect of S. europaea L. on skin epithelium.	Twenty-nine healthy women (age 30-55). Cream containing S. europaea L. extract was topically applied on the one side of the face of the participants. The test zones of the face were exposed to sun for 3 h daily from September to November.	12 weeks	Improved skin surface texture in the sun-exposed areas. No adverse effects were observed.	[44]
Evaluation of the influence of S. europaea L. on PGE2, NO production and ROS levels	In vitro cell culture study. Model cells: RAW 264.7 macrophages.	–	Suppression of PGE2 production. Inhibition of NO release. Inhibition of intracellular ROS activity.	[33]

Table 3. Phytochemical composition of S. maritima L.

Biological compound	Plant part	References
Macroelements
Sodium	Leaves and Stems	[11]
Calcium	Leaves and Stems	[11]
Potassium	Leaves and Stems	[11,64]
Magnesium	Leaves and Stems	[11,59]
Phosphorus	Leaves and Stems	[64]
Microelements
Iron	Leaves and Stems	[11,59]
Chromium	Leaves and Stems	[11,59]
Copper	Leaves and Stems	[11,59]
Manganese	Leaves and Stems	[11,59]
Zinc	Leaves and Stems	[11,59]
Nickel	Leaves and Stems	[11]
Pigments
Lutein	Leaves and Stems	[11]
β-Carotene	Leaves and Stems	[11,31]
Vitamins
Vitamin A	Leaves, Stems and Roots	[11,31]
Vitamin E	Leaves, Stems and Roots	[11,31]
Vitamin C	Leaves and Stems	[11,31,64]
Vitamin B1	Leaves and Stems	[64]
Vitamin B2	Leaves and Stems	[64]
Vitamin B6	Leaves and Stems	[11]
Phenolic acids
3,4-Dihydroxybenzoic acid	Leaves and Stems	[11]
p-Hydroxybenzoic acid	Leaves and Stems	[11]
3-Hydroxybenzoic acid	Leaves and Stems	[11]
Vanillic acid	Leaves and Stems	[11]
Syringic acid	Leaves and Stems	[11]
Salicylic acid	Leaves and Stems	[11]
Ellagic acid	Leaves and Stems	[11]
Hydroxycinnamic acids
Neochlorogenic acid	Leaves and Stems	[11]
Chlorogenic acid	Leaves and Stems	[11,31,66]
Caffeic acid	Leaves and Stems	[11,31,66]
Coumaric acid	Leaves and Stems	[11]
Ferulic acid	Leaves and Stems	[11,66]
Methyl trans-ferulate	Leaves and Stems	[31]
Methyl cis-ferulate	Leaves and Stems	[31]
Sinapic acid	Leaves and Stems	[31,66]
Rosmarinic acid	Leaves and Stems	[11]
Cinnamic acid	Leaves and Stems	[11]
n-Tetradecanyl dihydrocaffeate	Leaves and Stems	[66]
n-Hexadecanyl dihydrocaffeate	Leaves and Stems	[66]
Flavonoids
Catechin hydrate	Leaves and Stems	[11]
Epigallocatechin gallate	Leaves and Stems	[11]
Epicatechin	Leaves and Stems	[11,63]
Ouratea-catechin	Leaves and Stems	[11]
Quercetin	Leaves and Stems	[11,31,66]
Kaempferol	Leaves, Stems and Roots	[31,56,63,66]
Taxifolin	Leaves and Stems	[11]
Naringenin-7-glucoside	Leaves and Stems	[11]
Luteolin-7-o-glucoside	Leaves and Stems	[11]
Rutin	Leaves and Stems	[11]
Tannins
Ellagitannin	Leaves	[63]
Fatty acids
Myristic acid	Leaves	[65]
Palmitic acid	Leaves	[61,65]
Methyl palmitate	Leaves	[65]
Stearic acid	Leaves	[61]
Oleic acid	Leaves	[61]
Linoleic acid	Leaves	[61]
Linolenic acid	Leaves	[61]
6,11-Eicosadienoic acid methyl ester	Leaves	[65]
9,12-Octadecadienoic acid	Leaves	[65]
Steroids
Campesterol	Leaves	[65]
Essential oils
Cirtonellyl propionate	Leaves	[65]
Cirtonellyl acetate	Leaves	[65]
2-hexyl-1-octanol	Leaves	[65]
Citronellal	Leaves	[65]
Aciphyllene	Leaves	[65]

Table 4. Biological activities of S. maritima L.

Study objectives	Study design	Study duration	Main results	References
Evaluation of the antimicrobial activity of S. maritima L.	The antimicrobial activities of different S. maritima L. extracts were examined by using agar disc diffusion method. Four bacterial strains were used, including Escherichia coli, Klebsiella pneumonia, Staphylococcus aureus, and Streptococcus pneumoniae. For positive control was used levofloxacin. The plates were incubated at 37° for 24 h. The antimicrobial activities were determined by calculating the diameter of the growth inhibition zones.	–	Demonstrated inhibition against the tested gram-positive and gram-negative bacterial strains.	[62]
Assessment of the antibacterial activity of S. maritima L. against Pseudomonas aureginosa.	Forty-five fish were used for the study. They were infected with Pseudomonas aureginosa. The fish were equally divided into five groups. The first group was control group. The second group received amoxicilline 25 mg/g. The third group received 25 mg/g crude leaf extract and the fourth group received 10 mg/g purified leaf extract.	5 days	Observed antimicrobial activity against Pseudomonas aeruginosa.	[63]
Examination of the antioxidant activity of S. maritima L. extract.	The antioxidant activity was determined in vitro with different concentrations of leaf exctract. For control was used Vitamin C. The DPPH assay, nitric oxide radical scavenging assay, superoxide radical scavenging assay and lipid peroxide radical scavenging assay were performed.	–	Demonstrated radical scavenging activity.	[59]
Assessment of the activity of S. maritima L. against Hepatitis B virus.	The assay was performed with extracts with different concentrations by the radiometric method. Control was used without the halophyte leaf extract. Liquid scintillation was used to determine the radiation. The percent of inhibition of the DNA polymerase activity was calculated.	–	Demonstrated inhibitory effect against the Hepatitis B virus DNA polymerase.	[59]
Evaluation of the inhibitory activity of S. maritima L.against HIV-1 reverse transcriptase.	The assay was performed by the radiometric method. Control was used without the halophyte leaf extract. Liquid scintillation was used to determine the radiation. The percent of inhibition was calculated.	–	Demonstrated inhibitory effect against the HIV-1 reverse transcriptase.	[59]
Evaluation of the toxicity of S. maritima L. extract.	Female albino rats were used for the experiment. The animals received 250 mg/kg body weight of the S. maritima L. leaf extract. The animals were observed for 24 h. If there was no observed mortality, the experiment was conducted with a higher dose − 300 mg/kg body weight.	24 h	A toxic effect was not observed.	[59]
Evaluation of the depressant activity of S. maritima L. extract relative to central nervous system.	Twenty mice were used for the study. They were divided equally into four groups. The first group was for control. The second group received 1 mg/kg of diazepam. The third and the forth group received 250 mg/kg and 500 mg/kg, respectively. The number of movements of the mice were scored to assess the central nervous system depressant activity.	1 h	Significant depressant activity relative to central nervous system.	[52]
Assessment of the effect of S. maritima L. extract on gastrointestinal motility activity.	Twenty mice were used for the study. They were divided equally into four groups. The first group was for control. The second group received loperamide 25 mg/kg. The third and the fourth group received 200 mg/kg and 400 mg/kg respectively. After 30 min, the distances traveled by charcoal meal were measured.	30 min	Reduction in gastrointestinal motility.	[52]
Examination of the cytotoxic effect of S. maritima L. extract.	Brine shrimp lethality test was used. The percent of mortality was determined.	24 h	Strong cytotoxic activity was observed.	[52]

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