ABSTRACT
Plants belonging to the genus Curcuma are gaining importance globally as one of the significant ingredients in food and traditional medicines. Apart from being considered as nutritionally rich food products, interest in medicinal properties of Curcuma species has increased due to the discovery of novel bioactive compounds possessing wide bioactivities such as antioxidant, antiviral, antimicrobial, and anti-inflammation activities. This article summarizes the literature pertaining to the nutritional values, bioactive compounds, as well as the biological activities of 16 edible Curcuma species. Additionally, the bioavailability, cytotoxicity, and allied health benefits of these species are also discussed and highlighted. The brief information provided in this review will open future perspectives for investigations related to their possible use as functional foods and in pharmaceutical applications.
Introduction
Curcuma, belonging to the family Zingiberaceae, is an economically important genus having both medicinal and food values. According to Xia et al.,[Citation1] the genus Curcuma comprises of 70 perennial rhizomatous species, which are distributed widely throughout tropical and subtropical regions of the world. The rhizome of Curcuma is a source of a yellow dye and has been historically used as spices, food preservatives, flavoring agent, and household remedy for treatment of many diseases.[Citation2,Citation3] In terms of traditional medicinal uses, they have been used for the treatment of enlarged liver, spleen, stomach ulcer, diabetes, cough, hepatic disorders, chest pain, skin diseases, boils, blood purifier, and rheumatism.[Citation4–Citation7] Moreover, according to Larsen and co-workers,[Citation8] various parts of these plant species are reportedly eaten either raw or cooked as vegetables in many Asian countries. They are also considered as nutritionally rich food products since the plants are a rich source of starch, carbohydrates, proteins, fats, vitamins, and minerals.[Citation9–Citation13] Several reports concerning the phytoconstituents, essential oils, and pharmacological actions have been published earlier.[Citation14–Citation19] As a result, plants belonging to the genus Curcuma are gaining importance all over the world and are being the subject for many investigation and exploration in recent years. The plants have been shown to contain bioactive molecules that possess pharmacological properties like anti-inflammatory, antimicrobial, hypocholestraemic, antirheumatic, antiviral, antifibrotic, antivenomous, antihepatotoxic, antidiabetic, antinociceptive, anticancerous, and gastroprotective properties.[Citation14,Citation20–Citation22]
Although many studies have described the phytochemistry and pharmacology of different Curcuma species, there is limited literature available for studies related to food value, nutritional composition, and health benefits of the edible Curcuma species. Accordingly, our review comprehensively documents the nutritional value, phytoconstituent profile, and culinary purposes along with ethno medicinal as well as pharmacological properties of 16 edible Curcuma species, as gathered from previously published literature. As these plants have important nutraceutical and therapeutic potentials, the extraction and characterization of important bioactive compounds with vital medicinal properties may provide opportunities related to food and pharmaceutical applications. The 16 edible Curcuma species are discussed and reviewed.
Curcuma aeruginosa
Curcuma aeruginosa Roxb., commonly known as pink and blue ginger, is a perennial tropical plant with unbranched leafy stems up to 200 cm tall and mildly aromatic greenish blue rhizome.[Citation23,Citation24] The plant is a native of Myanmar, although it is also found in West Bengal, Bihar, Coromandel coast, South Karnataka, and Kerala.[Citation25] Further, according to Achut and Bandyopadhyaya,[Citation26] the natural population has come down and is listed in the critically endangered category of the International Union for Conservation of Nature report due to its high medicinal value and indiscriminate harvest from the wild.
Curcuma amada
Curcuma amada Roxb., popularly known as mango ginger, are perennials growing up to about 80 cm in height and are morphologically similar to Zingiber officinale and Curcuma longa but lacks pungency and has a raw mango flavor due to the presence of car-3-ene and cis-ocimene.[Citation27–Citation29] The plant species is endemic to South Asia and commonly distributed in many parts of northeast India and in the hills of south India.[Citation29]
Curcuma angustifolia
Curcuma angustifolia Roxb., also known as East Indian arrowroot, is characterized by the presence of narrow, green, glabrous leaves with small inflorescences bearing yellow flowers with pink coma bracts.[Citation29] Flowers usually appear near to the ground in the beginning of the rainy season before the leaves are fully developed and the leaves later reach up to about 1.5 m. It is endemic to northwestern, central, and south India, where the plants are utilized for its medicinal purposes by local herbalists.[Citation30]
Curcuma aromatica
Curcuma aromatica Salisb, also known as aromatic turmeric, wild turmeric, or yellow zedoary, is the most widely used Curcuma species next to the common turmeric (Curcuma longa Linn.).[Citation31] Fresh rhizomes of the plants are yellowish with camphoraceous smell and produce clumps of about 1 m tall erect and unbranched leaf stems. The inflorescence appears in early spring and flowers are pinkish white in color with an orange lip.[Citation29,Citation32] The plant species is distributed in India, China, and Sri Lanka.[Citation32]
Curcuma australasica
Curcuma australasica J. D. Hook, commonly known as Cape York lily, is an endemic species and the only native representative of the genus from Australia, as reported by Sharma.[Citation29] The plant species is usually distributed in shady rainforest margins of the Cape York Peninsula in northern Queensland, along the coast of the Gulf of Carpentaria and New Guinea.[Citation33]
Curcuma caesia
Curcuma caesia Roxb., also known as black zedoary or black turmeric, is a species of Curcuma characterized by deep bluish black or grayish black-colored rhizome having pungent smell and hot bitter taste and leaves with a deep red-violet patch, which runs throughout the whole lamina. The plant species is a native of northeast India but is also found in Java and Myanmar.[Citation32]
Curcuma caulina
Curcuma caulina J. Graham. [syn. Hitchenia caulina (J. Graham) Baker], commonly known as Indian arrowroot or arrowroot lily, is a herbaceous perennial plant producing erect, unbranched, leafy stems up to 120 cm tall from an underground rhizome bearing inflorescence with prominent greenish white or pinkish white-colored bracts and yellow or white-colored flowers.[Citation29] The plant is reported to be a native of India that grows in wild mainly in the Mahabaleshwar plateau and neighboring forest areas with high annual rainfall.[Citation34]
Curcuma leucorrhiza
Curcuma leucorrhiza is grown widely in Manipur, India, for its rhizomes, which are a source of an edible starch known as East Indian arrowroot.[Citation35,Citation36] Grieve[Citation37] described the plant species to be a stemless perennial plant growing up to 60 cm tall.
Curcuma longa
Curcuma longa Linn. (syn. Curcuma domestica Val.) is commonly known as “turmeric root” and is reported to be cultivated in India and throughout the tropics.[Citation32] It is a rhizomatous herbaceous perennial plant that reaches up to 1 m in height and bear cylindrical, aromatic, and yellow to orange-colored rhizomes. The plants also have characteristic white to green and sometimes tinged reddish-purple stem bracts with tapered upper ends at the top of the inflorescence.[Citation38]
Curcuma mangga
Curcuma mangga Val. & Zijp. is commonly known as “mango turmeric” and characterized by the mango-like smell of rhizome as in C. amada.[Citation29] The species was described by Perry[Citation39] to be a herbaceous, perennial plant producing clumps of about 30–110 cm tall erect pseudostems from a branched underground rhizome. Although the plant species was first described from Java, it grows commonly in Thailand also.[Citation40]
Curcuma phaeocaulis
Curcuma phaeocaulis Valeton, commonly known as rhizoma curcumae, is widely distributed in southern regions of the People’s Republic of China including Sichuan, Yunnan, Guangdong, and Fujian Provinces.[Citation29] The plant grows up to 1 m tall; rhizomes are pale blue, green, yellowish green or yellow; roots are tuberous at tip and inflorescences are borne on separate shoots arising from rhizomes. Sirirugsa et al.[Citation41] reported that this plant was earlier misidentified as Curcuma zedoaria, C. caesia, or C. aeruginosa in China.
Curcuma pierreana
Curcuma pierreana Gagnep, commonly known as false arrowroot, is a herbaceous perennial plant producing clumps of leafy stems about 60 cm tall from a rhizomatous rootstock.[Citation36] Plants belonging to this species are distinguished by the presence of sessile inflorescence and white staminodes with large purple blotched apices. It has its origin in Cambodia and Thailand.[Citation42]
Curcuma pseudomontana
Curcuma pseudomontana J. Graham., also known as hill turmeric, is endemic to the Western and Eastern Ghats of peninsular India and is grown as a potential ornamental species in Karnataka, Maharashtra, and Andhra Pradesh.[Citation43] It is characterized by its beautiful well-developed coma, deep yellow flowers, broadly ovate and prominently sulcate leaves with bright green color. This plant grows abundantly on rocky, shrubby slopes, and flowers richly from June to October.[Citation29]
Curcuma purpurascens
Curcuma purpurascens Blume is one of the lesser known species of Curcuma, which is considered of minor importance and limited phytochemical and biological investigations have been done on this plant. It is a perennial herb with up to 1 m tall pseudostems arising from a branched rhizome and each pseudostem is comprised of several leaves having 55–70-cm-long and 19–23-cm-wide leaf blades.[Citation44]
Curcuma zanthorrhiza
Curcuma zanthorrhiza, characterized by its deeply colored rhizome as turmeric, is native to Indonesia and was used as a dye earlier but now; it is often used as a substitute for C. aromatica in cosmetics.[Citation28,Citation29,Citation40] The plant bears a cluster of erect pseudostems up to 2 m tall from an underground rhizome and each pseudostem is made up of about eight leaves with blades that can be 40–90 cm long and 15–21 cm wide.[Citation45]
Curcuma zedoaria
C. zedoaria Rosc., also known as white turmeric or zedoary, is indigenous to Bangladesh, Sri Lanka, and India.[Citation46,Citation47] The plant is a rather pretty fragrant species about 1 m in height and flowers in the beginning of the rainy season when the leaves start to develop. The plant bears yellow flowers with red and green bracts and rhizomes are pale sulfur yellow to bright yellow inside and taste strong and bitter.[Citation29]
Food and nutritional value of edible Curcuma species
There is an increasing interest in the study of medicinal plants to validate their consumption as an alternative food. Among spices, turmeric and ginger have been extensively studied and more number of edible Curcuma species is yet to be explored. Mango ginger and other edible species of Curcuma are also such unique spices that remains untapped. Hence, detailed information on the nutritional composition of the 16 edible Curcuma species and their role in culinary purposes as well as their applications in food are reviewed here. In all the 16 mentioned Curcuma species, rhizomes were found to be the major edible portion of the plants. Rhizomes of C. angustifolia, C. caulina, C. leucorrhiza, and Curcuma xanthorrhiza are a good source of starch and thus used as nutritional food supplement and substitute for true arrowroot powder.[Citation28,Citation35,Citation48–Citation53] Rhizomes of C. aeruginosa, C. amada, C. aromatica, C. longa, C. pierreana, C. pseudomontana, purpurascens, C. xanthorrhiza, and C. zedoaria are also employed as dye, spice, and food flavoring and coloring agent in food preparations mainly due to their exotic aroma.[Citation10,Citation11,Citation28,Citation53–Citation59] Apart from rhizomes, other parts such as inflorescence, tuberous roots, and rootstocks of C. angustifolia, C. australasica, C. caulina, C. pierreana, and C. amada have been reported to be a rich source of proteins and carbohydrates and are used in culinary preparations as vegetables and food appetizers.[Citation32–Citation36,Citation55,Citation60–Citation63] The fresh tips of young rhizomes and shoots of another species, C. manga, are used in making pickles and its aromatic leaves are used for flavoring steamed and baked fish.[Citation64] In addition, the rhizomes of C. pseudomontana are crushed, boiled, and eaten in India (Deccan), whereas the rhizomes of C. xanthorrhiza are either eaten raw or used as spice.[Citation34,Citation45–Citation47]
All these edible species of Curcuma are a good source of carbohydrates, proteins, and dietary fiber along with vitamins and minerals. Studies on the nutritional values of species such as C. longa, C. amada, C. leucorrhiza, C. phaeocaulis, and C. pseudomontana have shown the plant species to be nutritionally rich containing sugars, fibers, essential oils, starch, proteins, amino acids, minerals like iron, zinc, copper, molybdenum, calcium, chromium, manganese, magnesium, phosphorous, nitrogen, potassium, sodium, and sulfur as well as vitamins like thiamine, riboflavin, vitamin A, niacin, pyridoxine, vitamin C, and vitamin E.[Citation12,Citation32,Citation54,Citation55,Citation65–Citation70] Due to the presence of minerals such as calcium, magnesium, iron, potassium, sodium, copper, manganese, and zinc, the rhizomes of C. phaeocaulis are also used in Chinese Pharmacopoeia as health food, in addition to being used as food supplement.[Citation69,Citation70]
Phytochemistry and pharmacology of edible Curcuma species
There are many published reports related to the phytoconstituents, essential oils, and pharmacological actions of the 16 reported edible species of Curcuma. The constituent bioactive compounds present in the edible Curcuma species are shown in , except for C. caulina, for which no reported data was available. and represent the essential oil composition of these edible plant species and their varied pharmacological properties, respectively.
Table 1. Phytoconstituents profile of edible Curcuma species.
Table 2. Essential oil composition of edible Curcuma species.
Table 3. Pharmacological properties of edible Curcuma species.
The various pharmacological activities possessed by these species may be attributed to the presence of diverse bioactive compounds. Rhizomes of C. angustifolia have been found to contain secondary metabolites such as alkaloids, flavonoids, terpenoids, phenols, tannins, saponins, curcumin, steroids, glycosides, and oils.[Citation51,Citation71] Similarly, Devi et al.[Citation51] have reported the presence of phytoconstituents like phenols, flavonoids, alkaloids, terpenoids, tannins, saponins, steroids, glycosides, oils, and carabrane-type compounds in the rhizomes of C. caesia. Phytochemical analysis of the rhizomes of C. leucorrhiza also revealed the presence of alkaloids, tannins, steroids, anthocyanins, terpenoids, triterpenoids, flavonoids, phenols, phlobatannins, and guaianolide sesquiterpene lactone.[Citation66,Citation72,Citation73] Many steroids, tannins, alkaloids, and flavonoid compounds have also been reported from the rhizomes of C. pseudomontana and bioactive sesquiterpenes compounds such as germacrone, zederone, dehydrocurdione, curcumenol, zedoarondiol, and isocurcumenol along with β-pinene or other sesquiterpene lactones have been shown to be responsible for the antiandrogenic effect and uterine relaxant property of C. aeruginosa.[Citation13,Citation68,Citation74]
According to Mujumdar et al.,[Citation75] the ethyl alcohol extracts of C. amada rhizomes contain compounds with hydroxyl, ester, carbonyl, and olefin functional groups, which contributed to the anti-inflammatory activity of the extracts in acute and chronic administration in albino rats. Further pharmacological researches in the plant has also reported the presence of other compounds like ar-turmerone, difurocumenonol, and amadannulen to be responsible for the antiplatelet property, antioxidant and antimicrobial activities.[Citation76–Citation78] Volatile oil constituents of the plant such as α- and ß-pinene confer turpentine-like odor to the plant while myrcene and ß- pinene have also been indicated to contribute to the antifungal and insecticidal activities of the plant.[Citation79,Citation80]
Rhizome extracts of C. phaeocaulis have been reported to exhibit inhibitory effects on nitric oxide production and phytochemical analysis of the rhizome extracts revealed the presence of guaiane-type sesquiterpenes, germacrane-type sesquiterpenoid, salvialane-type sesquiterpene, γ-elemene-type sesquiterpenes, eudesmane-type sesquiterpene, cyclic diarylheptanoid, and cadinane-type sesquiterpenes.[Citation18,Citation81–Citation84] Likewise, germacron has been identified as the main constituent present in the rhizome extracts of C. pierreana that showed inhibitory effect on the growth of microorganisms including Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus, Staphylococcus faecalis, and the fungus Candida albicans.[Citation85] Germacrone has also been identified as the active principle responsible for the anti-inflammatory and analgesic activities of C. xanthorrhiza by Ozaki.[Citation86] C. xanthorrhiza has also been shown to contain xanthorrhizol, a natural sesquiterpenoid, which possess antimetastatic effect and antimicrobial activities, as well as other curcumin analogues including 1-(4-hydroxyl-3,5-dimethoxyphenyl)-7-(4-hydroxy-3-methoxyphenyl)-(1E, 6E)-1 and 6-heptadiene-3,4-dione responsible for the potent antioxidant activity of the plant extracts against auto-oxidation of linoleic acid.[Citation87–Citation89]
Bioavailability and bioaccessibility of edible Curcuma species
Nutraceuticals can be incorporated into food systems for the development of functional foods. However, the effectiveness of a functional food depends on the solubility, stability, and bioavailability of the bioactive compounds. Curcumin and two other major curcuminoid compounds, demethoxycurcumin and bisdemethoxycurcumin, are one of the well-studied nutraceuticals with similar bioactivities and many health-promoting benefits.[Citation90–Citation92] However, evidence from numerous literatures has revealed that the bioavailability of curcuminoids is low, mainly due to their insolubility in water (~11 ng/ml) and rapid metabolism limiting not only its solubility/dispersion in food matrices, but also its bioavailability.[Citation93,Citation94] Therefore, continuous research on curcumin has led to the development of technologies like forming emulsions or gels to enhance curcuminoid solubility in water. Recently, an organogel system for high-loading (>1%) delivery of curcumin with high bioaccessibility (80%) has been developed.[Citation94] In addition, several attempts have been made to encapsulate curcumin by chemical/physicochemical and physical–mechanical methods including nanoparticles, liposomes, micelles, and phospholipid complexes to enhance its bioavailability and bioaccessibility.[Citation95–Citation102]
Cytotoxicity and health benefits of edible Curcuma species
During the last two decades, modern medicine and pharmacological industries have turned towards Curcuma with the hope of finding remedies for serious diseases as well as natural remedies for common maladies. Therefore, several studies have been conducted to explore the chemical contents, structure, and composition of curcuminoids and essential oils of these species and many of these studies reported important medicinal properties and health benefits of the edible Curcuma species. The detailed ethnomedicinal uses and pharmacological properties of each individual Curcuma species are presented in and , respectively. Several species of the genus Curcuma have been employed in Ayurveda and traditional folk medicine for treatment of various diseases and disorders. Rhizomes and other plant parts of C. aeruginosa, C. angustifolia, C. caesia, C. leucorrhiza, C. longa, C. mangga, C. phaeocaulis, and C. purpurascens have been reportedly used for treatment of dysentery, stomach ulcer, indigestion, gastrointestinal disorders, enlarged liver spleen, diabetes, fever, cough, boils, scabies, chest pain, tonic for sprains, bruises, body pain, hepatic disorders, anorexia, coryza, dyspepsia, rheumatism, sinusitis, antiseptic, bleeding, wound healing, and inflamed mucous membranes.[Citation4,Citation6,Citation19,Citation45,Citation58,Citation59,Citation103–Citation110] Additionally, C. amada have been reported to be used as an appetizer, alexteric, antipyretic, aphrodisiac, laxative, for mood disorders, biliousness, and bronchitis.[Citation111] The rhizomes and roots of C. zedoaria are also being utilized as a rubefacient, carminative, expectorant, demulcent, diuretic, and stimulant, while C. caesia also is used as a remedy for tonsillitis, leukoderma, piles, jaundice, as well as decoction in asthma and epilepsy.[Citation32,Citation112] Other species of Curcuma including C. aromatica, C. australasica, and C. pseudomontana are also used medicinally for the treatment of snakebites, contraceptive purposes, and as blood purifier.[Citation5,Citation33,Citation39,Citation63,Citation105,Citation113,Citation114]
Table 4. Ethnobotanical uses of edible Curcuma species.
A few studies have also been conducted to assess the cytotoxicity of the Curcuma species. Rhizomes of C. australasica have been shown to possess potent antitumor activity, which may be due to its direct cytotoxic effect or antioxidant properties.[Citation115,Citation116] Similarly, hydrodistilled rhizome oils of C. purpurascens and C. pseudomontana have been shown to possess cytotoxic activity against human ductal breast carcinoma cell line.[Citation117–Citation119] Several bioactive labdane diterpenoids isolated from C. mangga have also been shown to possess cytotoxic activity against human cancer cell lines, namely nasopharyngeal epidermoid cell line (KB), hormone-dependent breast cell line (MCF-7), colon cell lines (HCT 116 and HT-29), lung cell line (A549), and cervical cell line (Ca Ski).[Citation120,Citation121]
Molecular cloning of genes isolated from edible Curcuma species
Few studies related to molecular cloning of genes involved in plant defense mechanism have been identified and isolated from Curcuma species and majority of the reports are for the common turmeric, C. longa. Chan et al.[Citation122] performed the molecular cloning and characterization of a novel phytocystatin gene, a type of protease inhibitor gene involved in antipathogenic reaction, and stress tolerance isolated from C. longa. Identification and expression profiling has also been performed for another novel Kunitz trypsin inhibitor gene from C. longa by real-time quantitative polymerase chain reaction.[Citation123] Further, in a transcriptome deep sequencing study in C. longa by Santhi et al.,[Citation124] 27 conserved and 40 non-conserved miRNA families were identified by high-throughput Illumina sequencing and downstream in silico analysis. In addition, 97 novel candidate miRNAs specific to turmeric were also successfully identified. The selected and validated miRNAs were found to be involved in plant growth and development, stress response, and metabolism. Recently, Wu et al.[Citation125] reported the synthesis of the major bioactive component of oil products in C. zedoaria, germacrone, along with its derivatives. Molecular docking experiments and molecular dynamic simulations were also applied for further evaluation of the binding stabilities between the compounds and their receptors. All these reports may serve as the foundation for more future work on miRNA-based gene regulation and studies related to gene expression and molecular transformation of bioactive compounds of these edible Curcuma plant species.
Applications of edible Curcuma species
Among the edible species of Curcuma, C. longa is the most common one and also finds applications in food and cosmetic industries. Clinical trials and toxicology studies by Anand et al.[Citation93] have concluded curcumin, the active principle in C. longa, to be safe and well tolerated even at very high doses (12 g/day) in humans and the joint Food and Agriculture Organization/World Health Organization report on food additives has recommended that a maximum daily intake of curcumin is 0–1 mg/kg body weight with no adverse effects. A new method for making safe, nontoxic extracts of C. longa and its incorporation in sunscreen composition has also been developed and patented. The process involved the use of microemulsion and nanoemulsion techniques to enhance the bioavailability and stability in sunscreens that meets updated Food and Drug administration recommendations without any necessity of addition of titanium dioxide.[Citation126,Citation127] Apart from the usage of C. longa in cosmetics and food industry, the other edible species of Curcuma find application as ornamental plants due to their exotic fragrance and are also used as functional foods with high nutritive value.
Conclusions and future perspectives
All the 16 edible Curcuma species mentioned in this review are important because they possess culinary as well as medicinal properties, and thus have great potential for use as functional foods and medicines. Studies related to consumption safety, clinical trials, in vivo investigations, and cytotoxic studies will be useful as information related to this area is limited. Additionally, further research on nutritional values along with pharmacological studies of new uninvestigated compounds is desirable and will provide immense opportunities for the development of new plant-based food and pharmaceutical products.
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