Keywords

13.1 Introduction

The term halophyte is used to describe native flora grown in high salt concentrations with osmotic pressure of at least 3.3 bars, which are characterized by high physiological plasticity and the ability to thrive in a salinity-stressed environment (Jennings 1976). Halophytes have substantial economic potential by contributing enormously to environmental refurbishment and as potential sources of medicine. Halophytes have the ability to remediate the soil, accumulating large amounts of sodium salts through roots, improving nutrient availability, and creating microclimates favorable for the growth of fodder glycophytes, which contribute to the productivity of this ecosystem (Abdelly et al. 2011). Several species of halophytes are used as folk medicine and prove that halophytes have antipathogenic activity toward plants, animals, and humans. Recent reports reveal that secondary metabolites are responsible for their bioactivities in the pharmaceutical industry and medicine (Phillips et al. 2006; Falleh et al. 2011a, b). The Ayurveda system relies heavily on preventive medicine and the promotion of positive health. Ayurvedic preparations called Rasayanas are used to promote health. The Rasayanas are preparations from several plant extracts, containing strong antioxidants, and are used as rejuvenators or nutritional supplements (Govindarajan et al. 2005; Thyagarajan et al. 2002). In recent years, pharmacognostics and researchers of medicinal plants have identified the therapeutic properties of halophytes (Qasim et al. 2017).

Halophytic plants are salt-tolerant and have latent medicinal and nutraceutical properties that can potentially be used as a source of functional compounds in nutritional diets, such as flavonoids, high-molecular-weight tannins (Meot-Duros and Magné 2009; Falleh et al. 2011a), polyunsaturated fatty acids (Ksouri et al. 2009), and proteins and vitamins (Ksouri et al. 2011). In the Vedic period of India about 3500 years ago, the first medicine records books on Ayurveda and Charaka Samhita (600 BC) came about. Globally, approximately 25,000 halophyte species are known to grow under saline environments to date and are used as edible plants, animal fodder, biofuel, medicine, bioactive secondary metabolites (e.g., terpenes, phenols, antioxidants, anticarcinogenics), and ornamental plants (Abdelly et al. 2006). The species of halophytes from the genera Acanthus, Aegiceras, Avicennia, Bruguiera, Ceriops, Exoecariaceae, Kandelia, Rhizophora, Sonneratia, Suaeda, and Xylocarpus plants grow in brackish soil because they have the ability to survive in high-saline environments and in anaerobic soil (Thatoi et al. 2014). These genera of halophyte plants contain a number of phenolic compounds, such as anthocyanins, catechins, coumarins, flavones, flavonoids, isoflavones, isocatechins, and lignans, which are used as a rich source of antioxidants (Schwarzlander et al. 2008).

Currently, halophytes are attracting attention because of their nutraceutical potential, their strong antioxidant powers, and their therapeutic role in curing a number of diseases such as autoimmune pathological conditions, digestive system disorders, inflammation, neurodegenerative disorders, and viral infections. They are also used as an external source of antioxidants to detoxify the excess production of free radicals in the human body (Ramchoun et al. 2009). The antioxidants obtained from halophytes are in the form of herbal drugs used to protect against free radical-induced injury (Ksouri et al. 2009). The present review reports the pharmaceutical and therapeutic medicinal roles of halophytes for economic and safety reasons. They are the sources of natural antioxidants and biologically active compounds that may be used as potential substitutes in the pharmaceutical industry to replace synthetic medicine from natural biologically active compounds.

13.2 Folk Halophyte Species Used for Medicinal Value

The scarce literature available reveals that halophytes have been used in traditional medicine up to the present day. In this chapter, we discuss some of the medicinal halophyte species and their uses in folk medicine around the world.

Sea fennel or rock samphire (Crithmum maritimum) is an aromatic perennial plant present on cliffs and rocks or on the beach (Males et al. 2003). Guil-Guerrero et al. (1996) showed a keen interest in folk medicine, such as diuretics, antiscorbutics, and its digestive and purgative properties.

The root and rhyzomes of the salt-tolerant plant Glehnia littoralis, a perennial herb native to sandy seashores, of which the young flower buds and leaves are edible, have been customarily used as a diaphoretic, an antipyretic, and an analgesic (Rozema et al. 1985; Masuda et al. 1998; Um et al. 2010). Another salt-tolerant plant, Cynara cardunculus, commonly named “cardoon,” of the family Asteracae, is naturally grown under adverse environmental conditions, such as drought, high salinity, and high temperature (Fratianni et al. 2007). The plant leaf and stem are used in soups, salads, and sweet dishes (Gominho et al. 2000), the flowers are used in the preparation of cheese (Valentão et al. 2002), whereas leaves are mainly used in folk medicine as diuretic, antidiabetic, cholagogue, choleretic, and antimicrobial agents (Krizková et al. 2004; Fratianni et al. 2007).

In folk medicine, Inula viscosa, a member of the Asteracae family used as an anti-inflammatory, with antiscabies, antipyretic, antiseptic, and antiphlogistic activity for wound healing (Lauro and Rolih 1990; Ali-Shtayeh and Abu Ghdeib 1999) and in the treatment of diabetic patients (Yaniv et al. 1987). Also, the plant has been used in gastroduodenal disorders, in the treatment of tuberculosis, bronchitis, anemia, and as a promoter of female sterility and abortion induction (Al-Dissi et al. 2001). Cakile maritima L., an annual succulent halophyte, belongs to Brassicaceae and is distributed globally in sandy coastal areas (Clausing et al. 2000). It is traditionally used for its antiscorbutic, diuretic, digestive, and purgative properties (Guil-Guerrero et al. 1996; Davy et al. 2006). The weed Chenopodium album L. is a widely distributed halophyte. Its dried fruits have been used in folk medicine for their laxative, sedative, diuretic, hepatoprotective, and antiparasitic properties for many years (Fournier 1999; Dai et al. 2002). Roots of Asparagus officinalis are used to cure pains of the joints, hips, and back, and to rinse out the harmful substances of the bladder that cause gout in the feet. The roots of Asparagus racemosus are used against rheumatism and inflammation in traditional medicine (Goyal et al. 2003).

Thespesia populnea is a large halophytic plant found in the coastal regions of India. The above-ground part, such as the bark, leaves, flowers, and fruits, are used for medicinal purposes against dysentery, cholera, hemorrhoids, and infections such as eczema, guinea worm, psoriasis, ringworm, and scabies (Ilavarasan et al. 2003a, b), whereas the root, bark, and fruits are used against dysentery, cholera, and hemorrhoids (Ilavarasan et al. 2003b). The fruits are used to control diabetes, as vividly described in Ayurveda (Sathyanarayana et al. 2004). In southern India and Sri Lanka, the leaves and bark used for oil production are also used for fracture wounds and as an anti-inflammatory poultice applied to ulcers and boils (Jayaweer 1982). The plant Limoniastrum monopetalum is used in folk medicine for its antidysenteric, antibacterial, and anti-inflammatory properties against infectious diseases that cause body pain, bloody diarrhea, and for treating hemorrhage and menstrual disorders in women (Chaieb and Boukhris 1998; Aniya et al. 2002; Murray et al. 2004). A broad range of halophytes are used as natural medicines for a number of diseases, such as asthma (Evolvulus alsinoides), as a diuretic (Portulaca quadrifida), for the eyes (Zygophyllum simplex), gonorrhea (Portulaca oleracea), heart disease (Capparis decidua, Kochia indica), as a laxative (Capparis decidua), pain killer (Solanum surattense), for pneumonia (Corchorus depressus), as a sedative (Withania somnifera), for skin diseases (Salsola imbricata), snakebites (Rumex vesicarius), and ulcers (Ceriops tagal) (Khan and Qaiser 2006; Ksouri et al. 2011).

13.3 Release of Bioactive Compounds, Properties, and Medicinal Uses

Medicinal halophytes have a wide range of bioactive compounds that can used to treat human infirmities. They are consumed either as whole plants or specific parts only for medicinal purposes. Currently, a huge range of medicinal halophytes are being used in salads, vegetables, coloring, flavoring, and as spicing agents in food (Qasim et al. 2014). Halophytes have a broad range of bioactive complexes (primary and secondary metabolites), i.e., essential oils (terpenes), polyunsaturated carotenoids, fatty acids, glycosides, polysaccharides, sterols, phenolic compounds, and are a rich source of vitamins. These bioactive substances have potent anti-inflammatory, antimicrobial, antioxidant, and anticarcinogenic activity, and the complexes avert various diseases (such as atherosclerosis, cancer, cardiovascular disorders, and chronic inflammation). They are a modern source of health products such as nutraceuticals, growth regulators, and are cost-effective medicines. Bioactive compounds that are beneficial to health are the primary and secondary metabolites discussed in this chapter.

13.3.1 Primary Metabolites

A primary metabolite (central metabolites) is one that plays a direct role in growth, development, and differentiation. Usually synthesized directly by sunlight, it has a physiological function in the organism and is a major constituent of organisms or cells (Bernal et al. 2011). Primary metabolites are mainly carbohydrates and their derivatives, lipids, certain amino acids, and related compounds (Ksouri et al. 2011).

13.3.2 Carbohydrates and Glycosides

Carbohydrates are primarily synthesized by the photosynthetic activity of plants acting as storage and structural components. These compounds have a probiotic effect or commonly have antioxidant or anti-inflammatory activity (Bernal et al. 2011). Macrophages stimulated by S. herbacea play a substantial protagonistic role in the host–pathogen defense mechanism by releasing nitric oxide and cytokines (Im et al. 2003) and have an inhibitory effect on tumor cell growth and micro-organism infection (Lee et al. 2006). Many halophytic plant glycosides have antidiabetic, antibacterial, anti-obesity, and cancer prevention activity, in addition to antineoplastic effects (Erkucuk et al. 2009). A metabolite, namely a glucosinolate derived from amino acid biosynthesis (Podsedek 2007), is one of the most important metabolites of the Brassicaceae family and acts as a cholesterol-reducing agent, an anticarcinogenic substance, and has folk pharmacological effects in humans (Cieslik et al. 2007). Radwan et al. (2008) reported that glucotropaeolin, ethyl glucosinolate, 2-methyl butyl, and 4-pentyl glucosinolate are major constituents of the halophyte C. maritima. These four glucosinolates display robust antioxidant activity against molluscicidals caused by Biomphalaria alexandrina. Cardiac glycosides (bufadienolides) are synthesized by Urginea maritima (Adams et al. 2009) and extract obtained from this halophyte is widely used for the prevention of heart failure and kidney disorder (Hänsel et al. 1994). Saponins are amphipathic glycosides and have hemolytic, immunological, antibacterial and antidiabetic properties, increase testosterone levels, and stimulate muscle growth (Kimura et al. 2006; Li et al. 2009). The pharmaceutical industry requires saponins, because researchers believe them to be a major constituent of drugs and folk medicines obtained from natural plants and used in the cosmetic and phytotherapy industries (Estrada et al. 2000). Bioactive compounds obtained from the extract of Tribulus terrestris have anti-hypertensive activity in rats and are also involved in smooth muscle relaxation via membrane hyperpolarization and in releasing nitric oxide (Phillips et al. 2006).

13.3.3 Lipids

Natural lipids and their derivatives quarantined from halophytic plants show important biological activity and antibacterial qualities, including phototoxic, antimicrobial, anticarcinogenic, and antifungal medicinal properties (Dembitsky 2006). Lipids are a large cluster of regular compounds that include carotenoids, natural fats, fat-soluble vitamins (A, D, E, and K), phospholipids, sterols, mono- and di-glycerides, and waxes (Ksouri et al. 2011). Lipids obtained from halophytic plant species are used as nutraceuticals and for medicinal purposes in humans. Halophyte seeds and stems are an original source of unsaturated fatty acids with a cis-configuration double bond between carbon skeleton C16 and C20 (Stuchlik and Zak 2002). Humans cannot synthesize certain fatty acids, such as ω-3 (α-linolenic acid), ω-6 (linoleic acid), and ω-9 (oleic acid), but halophytes are a good source of these polyunsaturated fatty acids (Herbaut 2006). Eicosapentaenoic acid and docosahexaenoic acid are synthesized from ω-6 (linoleic acid), which is converted to eicosanoids (hormone-like compounds), for vital organ functioning and intracellular activity (Reiffel and Mc Donald 2006). 5-hydroxyindoleacetic acid in cerebrospinal fluid can cause depression and suicide, but is neutralized by docosahexaenoic acid extracted from Salicornia bigelovii (McNamara et al. 2009). γ-Linolenic and arachidonic acids are precursors of prostaglandins in the human body, which protect the blood vessels of the brain and prevent oxygen deficiency. Descurainia sophia, commonly known as a Chinese halophyte, contains 76.6% polyunsaturated fatty acid, 53.7% linolenic acid with α-linolenic acid, γ-linolenic acid, and the arachidonic acid content is 5.3% (Yajun et al. 2003) (Tables 13.1 and 13.2).

Table 13.1 Halophytes traditionally used as folk medicine
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Table 13.2 Bioactive compounds of halophytes and their medicinal uses
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The halophyte species Crithmum maritimum contains 81% total fatty acids, and has resilient antimicrobial activity against Bacillus cereus, Candida albicans, Erwinia carotovora, Micrococcus luteus, P. aeruginosa, P. marginalis, Pseudomonas fluorescens, and Salmonella arizonae, with a low concentration ranging between 1 and 100 μg ml−1 (Zarrouk et al. 2003; Meot-Duros et al. 2008). The genus Thapsia has a high level of petroselinic acid, an isomer of oleic acid, which is interestingly used as a oleochemical in the cosmetics and pharmaceutical industries (Murphy 1994; Avato et al. 2001).

Halophytes are rich sources of phytosterols and tocopherols because they have lipophilic constituents, protecting against lower risk cancer and long-lasting diseases, maintaining the concentration of serum cholesterol, and preventing the risk for atherosclerosis (Ortiz et al. 2006; Patel and Thompson 2006). Oils obtained from the unsaponifiable fraction of halophytes, biological active emulsifiers, and the high content of phytosterols maintain the structure and permeability of the membrane, interacting with alcohol, lipids, phenol, and some heterocyclic ingredients (Gusakova et al. 1998). Isolation from halophyte species Teucrium abutiloides and Teucrium betonicum extract results in a wide range of biologically active complexes, i.e., poriferasterol, clerosterol, and (24S)-24-ethylcholesta-5, 22, 25-trien-3β-ol (Gaspar et al. 1996; Fontana et al. 1999). Oil from Teucrium seeds is rich in tocopherols, with a total content varying between 534 and 569 mg/kg of seed oil (Hachicha et al. 2009). The alpha-tocopherol level in T. nabli it is 296 mg kg−1), in T. alopecurus it is 316 mg kg−1), and in T. polium it is 277 mg kg−1, whereas the lowest amount of β-tocopherol is detected. Hippophae rhamnoides L. pericarp oil is enriched with triacylglycerols (palmitoleic 16:1(9) acid), vitamins E and F, carotenoids (cryptoxanthin, carotene, physalin, zeaxanthin), alkanols, phytosterols, and tocopherols (Gusakova et al. 1998). Teucrium (and Batis maritima and Hippophae rhamnoides oil) (Kallio et al. 2002; Hachicha et al. 2009) contains phytosterols and tocopherols in higher amounts than Glycine max, Medicago sativa, Avocado persea, Olea europeae, and Zea mays, but protects from melanocyte-forming processes and skin diseases (Hachicha et al. 2009). Apium graveolens root extract contains high amounts of falcarindiol, falcarinol, and panaxadiol (Zidorn et al. 2005).

13.3.4 Secondary Metabolites

The term secondary metabolite, or phytochemical, refers to a broad spectrum of plant metabolites that have low molecular weights and are widely distributed in plants (Acamovic and Brooker 2005; Edreva et al. 2008). Plants produce secondary metabolites to protect themselves against environmental stresses and they are defined as those substances (Smitha Patel et al. 2013) generated in natural food stuffs by the normal metabolism of species and by different mechanisms, for example, the inactivation of some nutrients, the diminution of the digestive process, or the metabolic utilization of food that exerts effects contrary to optimal nutrition (Kumar 1991).

13.3.4.1 Phenolic Compounds

Phenolic compounds are simple phenol derivatives of hydroxybenzoic acid (hydrolyzable tannins) to condensed tannins (Tania da et al. 2012). The two types differ in their effects on animals, one with respect to nutrient digestibility and the second causes toxic manifestations owing to hydrolysis in the rumen (Smitha Patel et al. 2013). A wide range of phenolic compounds are present in different halophyte species, such as flavonoids, isoflavones, coumarins, and phenolic acids, which are widespread in the leaf, stem, flower, and seed of halophytes (Miniati 2007). The main difference between usual phenolic and biological active phenolic complexes is that they act as folk medicine and have nutraceutical properties without any antagonistic effect (Bernal et al. 2011). Nowadays, in human food, halophytes are supplementary in the promotion of health care activities such as reducing body weight, having anticarcinogenic and anti-inflammatory properties, decreasing blood sugar levels, and having antithrombotic and anti-aging actions (Senevirathne et al. 2006). A finding from Sharifi et al. (2003) showed that Tribulus terrestris roots and fruit are rich sources of alkaloids, flavonoids, glycosides, saponins, and play a potential biological role in growth and development.

The species Atriplex halimus and Nitraria tangutorum have potent antioxidant activity owing to abundant flavonoids (isorhamnetin, kaempferol, patuletin, quercetin, spinacetin, and tricin) in food (Benhammou et al. 2009). Phenol derivative compounds, i.e., ferulic acid betacyanin, flavonol, hyperoside, and rutin isolated from the shoots of Mesembryanthemum edule, are used to prevent oxidative stress-related diseases and nutritional food in folklore (Van Der Watt and Pretorius 2001; Falleh et al. 2011a, b). These compounds are derived from a phenolic structure, with -OH groups showing antibacterial, anticancer, and antiviral activities (Okuda 2005). Mesembryanthemum edule has antioxidant properties and detoxifies the superoxide, 2,2'-azino-bis-3-ethylbenzothiazoline-6-sulfonic acid, and 2,2-diphenyl-1-(2,4,6-trinitrophenyl) hydrazyl radicals that accumulate during oxidative stress. Herba Artemisiae Scopariae is found in abundance in phenolic bioactive compounds, i.e., chlorogenic acid, P-hydroxyacetophenone, and caffeic acid, and is clinically used for the treatment of severely icteric contagious oral ulcer and hepatitis (Xu 1995).

Seo et al. (2003) also found that methanolic extract from Artemisia capillaris shows strong antioxidant activity in hyperlipemia. Cynarin is a caffeoyl derivative phytocompound of poly-phenols in the halophyte species Cynara cardunculus, which acts as an antioxidant, cholesterol synthesis inhibitor, and hepato-protector (Gebbart 1998). Limoniastrum monopetalum leaf extract, which is rich in polyphenol content, shows antioxidant, superoxide scavenger, and antimicrobial activity (Trabelsi et al. 2010). Cocos nucifera leaf and stem extract has larger amounts of bioactive polyphenol compounds, i.e., vanillic, chlorogenic, and ferulic acids, as identified by Ralay Ranaivo et al. (2004). Five different classes of bioactive complexes have been identified in Plantago major, namely vanillic acid (benzoic compound), baicalein, luteolin (flavonoids), aucubin (iridoid glycoside), caffeic acid, p-coumaric acid (hydroxy-cinnamic acids), and ursolic acid (triterpenes) (Duke 1992; Samuelsen 2000).

Tungtungmadic acid, quercetin 3-O-glucoside, and isorhamnetin 3-O-glucoside with 1,1 diphenyl-2-picrylhydrazyl have a scavenging effect against oxidative stress and have been reported in Salicornia herbacea (Park and Kim 2004; Rhee et al. 2009). Chenopodiaceae and Plumbaginaceae families have a number of bioactive compounds that play pharmacological and bio-technological roles (Saïdana et al. 2008) in the development of new drugs. The halophyte Suaeda fruticosa has been found to have hypolipidemic and hypoglycemic properties (Benwahhoud et al. 2001). A wide range of secondary metabolites in Rubia tinctorum extract, i.e., di-hydroxyanthraquinones, tri-hydroxyanthraquinones, and purpurin derivatives, show bactericidal, antifungal, antipruritic, antinociceptive, and anti-inflammatory effects (Bányai et al. 2006).

Terminalia catappa has a great antioxidant, antibacterial, and antisickling potential, in addition to antisteroidogenic and hepatoprotective activity owing to bioactive punicalagin, punicalin, quinones, and tannin components of inflammation induced by carrageenan in rats, and genotoxicity induced by bleomycin in rabbits (Chen et al. 2000). Asparagus officinalis root extract contains an active amino acid and its derivatives, flavonoids, oligosaccharides, and steroidal saponins (Fukushi et al. 2000; Hayes et al. 2006). Two halophyte species, Cakile maritima and Thellungiella salsuginea, have been found to have a high degree of salt tolerance and a potential rich in antioxidants owing to higher amounts of phenolic compounds, glucosinolate compounds, ascorbic acid, alkaloids, coumarins, flavonoids, sterols, sulfur glycosides, and triterpenes (Jahangir et al. 2008; Radwan et al. 2008). Hippophae rhamnoides fruits, which are rich in fatty acids, flavonoids, and other healthy components (vitamin C, E, and other nutrients), are used in the formation of soft gelatin capsules for treating cardiovascular disease (Rosch et al. 2004).

13.3.4.2 Uses of Bioactive Compounds

Usually, halophytes contain a wide range of primary and secondary compounds in bioactive form and they are used as a potential source of natural vitamins, fatty acids, amino acids, flavonoids, alkaloids, terpenes, and isoflavonoids. Halophytes have been used since ancient times in folk medicine and play an important role in community health and safety owing to confirmed roles in human growth and development, in addition to reducing the risk of disease (Lagos et al. 2015). Halophytes contain nutritional components required for the healthy survival of humans, or nutraceuticals, when the aim is to treat/prevent a disease or disorder (Kalra 2003), with various reported bioactive functions (e.g., antioxidant, antimicrobial, immunomodulatory, hypocholesterolemic, etc.), often because of the incorporation of functional enzymes, fibers, isoflavones, peptides, phytic acids, phytosterols, prebiotics, probiotics, proteins, and saponins (Stankovi et al. 2015; Jdey et al. 2017).

13.4 Conclusion

Halophytes are exclusive sources of folk medicine and are of nutraceutical value for most of the world’s population (Hamburger and Hostettmann 1991). A variety of plant chemicals have therapeutic importance, such as low-molecular-weight proteins and peptides or glycosides. These metabolites, which include alkaloids, essential oils, flavonoids, phenolic acids, phytoalexins, saponins, and tannins, could also form part of a plant’s defense against microbes (Van Etten et al. 1989; Maher et al. 1994), and show antifungal, antimicrobial, anti-inflammatory, antioxidant, and anticarcinogenic activity (Robert and Seletrennikoff 1986; Terras et al. 1992). In addition, they can cure various diseases and are a novel source of nutraceuticals and growth regulators. Despite the wide use of halophytes, their therapeutic value has not been fully substantiated and the mode of action of bioactive compounds against diseases has not yet been established. Alkaloids, flavonoids, and glycosides isolated from halophytes may be responsible for their pharmacological activities. The road ahead consists in establishing the specific bioactive molecules that might be responsible for these actions. Therefore, the cultivation, collection, and further pharmacological exploration of halophytes are essential.