doi 10.1515/jcim-2013-0046

J Complement Integr Med. 2014; 11(2): 55–62

Review Nusrat Fatimaa, Mohammad Mijanur Rahmana, Md. Asaduzzaman Khan* and Junjiang Fu

A review on Ipomoea carnea: pharmacology, toxicology and phytochemistry Abstract: Phytomedicines are increasingly being established in modern medical science. The shrub Ipomoea carnea has been used traditionally for thousands of years. However, there are few scientific studies on this medicinal plant, and most of the information are scattered. In this review, we have summarized the existing knowledge and recent progress on the medicinal importance of I. carnea. Different extracts of I. carnea plant possess anti-bacterial, anti-fungal, anti-oxidant, anti-cancer, anti-convulsant, immunomodulatory, anti-diabetic, hepatoprotective, anti-inflammatory, anxiolytic, sedative and wound healing activities. However, some toxicological effects have been also reported. Some of the major phytochemicals associated with the bioactivity of I. carnea have been characterized, which have been discussed in this study too. This review article might be beneficial for phytotherapy research, as I. carnea can be a good source for drug development. Keywords: calystegines, Ipomoea carnea, medicinal value, phytomedicine, swainsonine, toxicity

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Nusrat Fatima and Mohammad Mijanur Rahman have equally contributed to this work. *Corresponding author: Md. Asaduzzaman Khan, Department of Biochemistry and Molecular Biology, Jahangirnagar University, Savar, Dhaka 1342, Bangladesh; Research Center for Preclinical Medicine, Luzhou Medical College, 3–319 Zhongshan Road, Luzhou, Sichuan 646000, P.R. China, E-mail: [email protected] Junjiang Fu, Research Center for Preclinical Medicine, Luzhou Medical College, 3–319 Zhongshan Road, Luzhou, Sichuan 646000, P.R. China Nusrat Fatima, Mohammad Mijanur Rahman, Department of Biochemistry and Molecular Biology, Jahangirnagar University, Savar, Dhaka 1342, Bangladesh

Introduction Plants are the natural friends of human being, which provide food, cloth, house and medicine from the

prehistoric time. Being a self-dependent creature, plants synthesize a wide variety of chemical compounds, generally known as phytochemicals. A panel of phytochemicals are not necessary for the basic metabolic function, and they are known as secondary metabolites that usually exert differential biological function like defense (against herbivores, microbes, viruses or competing plants) and signal compounds (to attract pollinating or seed dispersing animals). Some of these compounds mimic the endogenous metabolites of human cells, including ligands, hormones or other molecules involved in inter- and intra-cellular signal transduction to exert their biological effects [1]. Others perform the similar function of human metabolites, probably because of similar molecular target. Such as brassinolides are plant steroid hormones, which regulate cell division and cell development in the plant, and are structurally similar to human growth-regulating steroids [2]. Tracing the history of medical knowledge claims that plants are the root of medicine. Archaeological, anthropological and historical evidences support the use of medicinal plants by thousands of years ago [3]. A historical dissection of medicinal source showed that many of the drugs were originally from the plants or herbs, for example, salicin from Salix alba, emetine from Cephaelis ipecacuanha, strychnine and brucine from Strychnos nux-vomica, quinine from Cinchona ledgeriana, colchicine from Colchicum autumale, caffeine from Coffea arabica, nicotine from Nicotiana tabacum, atropine from Atropa belladonna and cocaine from Erythroxylum coca [4]. These drugs are still used now-a-days. Actually, about 60% of the drugs that are now available, including household names such as artemisinin, camptothecin, lovastatin, maytansine, paclitaxel, penicillin, reserpine and silibinin, were either directly or indirectly derived from natural products [5]. Although the usage of natural substances as therapeutic agents has been declined from the beginning of last century, search for bioactive compounds from nature (plants, animals and microflora) continues to play an important role in fashioning new medicinal agents [6].

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The trends to revert to the plant-derived medicine are being soughed recently due to the cost, safety issue of conventional drugs. According to the report from World Health Organization, herbal medicine is the most lucrative among the traditional medicines, and 70–80% of the world’s population relies on traditional herbal medicine for their primary health care [7]. Out of vast numbers of plant species, only about 6% have been screened for biological activity, and 15% have been evaluated phytochemically [8]. Ethnopharmacological study of these vast numbers of plants is considered as a highly diversified and promising approach in drug discovery.

Ipomoea carnea: basic features and traditional usage The shrub Ipomoea carnea (I. carnea) is up to 2.5 m tall, of which, branches are ascending, usually fistular, and contain milky juice. The stem of I. carnea is erect, woody, hairy, more or less cylindrical in shape and greenish in color, monopodially branched, and bears alternate leaves. The

seed is three sided, with two flat ventral surfaces that may have a central depression and one convex dorsal surface [9, 10]. I. carnea belongs to the class of Magnoliphyta and family Convolvulaceae [11]. I. carnea is highly distributed throughout American tropics, ranging from Argentina to the southern parts of USA [12, 13]. This plant species has also been reported from South Asia, including Bangladesh, India, Pakistan and Sri Lanka, and several African countries like Egypt, Kenya and coast of tropical East Africa [10, 14]. It is quite a common flower in the rural areas of Bangladesh and India as well as the roadside. In some parts of China, Hainan, Guangxi, as well as Taiwan, I. carnea sub-species I. fistulosa is cultivated [15]. Ecological amplitude for I. carnea is much wide, and they are observed to growing in xeric and hydric conditions [14]. I. carnea commonly grows in dense populations along river beds, drain banks, road sides, field edges, banks, canals and other waterlogged areas. I. carnea is a flowering plant and is cultivated in the garden as ornamental plant. It is also cultivated as hedge plant in the crop fields, fence and fire wood (dry) due to its rapid propagating behavior, wide ecological amplitude and extraordinary competitive abilities [10]. A photograph of I. carnea is presented in Figure 1. Before the recent flourish of

Figure 1 Photograph of flowering plant Ipomoea carnea.

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Fatima et al.: Ipomoea carnea: pharmacology, toxicology and phytochemistry

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Figure 2 Major bioactive constituents of Ipomoea carnea. (A) Swainsonine, (B) calystegine a3, (C) calystegine b1, (D) calystegine b2, (E) calystegine b3 and (F) calystegine c1. Source: Pubchem: www.pubchem.ncbi.nlm.nih.gov

pharmacological properties, I. carnea was used as a medicinal plant by several communities within the framework of folk medicine, mostly in Indian sub-continent. The milky juice of this plant is used for the treatment of leukoderma and other related skin diseases, as well as topical anti-septic in lesions [16, 17], and the boiled roots are used as laxative and menstruation provocation [18]. In central Himalaya, I. carnea is used for rheumatism and gout treatment [19]. Among other traditional uses of this plant, treatments for venereal diseases, dysentery, hypertension and immunodeficiency are notable [20]. This review summarizes the medicinal importance of I. carnea with possible mechanism of actions, which have been evaluated by scientific studies. Also the adverse effects of this plant and its chemical properties have been explored. This may be beneficial for the pharmacological establishment of I. carnea from traditional use to modern health science.

Medicinal/pharmacological action of Ipomoea carnea Over the last few decades, a number of researches demonstrated several pharmacological effects of I. carnea, including anti-bacterial, anti-fungal, anti-oxidant, anti-cancer, anti-convulsant, immunomodulatory, antidiabetic, hepatoprotective, anti-inflammatory, anxiolytic, sedative and wound healing activities.

Anti-microbial activity Anti-bacterial activity of I. carnea has been reported in different studies. Adsul et al. [21] reported that the acetone extract of I. carnea is effective against Ptroteus vulgaris and Salmonella typhimurium bacteria, while the ethanol extract was found effective against Pseudomonas aeruginosa. A secondary metabolite from I. carnea, dibutyl phthalate was found to have anti-bacterial activity against some gram negative bacteria, like Klebseilla pneumonia, Proteus mirabilis and P. aeruginosa [22]. A number of resin glycosides of I. carnea have been found to potentiate effect of anti-biotics, like tetracycline, kanamycin and chloramphenicol, which are clinically useful against bacteria [23]. It is suspected that these resin glycosides might have synergistic effect on its anti-bacterial phytoconstituent. The tropical use of I. carnea in skin disease has been practiced in traditional medicine for a long time, but with a very few scientific study. Mogle [24] showed the antifungal activity of aqueous leaf extracts of I. carnea against seven fungi namely Aspergillus niger, Penicillium digitatum, Botrytis cinera, Rhizopus arrhizus, Aspergillus flavus, Chaetomium brasiliense and Rhizoctonia solani. Among these, against A. niger, the extract showed most potential effect [24]. The major anti-fungal fraction of I. carnea leaves was reported to contain two cumarate isomers: (E)-octadecyl p-coumarate and (Z)-octadecyl p-coumarate [25].

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Anti-oxidant activity

compared with the control in pentylenetetrazole and MES-induced seizures [30].

Anti-oxidants are a group of molecules that can prevent the oxidation of other molecules by quenching reactive free radicals and, therefore, may have health beneficial effects in the prevention of degenerative diseases. Khatiwora et al. [26] reported the substantial presence of antioxidants like, polyphenols and flavonoids, in leaves, stem and flowers of I. carnea. The polyphenol and flavonoid contents of I. carnea were found to have a strong DPPH radical scavenging activity (a reliable assay for anti-oxidant capacity measurement) [27]. Specifically, the flower part of this plant is more abundant in anti-oxidant phytoconstituents.

Immunomodulatory effect Immunomodulatory effect of I. carnea has first come into focus by the study of Hueza et al. only 10 years ago [31]. They reported that a low dosage of I carnea aqueous fraction induced phagocytosis and hydrogen peroxide production by macrophages. The I. carnea alkaloid swainsonine has immunomodulatory effects too [32]. Swainsonine usually works by inhibiting the metabolism of glycoprotein. Swainsonine modulates the immune function in adult rats if they were exposed at their juvenile stage, during lactation [32].

Anti-cancer activity The study of Sharma et al. [28] suggested the cytotoxic effect of hexane, chloroform and ethyl acetate fraction of I. carnea with a LC50 value of 141.4 μg/mL, 211.28 μg/mL and 307.28 μg/mL, respectively. Swainsonine, a natural alkaloid isolated from I. carnea, has been reported to exhibit anti-cancer activity on several mouse models of cancer and human carcinoma. Swainsonine inhibits the cell growth through the induction of apoptosis in human lung cancer cell line A549 [29]. Upregulation of Bax, downregulation of Bcl-2, promotion of Bax translocation to mitochondria, mitochondria-mediated apoptotic pathway as well as cytochrome C release and the activation of caspase-9 and caspase-3 have been found as the factors behind apoptosis induction in A549 cells by I. carnea alkaloid swainsonine [29].

Anti-diabetic effect The anti-hyperglycemic effect of aqueous extract of I. carnea leaves in streptozotocin-induced diabetes in rats was studied by Khalid et al. [33]. A significant effect was observed by the extracts at 500 mg/kg dosage that was comparable to Glibenclamide (10 mg/kg). The phytoconstituents probably explains such anti-diabetic or hypoglycemic effect. The polyhydroxylated nortropane alkaloids calystegines are found in I. carnea and other Convolvulaceae plants [34]. Calystegines B1 and C1 are potent competitive inhibitors of bovine, human and rat βglucosidase activities. Calystegine B2 is a strong competitive inhibitor of the α-galactosidase activity in the livers of bovine, human and rat, while calystegines A3 and B2 are selective inhibitors of rat liver β-glucosidase [34].

Hepatoprotective activity

Anti-convulsant activity The anti-convulsant activity of both polar and nonpolar extract was evaluated in mice and rats using the pentylenetetrazole and maximal electroshock (MES)-induced seizure models by Rout et al. [30]. The result of MESinduced convulsion showed that the polar extract significantly reduced extensor phase and stupor phase at a dose ranging from 200 mg/kg to 400 mg/kg. Indeed, the anti-convulsant activity was comparable to that of standard drug, Phenytoin. The polar extract also delayed the onset of time and increased the duration of pentylenetetrazole-induced convulsion. Thus extracts caused a significant dose-dependent increase in onset of convulsion

In carbon tetrachloride treated hepatotoxic rat model, aqueous extract of I. carnea leaves were found to restore the hepatic structural and functionality indicating markers (activity and/or expression) in a dosedependent manner [35]. Hepatoprotective effect is partially attributed due to anti-oxidant effect of I. carnea. It was reported that the aqueous extract of leaves reduces the lipid peroxidation in the liver tissue and restores activities of anti-oxidant enzymes, like superoxide dismutase and catalase toward normal levels [35]. Histological features also indicated the improvement of the hepatocellular necrosis and reduction of inflammatory cells infiltration [35].

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Anti-inflammatory effect

Wound healing activity

The anti-inflammatory activity of methanolic and petroleum ether extracts of I. fistulosa, a sub-species of I. carnea, leaves was reported by Ruchi et al. [36] in formalin (0.1%)-induced rat paw edema model. A timedependent evaluation of anti-inflammatory activity suggested that the extract shows anti-inflammatory activity at various acute phases of inflammation. This antiinflammatory property might be attributed by the β-sitosterol content of I. fistulosa, or I. carnea [36]. Anti-inflammatory activity of aqueous extracts of I. carnea leaves was evaluated in carrageenan (0.1%)-induced rat paw edema model [37]. The result of this study is similar to the above-mentioned study [36], but more prominently the anti-inflammatory effect is evolved in early phase of inflammation [37].

The study in incision and excision wound model revealed significant wound healing activity of flavonoids (Kaempferol and Kaempferol-3-O-â-D-glucoside) isolated from I. carnea flowers [44]. The macroscopic, biochemical and histological features suggest the healing effect of these two flavonoids with prominent effect on both inflammatory and proliferative phase of wound healing [45]. In another study, histological features of healing represented the improvement of inflammatory phase, which includes fewer macrophages that are the predominating inflammatory cell type cells at the wound site [46]. Interestingly, a combination of macroscopic features and biochemical features, including increase of granulation tissue and hydroxyproline content, respectively, confirmed the improvement of the proliferative phase of wound healing [47]. The extent of the biochemical, histological and macroscopic features varies depending on the flavonoid types and wound types.

Anxiolytic activity I. carnea appears to fall under the sedative–hypnotic category of central depressants. The anxiolytic effect of the aqueous and methanolic extract of I. carnea leaves was evaluated in mice using several behavioral paradigm like elevated plus maze, open field test and hole-board test model [38]. The elevated plus maze is a widely used behavioral paradigm for animal model of anxiety on pharmacological, physiological and behavioral grounds [39]. Both of open field test and hole-board test reflect the explorative behavior and usually reflect emotionality and/or anxiety responses to stress [40, 41]. All of these behavioral paradigms confirm the anxiolytic activity of aqueous and methanolic extract of I. carnea leaves [38]. Several nortropane alkaloids like calystegines B1, B2, C3 and the indolizidine alkaloid swainsonine are supposed to be responsible for the anxiolytic activity of I. carnea [42, 43].

Sedative activity The sedative effect of the petroleum ether, alcohol and aqueous extracts of I. carnea leaf was evaluated in mice and rats using phenobarbitone-induced sleeping time and head dip test [30]. Study reported that the duration of sleeping time in phenobarbitone-induced experimental models was increased in a dose-dependent manner with a significant decrease in locomotor activity at high dose, and in case of head dip test, exploratory behavioral potential was found to be decreased due to high dose of alcoholic and aqueous extract [30].

Adverse effects of Ipomoea carnea General toxicity A number of studies reported the toxicological effects of I. carnea, mainly in goats and sheeps. Chronic ingestion of I. carnea has been reported to cause general weakness, loss of body weight, loss of hair, locomotor disturbance, loss of reflexes, intero-hepato-nephropathy, muscle tremors, ataxia, posterior paresis, paralysis and even death [42, 48, 49]. In Wister rats, some of the biochemical changes, like leukocytosis, anemia, an increase in serum aspartate Amino Transferase activity and decrease of albumin level have been noticed after I. carnea treatment [50]. The dihydroxynortropane alkaloids are thought to be responsible for these toxic effects of I. carnea [51]. Also, it is suspected that the calystegines might act as coadjuvants of swainsonine in I. carnea toxicosis [52].

Induction of lysosomal storage disease Lysosomal storage disease is a group of rare inherited metabolic disorders that result from lysosomal dysfunction [53]. Most of lysosomal storage diseases are genetic disorders, but a few are induced by environmental factors, for example, the ingestion of toxic plants like locoweeds (Astragalus and Oxytropis spp.) [54]. It has been

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reported that I. carnea induce lysosomal storage disease in goats [42]. Affected animals were found ataxic with head tremors and nystagmus. The glycosidase inhibitor phytoconstituents of I. carnea, including swainsonine and calystegines, are thought to be responsible for the lysosomal storage disease.

Teratological effects The effects of prenatal administration of I. carnea on pregnant rats and their offspring were evaluated by the oral administration of the plant extract from day 6 to day 20 of gestation [55]. The result of that study found the organ-specific I. carnea toxicosis in thyroid, pancreas, liver and kidneys of offspring, characterized by cytoplasmic vacuolization. I. carnea administration also caused reducing of body weight, thymus atrophy and spleen enlargement in pups [55]. It has been shown that feeding of the aqueous extract of I. carnea to the offspring did not cause severe development alterations that produce behavioral change [56]. But in another study, Schwarz et al. [57] showed that feeding of I. carnea aqueous extract results in a significant decline of 3,4-dihydroxyphenylacetic acid and increase in vanilmandelic acid levels in striatum, cortex and hypothalamus in a diffusive manner. This indicated the decreased dopamine and enhanced norepinephrine activity in pups [57].

Phytochemical properties of Ipomoea carnea The phytochemicals are the underneath component responsible for the pharmacological and medicinal properties of a plant material. A long history of traditional medicinal usage indicated the presence of bioactive phytochemicals, but those were mostly unknown. Legler [58] reported the presence of L-rhamnose, D-fucose, D-chinovose (6-deoxy-D-glucose), D-glucose, convolvulinolate (11-hydroxy-pentadecane acid), jalapinolate (11-hydroxypalmitic acid), 7-hydroxy-decane acid, ipurolic acid (3,11dihydroxy-tetradecane acid) in the latex of I. carnea and sub-species I. fistulosa. Tirkey et al. [59] reported the phytochemical studies of the leaves of I. carnea and found the presence of alkaloids, reducing sugars, glycosides and tannins in the dried powdered leaves, while acacetin-7-galactoside, flavone glycoside and saponin of unknown chemical structure called ipomotocin contain in the latex. In recent studies, the leaves, stem and flowers

of I. carnea have been reported to contain appraisable amount of polyphenols (30–70 mg catechol equivalent/g dry material) and flavonoid (80–120 mg quercetin equivalent/g dry material) [26]. Arora et al. [60] reported the presence of alkaloids, carbohydrates, tannins, phenolic compounds, proteins and amino acid, terpenoids and sterols and saponins in methanol extract of leaves and flowers of I. carnea. Among these phytochemicals, only alkaloids of polyhydroxylated class and terpenoid in the leaves, flowers and seeds have been characterized partially. Chromatographic study on the leaves, flowers and seeds resulted in the isolation of swainsonine, 2-epi-lentiginosine, calystegines B1, calystegines B2, calystegines B3, calystegines C1 and N-methyl-trans-4-hydroxy-L-proline at varying combination and concentration [17]. A gas chromatography–mass spectrometry study on the hexane extract of I. carnea showed the presence of a panel of 13 compounds including hexadecanoic acid, stearic acid, 1,2-diethyl phthalate, n-octadecanol, octacosane, hexatriacontane, tetraacontane and 3-diethylamino-1-propanol [43]. In case of protein, only one protein molecule has been isolated and characterized from the latex of I. carnea, known as “Carnein”, which is a serine protease with a molecular weight of 80.24 kDa [61].

Concluding remarks There is the resurgence of interests on phytomedicine recently. Modern medical science is looking for the establishment of traditional medicine, especially phytomedicine, in parallel with modern chemical medicine. In fact, the phytomedicines are the source of many chemical medicines, too. Phytotherapy is believed to be one of the mainstream therapeutic approaches in future, for its safety and potency. I. carnea was being used for thousands of years, but very few scientific studies have been done on this promising medicinal plant. Some interests among the scientists were noticed only recently. However, most of the researches on the medicinal issue of I. carnea have explored only in in vitro cellular and animal models. To establish this important medicinal plant for human drug development, more pre-clinical and clinical studies are required. This review emphasized more on basic research on the therapeutic effect of I. carnea and its phytoconstituents using disease-specific animal (e.g. diabetic, immune-deficient, cancerous, etc,) model first. In vitro animal cell experiment (e.g. mouse embryonic fibroblast 3T3, cerebral cortex bEnd.3, embryo NIH-3T3, pancrease RIN-5F, myocardial endothelial

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Fatima et al.: Ipomoea carnea: pharmacology, toxicology and phytochemistry

MyEnd, Hamstar kidney BHK-21, etc. cell lines.) may provide a feasible technique to figure out both organspecific pharmacological effect and active principles of I. carnea besides preliminary toxicological evaluation. A stepwise evaluation of the therapeutic effect of I. carnea using normal and diseased human cell line can provide a strong pre-clinical scientific basis of the I. carnea usage. Finally, I. carnea and/or its phytoconstituents of clinical significance might be applied clinically only after safety evaluation. It is hopeful that some active bio-components have been characterized in I. carnea, which might be used as clinical trial for drug development. More scientific studies (both clinical and basic studies) can give I. carnea a notable position in modern phytotherapy research. Acknowledgments: This work was supported in part by the National Natural Science Foundation of China (81172049 and 30371493) and the Science and

Technology Innovation Team of Colleges Universities in Sichuan Province (13TD0032).

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Conflict of interest statement Authors’ conflict of interest disclosure: The authors stated that there are no conflicts of interest regarding the publication of this article. Research support played no role in the study design; in the collection, analysis and interpretation of data; in the writing of the report or in the decision to submit the report for publication. Research funding: None declared. Employment or leadership: None declared. Honorarium: None declared.

Received September 18, 2013; accepted February 9, 2014; previously published online March 22, 2014

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A review on Ipomoea carnea: pharmacology, toxicology and phytochemistry.

Phytomedicines are increasingly being established in modern medical science. The shrub Ipomoea carnea has been used traditionally for thousands of yea...
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