Vartika Jain¹, Bhavika Kunwar¹ and S. K. Verma^2*

¹Department of Botany, Government Meera Girls’ College, Udaipur, Rajasthan, India,

²Department of Medicine, Pacific Medical College and Hospitals, Udaipur-313001, Rajasthan, india.

Corresponding Author E-mail: skvermaster@gmail.com

DOI : https://dx.doi.org/10.13005/bpj/2709

Abstract

Impaired thrombolysis is one of the causes of the development of cardiovascular diseases (CVD). The synthetic thrombolytic agents such as streptokinase, urokinase and antistreplase have their own side effects. Plants are always considered as safe and cost-effective therapeutic agents. Dietary therapeutics is an emerging branch for the prevention and treatment of several ailments. The present article compiles 43 edible plants which have shown in vitro thrombolytic potential and are also employed in the diets of several ethnic communities in India. Among these, Bauhinia purpurea and Baccaurea ramiflora are two plants having more than 70% in vitro clot lysis potential; Coccinia grandis, Curcuma longa, Cyperus rotundus, and Typha domingensis have 50-70% thrombolytic activity; and the rest of the plants have 11-49% thrombolytic activity. These 43 plants also include spices and condiments such as Turmeric, Black pepper, Indian Bayleaf, Coriander and Ginger, which affirms the traditional saying of using food as medicine. Besides, these edible plants also possess various phyto-constituents and health-beneficial pharmacological activities. If these plants could be incorporated into a routine diet, it might be possible to prevent or delay the onset of CVD. However, detailed studies are required to evaluate the pattern of CVD in ethnic communities consuming such plants, as well as systematic clinical trials are warranted to investigate the thrombolytic efficacy of these plants.

Keywords

Bauhinia purpurea; Cardiovascular Disease; Food; Streptokinase; Traditional Medicine; Turmeric

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Copy the following to cite this article: Jain V, Kunwar B, Verma S. K. A Review on Thrombolysis Enhancing Indian Edible Plants. Biomed Pharmacol J 2023;16(3).

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Introduction

Plants are nature’s wonderful gift to mankind, not only for providing oxygen as one of the most essential requirements of human existence but also for providing food, fodder, fiber, fuel, medicine, dye, timber, etc. Primitive people lived in forests and used natural resources for survival. They realized the importance of various plant species available in the surroundings and started using those species to fulfil the needs of daily life. They also noticed that plants can also act as medicine for prevention and cure of many diseases and ailments and therefore, included several plants in diets. The study of such man-plant relationships forms the discipline of Ethnobotany¹.

Several edible plants play a very important role in the lives of ethnic communities as they not only provide fresh food but also useful sources of nutrients, medicines, firewood, dyes, building materials, and help in generating income. Moreover, cultivation of edible plants also helps in the conservation of many wild plants which are under pressure due to various biodiversity threats. Therefore, a number of studies have been carried out in various parts of the world to document the ethnobotanical knowledge associated with wild edible plant species^2-7. Interestingly, many such plant species have demonstrated significant pharmacological activities in animal and human studies, such as antioxidant, anti-inflammatory, analgesic, antimicrobial, hypoglycemic, hepatoprotective, anticonvulsant, anti-platelet aggregation, adaptogenic, immunomodulatory, hypotensive, hypolipidemic, cytotoxic, anti-proliferative, diuretic, and nootropic^8-10. Furthermore, these plants are rich in various phytochemicals such as flavonoids, phenols, tannins, alkaloids, saponins, steroids, etc. The presence of bioactive molecules and pharmacological activities scientifically validate many of the folk medicinal claims for the edible plant species and serve as good evidence to recommend them as functional foods.

Thrombus is the main culprit behind cardio-vascular diseases (CVD), leading towards the development of diseases like stroke, embolism, ischemia, deep vein thrombosis etc. Lysis of thrombus is an important event naturally going on in the body with the help of processes such as fibrinolysis. The mechanism behind thrombolytic action is by activating plasminogen, which forms plasmin. Plasmin thus formed cleaves the fibrin and the clot is finally dissolved. If the body’s natural thrombolysis is reduced or impaired for several reasons, it may have serious consequences. In that case, modern medicine takes the help of synthetic thrombolytic agents such as streptokinase, urokinase, tissue plasminogen activator and/or anistreplase, reteplase, tenecteplase. These agents mainly activate plasminogen to start a cascade of events related to thrombolysis. However, some serious side effects are also associated with these agents, necessitating the need for the development of comparatively safer as well as cost-effective thrombolytic molecules^11-13.

The diet-disease relationship has been explored in many scientific studies, and changes in dietary behaviour have been shown to reduce the risk of cardio-metabolic disorders. Dietary modifications to improve various health conditions are now a preferred method of treatment as well as prevention of upcoming diseases¹⁴. Plants have played an important role in various therapeutic diets, such as, Mediterranean diet and Dietary Approaches to Stop Hypertension (DASH) diet¹⁵. It is recommended that intake of plants which are easily digestible and have high fiber content could be less stressful for heart during acute stages of heart disease¹⁶. In view of this, plants have been explored to provide safe, effective, and cheaper thrombolytic molecules. Many plant species have exhibited in vitro thrombolytic potential in scientific studies carried out in different parts of the world¹⁷. Moreover, some of those studied plants are also used as edibles among Indian ethnic communities. The present paper is to provide an overview of current knowledge on edible plant species that have demonstrated in vitro thrombolytic potential and to provide scope for future research.

Materials and Methods

For this purpose, first, a listing of plants which have shown in vitro thrombolytic activity was done by screening online databases such as Pubmed, Google Scholar, Research Gate, Science Direct, Taylor and Francis, and Springer Link as well as books and non-impact and non-indexed journals using keywords such as ‘in vitro thrombolysis, clot lysis, plants, herbs’ up to July 2022. Further short-listing of those plants was carried out by using ‘Compendium of Indian Folk Medicine and Ethnobotany’⁶ as a reference book to find out whether those plant parts are consumed in diets of Indian ethnic communities. The resultant plants were categorised into four, i.e., having more than 70%, between 50 and 70%, between 30 and 50%, and less than 30% thrombolytic potential and details are given in Tables 1-4 respectively in which the plants are listed alphabetically by botanical names, along with their families, common names in English, habit, plant part used, percent clot lysis, and the corresponding reference. Updated botanical nomenclature for all the plants was used as available on the website 1⁵¹.

Results and Discussion

The present paper provides the botanical names and families of 43 edible plant species along with their in vitro percent clot lysis activity. These 43 plants have been distributed in 33 Angiosperm families and the most dominant family was Asteraceae with four plants, followed by Fabaceae with three plants and two each in the Cucurbitaceae, Solanaceae, Rutaceae, Zingiberaceae, and Araceae families. Rest 26 families represent a single plant species. Seven plants belong to the monocotyledon group and 36 plants belong to the dicotyledon group (Tables 1-4). The highest number of plants is represented as herbs (58.13%) followed by trees (23.25%), shrubs, and climbers (9.3% each) as depicted in Figure 1.

Table 1: Edible plants with in vitro thrombolytic potential > 70%

Botanical name & Family	Common name	Habit	Plant part	Percent clot lysis	References
Baccaurea ramiflora Lour. (Euphorbiaceae)	Burmese grape	Tree	Seed	88.21	18
Bauhinia purpurea L. (Fabaceae)	Purple butterfly tree	Tree	Leaves	91.02	19

The studies included in this paper have a range of 41 to 86% thrombolytic activity for the positive control, streptokinase, and a two-to-ten percent range of thrombolytic activity of distilled water as a negative control.

Figure 1: Growth form of Indian edible plants showing in vitro clot lysis Click here to view Figure

Table 2: Edible plants with in vitro thrombolytic potential between 50-70%

Botanical name & Family	Common name	Habit	Plant part	Percent clot lysis	References
Coccinia grandis (L.) Voigt. syn. Coccinia indica Wight. & Arn. (Cucurbitaceae)	Scarlet-fruited Ivy gourd	Climber	Leaf	57.94	20
Curcuma longa L. (Zingiberaceae)	Turmeric	Herb	Rhizome	53.32	21
Cyperus rotundus L. (Cyperaceae) Typha domingensis Pers. (Typhaceae)	Common Nut Sedge       Southern Cattail	Herb      Herb	Rhizome   Whole  plant	60.00           67.16	22   23

Notably, two plants have shown more than 70% thrombolytic potential (Table 1) and four have shown 50-70% thrombolytic potential (Table 2). Twenty-six plants have shown between 30 and 50% in vitro thrombolytic potential (Table 3) and twelve plants have shown less than 30% thrombolytic potential (Table 4).

Table 3: Edible plants with in vitro thrombolytic potential between 30-50%

Botanical name & Family	Common name	Habit	Plant part	Percent clot lysis	References
Acmella paniculata (Wall. ex DC.) R.K. Jansen syn. Spilanthes paniculata Wall. ex DC. (Asteraceae)	Panicled spot flower	Herb	Leaves	42.77	24
Anacardium occidentale L. (Anacardiaceae)	Cashew nut	Tree	Nut	33.79	25
Bacopa monnieri Wettst. (Plantaginaceae)	Water hyssop	Herb	Leaf	47.39	26
Boerhavia diffusa L. (Nyctaginaceae)	Horse Purslane	Herb	Leaf	38.42	27
Brassica oleracea L. (Brassicaceae)  Capparis decidua Edgew. (Capparaceae)	Cabbage   Bare Caper	Herb   Shrub	Flower Leaves Fruit	42.75 30.24  32.39	28 29 30
Capsicum frutescens L. (Solanaceae)	Capsicum	Herb	Fruit	36.87	29
Coriandrum sativum L. (Apiaceae)	Coriander	Herb	Fruit	43.25	21
Cuscuta reflexa Roxb. (Cuscutaceae)	Devils hair	Climber	Whole plant	44.63	31
Ficus racemosa L. syn. Ficus glomerata Roxb. (Moraceae)	Cluster fig	Tree	Fruits	47.23	32
Homalomena aromatica (Spreng.) Schott (Araceae)	Gandh kochu	Herb	Leaf	33.31	33
Leea indica (Burm.f.) Merr. (Leeaceae) Luffa cylindrica L. (Cucurbitaceae)	Bandicoot berry Sponge gourd	Shrub   Climber	Leaf   Fruit	39.30   45	34   35
Merremia vitifolia (Burm.f.) Hallier. f. (Convolvulaceae)	Grape-leaf wood rose	Herb	Leaf	42.48	36
Moringa oleifera Lam. (Moringaceae)	Horse Raddish Tree	Tree	Leaf	41.40	37
Ocimum tenuiflorum L. syn. Ocimum sanctum L. (Lamiaceae)	Holy Basil	Shrub	Leaves	30.01	25
Piper nigrum L. (Piperaceae) Punica granatum L. (Punicaceae)	Black Pepper Pomegranate	Climber   Shrub	Fruit   Fruit	35.4   38	38   39
Sesamum indicum L. (Pedaliaceae)	Sesame	Herb	Seed	32.94	38
Spinacia oleracea L. (Amaranthaceae)	Spinach	Herb	Leaves	40.9	40
Solanum torvum Swartz. (Solanaceae)	Turkey berry	Herb	Fruit	31.51	34
Syzygium aromaticum Merr. & L.M.Perry. (Myrtaceae) Tribulus terrestris L.(Zygophyllaceae)  Vigna mungo (L.) Hepper (Fabaceae)	Clove   Puncture vine   Black Gram	Tree   Herb   Herb	Flower buds Seed   Seed	32.18   33   31.52	21   41   42
Vigna unguiculata (L.) Walp. (Fabaceae) Zingiber officinale Roscoe (Zingiberaceae)	Cowpea     Ginger	Herb     Herb	Seed     Rhizome	40.33     30.13	43     44

Table 4: Edible plants with in vitro thrombolytic potential <30%

Botanical name & Family	Common name	Habit	Plant part	Percent clot lysis	References
Averrhoa bilimbi L. (Oxalidaceae) Camellia sinensis (L.) O. Kuntze (Theaceae)	Bilimbi   Black Tea	Tree   Herb	Fruit   Leaves	23.94   11.64	45   46
Cinnamomum tamala T. Nees & Eberm. (Lauraceae)	Indian bay leaf	Tree	Leaves	22.10	21
Eclipta prostrata (L.) L. (Asteraceae)	False Daisy	Herb	Leaves	15.19	24
Emilia sonchifolia (L.) DC.ex DC. (Asteraceae)	Red tassel-flower	Herb	Leaf	28.71	24
Launaea sarmentosa Schult. Bip. ex Kuntze (Asteraceae)	Beach Launaea	Herb	Whole plant	22.57	47
Moringa oleifera Lam. (Moringaceae)	Horse Raddish Tree	Tree	Flower	20.52	37
Murraya koenigii Sprin (Rutaceae)	Curry leaf tree	Tree	Leaves	22.14	40
Musa sp. var. Nanjangud rasa bale (Musaceae)	Banana	Herb	Flower pseudostem	18 13	48
Nigella sativa L. (Ranunculaceae)	Black cumin	Herb	Seeds	28.49	21
Pistia stratiotes L. (Araceae)	Water lettuce	Herb	Leaves	12.06	49
Zanthoxylum rhetsa DC. (Rutaceae)	Indian prickly ash	Tree	Leaves	25.23	50

One plant, namely, Moringa oleifera (Fig. 2), has been listed twice in Tables 3 and 4 with different plant parts (leaves and flowers) and counted only once. M. oleifera is considered as ‘The Miracle tree’ with its multifarious beneficial activities for human health. Though its leaves and flowers possess moderate thrombolytic potential (between 20 to 42%), but along with many nutritive and therapeutic phytochemicals and other pharmacological activities, this plant could be very well recommended for dietary therapeutics in the prevention of cardiovascular diseases⁵².

Plants having >70% thrombolytic activity

Interestingly, ethanolic extract of Bauhinia purpurea (Fig. 3) leaves have shown 91.02% clot lysis activity, which was more than the standard drug streptokinase, having 72.83% clot lysis activity (Table 1). Leaves of B. purpurea are used as vegetables in Bengal, Bihar, Odisha, Jharkhand, Madhya Pradesh and some North-East states of India⁶. Leaves have shown presence of flavonoids, quercetin, rutin, apigenin and apigenin 7-O-glucoside along with lupeol (34.48%), stigmasterol (15.63 %), lanosterol (4.15 %), ergosterol (2.82 %), hexadeconic acid, hexadeconic acid methyl esters, octadecadienoic acids and octadecatrienoic acid, beta-tocopherol, phytol, and vitamin E acetate^53,54 as well as hypoglycemic, antidiarrhoeal and antimicrobial⁵⁵ activities. Similarly, aqueous extract of Baccaurea ramiflora seeds have shown 88.21% clot lysis, which was more than the standard drug streptokinase, which had 78.98% clot lysis (Table 1). B. ramiflora is a wild edible plant native to north-eastern states such as Meghalaya, Manipur, and Arunachal Pradesh⁶. It is also used during the holy rituals in the‘Rathyatra’ procession of Lord Jagannath in Odisha⁵⁶. The fruits of B. ramiflora are rich in vitamin C, protein, and iron⁵⁴. Seeds have shown presence of Sapidolide A and cytotoxic, analgesic, anti-inflammatory, CNS depressant and antidiarrheal^57-58, antioxidant⁵⁹, hypolipidemic⁶⁰ and antimicrobial activities⁶¹. Seed oil contains palmitic acid (33.67%), stearic acid (19.38%), arachidic acid (9.38%), oleic acid (24.48%), 11-transeicosenoic acid (12.75%) and a high iodine value of 80.32⁶². In view of this, seeds of B. ramiflora could be included in the diet for nutritional as well as therapeutic benefits.

Plants having 50-70% thrombolytic activity

Table 2 shows that there are four plants that have shown more than 50% but less than 70% thrombolytic potential. These are Coccinia grandis (Fig. 4), Curcuma longa, Cyperus rotundus and Typha domingensis. Leaves of C. grandis have been shown to possess anti-inflammatory, antioxidant, hypoglycemic, hypolipidemic, analgesic, and antipyretic activities with beta-sitosterol as an important phyto-constituent along with phenolic and flavonoid compounds⁶³. These are added advantage to its in vitro thrombolytic effect, which was 57.94% as observed in a study by Sultana et al.²⁰. Methanolic extract of rhizome of C. longa has shown 53.32% in vitro clot lysis potential. In view of this and its other activities such as platelet aggregation inhibition, anti-inflammatory, antioxidant activities, it is one of the most useful spices used in Indian cuisines^64,65. The active ingredient of Turmeric is Curcumin, which possesses anti-viral and immunomodulatory activities along with other pharmacological activities⁶⁶. Tuberous roots of Cyperus rotundusL. are popularly known as ‘Nagarmotha’ in Western India and are used to treat various ailments by native communities of India. It is also used as an edible inNorth Bihar, Rajasthan and the Attapadi hills situated in the Western Ghats of India⁶. Ethanolic extract of its rhizome (200µg/ml) has shown 60% in vitro thrombolytic potential²² which validate the traditional knowledge on its use to treat heart stroke by Taungya community in Terai Arc Landscape of India⁶⁷. Antioxidant, anti-inflammatory, cardioprotective, hypolipidemic, antidiabetic, antiobesity, antiplatelet etc. are some of its other health-beneficial activities, recommending it for dietary intake⁶⁸. Leaves and shoots of Typha domingensis are used for food purpose by Konda Reddis of Rampa Agency, East Godavari District, Andhra Pradesh, and the inflorescence is consumed in North-East states of Assam and Arunachal Pradesh⁶. It has been shown to possess antioxidant, vasodilator, hypolipidemic, bronchodilator, cytotoxic, antimicrobial activities and is rich in vitamin E, nonacosane, piperine, triacontane, n-hexadecanoic acid, decanoic acid, tetracosane, oleic acid, phytol, sitosterol, naringenin, n-acetoacetyl-deacetylcolchicine and many other phyto-therapeutic compounds^23,69.

Figure 2: Moringa oleifera Click here to view Figure

Figure 3: Bauhinia purpurea Click here to view Figure

Figure 4: Coccinia grandis Click here to view Figure

Spices having thrombolytic activity

Spices have shown moderate thrombolytic potential such as Clove (Syzygium aromaticum),Black pepper (Piper nigrum), Ginger (Zingiber officinale), Red chilly (Capsicum frutescens), Coriander (Coriandrum sativum), Indian Bayleaf (Cinnamomum tamala) as depicted in Table 3 and 4. Some of these spices have also demonstrated anti-platelet potential, which is an important mechanism of clot lysis¹⁷. Figure 5 depicts 20 common edible plants having in vitro thrombolytic activity out of the 43 scrutinized plant species. These species also possess several therapeutic bioactive compounds. For example, capsaicinoids, flavonoids, carotenoids, steroids, saponins in Capsicum; monoterpene, sesquiterpene, geraniol, linolol, bornyl acetate, phytosterols, caryophylene oxide, pcoumaric acid, vanillic acid etc. in Cinnamomum tamala; flavonoids, gallic acid, ferulic acid, coumarins, salicylic acid, tartaric acid, maleic acid, arbutin etc. in Coriandrum sativum; murrayazolidine, murrayazoline, murrayacine, koenimbine, koenine, mahanimbine,

Figure 5: Some common edible plants demonstrating in vitro thrombolytic activity Click here to view Figure

girinimbine, mukoeic acid etc. in Murraya koenigii (Fig. 6); p-cymene, carvacrol, thymoquinone, thymohydroquinone, dithymoquinone, 4-terpineol, tanethol, sesquiterpene longifolene α-pinene etc. in Nigella sativa; eugenol, carvacrol, linalool, β-caryophyllene, rosmarinic acid, oleanolic acid, ursolic acid etc. in Ocimum tenuiflorum (Fig. 7); gingerol, shoagaol, paradol, quercetin, zingerone, gingerenone-A in Zingiber officinale (Fig. 8); Piperine as major constituent in Piper nigrum besides volatile oil, oleoresins, and alkaloids; sesamin, sesamol, sesamolin, pinoresinol etc. in Sesamum indicum (Fig. 9) and eugenol, eugenyl acetate, β-caryophyllene etc. in Syzygium aromaticum⁷⁰. Besides, many pharmacological activities such as antioxidant, anticancer, antidiabetic, anti-inflammatory, immuno-modulatory, hepatoprotective, platelet aggregation inhibition, neuro-protective, nephroprotective, and cardio-protective have also been reported from these plants^8,70-72. This further emphasizes that use of these plants in the diet could be beneficial for many purposes.

Figure 6: Murraya koenigii Click here to view Figure

Figure 7: Ocimum tenuiflorum Click here to view Figure

Figure 8: Zingiber officinale Click here to view Figure

Figure 9: Sesamum indicum Click here to view Figure

Thrombolytic activity of leaves of edible plants

Plant based diets including leafy green vegetables provide strong evidence for benefits in cardiovascular risk factors such as obesity, diabetes, hypertension, high lipid levels etc.⁷³. In the present analysis, leaves of 42% of the plants were consumed and reported to possess thrombolytic activity, followed by fruits (22%), seeds (13.33%), flowers (8.88%), and rhizome and whole plant (6.66% each), which is depicted in Figure 10.  

Figure 10: Percent contribution of parts of the edible plants demonstrated  in vitro thrombolytic activity. Click here to view Figure

Spinacia oleracea is a well-known leafy vegetable that has shown 40.9% thrombolytic potential (Table 3). It is considered a functional food as it is rich in various vitamins and minerals as well as many therapeutic phytochemicals such as flavones, flavanols, glucuronides, methylenedioxyflavonol glucuronides, and carotenoids. Spinach helps in scavenging reactive oxygen species and thereby prevents macromolecular oxidative damage. It has also been shown to modulate genes which are involved in metabolism, proliferation, inflammation, and antioxidant defense and therefore, demonstrates various pharmacological activities such as antioxidant, hypolipidemic, hypoglycemic, anti-hypertriglyceridemia, anti-obesity, anticancer, anti-inflammatory, anti-α-amylase, and bileacid binding capacity^74,75. In view of this, intake of spinach can help in thrombolysis and also provide protection against several other ailments.

Figure 11: Anacardium occidentale Click here to view Figure

Leaves of Murraya koenigii; known as Curry leaf tree is used for flavor in various Indian cuisines⁶ and exhibited 22.14% in vitro thrombolytic potential (Table 4). The cardioprotective potential of Murraya koenigii has been demonstrated in doxorubicin-induced cardiotoxicity in Wistar albino rats. Lyophilized leaf extract of M. koenigii was administered orally in a concentration of 2 g/kg to animals for 14 days, which significantly reduced the levels of cardiac troponin I, NT-pro BNP, aspartate aminotransferase, lactate dehydrogenase, myeloperoxidase along with improvement in reduced glutathione, glutathione reductase, glutathione peroxidase, total antioxidant capacity, superoxide dismutase, and catalase activity, along with a reduction in lipid peroxidation levels⁷⁶. This clearly indicates the cardio-protection ability of M. koenigii along with antioxidant and anti-inflammatory activities, and therefore, its daily consumption could be beneficial for the heart. Leaves of Bacopa monnieri; a well-known memory-improving plant, have shown 47.39% thrombolytic activity (Table 3). This small herb is rich in several phytochemicals for example, luteolin, quercetin, apigenin, ursolic acid, bacopasides, β-sitosterol, stigmasterol, ascorbic acid, bacopasaponins, bacoside, cucurbitacins, wogonin and exhibited various health-beneficial activities such as adaptogenic, antioxidant, antihypertensive, antilipidemia, anti-inflammatory, analgesic, antidiabetic, antiarthritic, anticancer, smooth muscle relaxant antipyretic, neuroprotective, and hepatoprotective⁷⁷. Thus, clot lysis activity is an additional benefit gained by people after consuming its leaves. The leaves of sacred Holy Basil (Ocimum tenuiflorum) have also demonstrated anticoagulant properties by prolonging prothrombin time and activated partial thromboplastin time with linolenic acid as a major constituent⁷⁸. The cardioprotective potential of hydroalcoholic extract of O. tenuiflorum has also been observed in isoproterenol induced myocardial infarction in rats at a dose of 50 mg/kg further indicating the importance of this herb in CVD⁷⁹.

Leaves of Emilia sonchifolia are used to prepare vegetable in western Maharashtra and Nagaland states of India. It is also recommended to treat chest pain by tribal communities in India⁶. Notably, it has demonstrated 28.71% clot lysis activity (Table 4). This plant is rich in flavonoids, flavones glycosides, beta-sitosterol, stigmasterol, ursolic acid, quercetin, quercitrin, rutin, kaempferol 3-β-D-galactoside, senkirkine, doronine, n-hexacosanol, and triacontane and has been shown to possess antioxidant, antidiabetic, anti-cataract, anti-inflammatory, antiviral, analgesic and anti-cancer activities⁸⁰. Leaves of Acmella paniculata are used for making vegetables in the north-eastern states of India and are mostly used for the treatment of toothache⁶. It is rich in phyto-constituents such as spilanthol, β-sitosterol, stigmasterol, α-and β-amyrin, vanillic acid, limonene, β-caryophyllene, (z)-β-ocimene, germacrene-D, scopoletin and trans-ferulic acid and has also demonstrated anti-inflammatory, antioxidant, vasorelaxant, immunomodulatory, and analgesic activities in animal studies⁸¹.

Brassica oleracea is another popular vegetable in India. Its flowers and leaves contain phenolics, polyphenols, saponins, tannins, steroids, flavonoids, alkaloids, glucosinolates, reducing sugars, and vitamin C. It has been shown to possess strong antioxidant activity in different antioxidant assays. Moreover, inhibition of DNA methylation, prevention of DNA damage and threats to cancer and cardiovascular diseases are its other benefits. All these bioactive molecules and pharmacological activities make it a good candidate for recommending as a nutraceutical in daily diet⁸². Whole plant of Launaea sarmentosa is used as vegetable in Lakshadweep Island⁶ and also in Vietnam as nutritious vegetable⁸³. It has also shown anti-inflammatory, antioxidant, antidiabetic, and hepatoprotective properties along with 22.57% clot lysis potential⁸⁴.

Thrombolytic activity of fruits of edible plants

Out of these 43, fruits from 10 plants are used in the diet (Fig. 10). For example, Anacardium occidentale (Fig. 11) is one of the famous edible tree nuts. It is consumed as raw, roasted form or also used to prepare sweets in the winter season⁸⁵. Its kernels are rich in protein, vitamin E, K, B6, riboflavin, minerals like potassium, calcium, magnesium, phosphorous, iron, copper, zinc, manganese, selenium etc., glutamic acid, arginine, cholesterol-lowering phytosterols, phosphatidylcholine, beta-sitosterol, lutein, zeaxanthin, epicatechin, catechin, polyphenols, flavanol etc. Cashewnuts have been shown to possess antioxidant, hypoglycemic and hypotensive potential⁸⁶. Thus, the thrombolytic action of A. occidentale is an additional weapon for protection from several diseases, including cardiovascular diseases and metabolic syndrome. Pomegranate is another well-known fruit plant which is rich in ellagitannins, polyphenols, luteolin, kaempferol, quercetin, gallic acid, ellagic acid, punicalagin, gallagic acid, delphinidin, cyanidin, pelargonidin, catechin, punicalin, and minerals, such as sodium, potassium, calcium, magnesium, phosphorus, and nitrogen. Fruit and peel of Punica granatum have shown anti-thrombotic potential besides anti-inflammatory, anti-diabetic, hypolipidemic, anti-platelet, anticoagulant, cardio-protective and anticancer properties^87-89.

Fruits of Ficus racemosa, known as ‘Gular’ in India, are rich in nutritive value and full of phytochemicals such as hentriacontane, β sitosterol, tiglic acid, esters of taraxasterol, lupeol acetate, phytosterol, euphol, euphorbinol, isoeuphorbol, tannins, steroids, tinyatoxin, tri-methyl ellagic acid, flavonoids, alkaloids and have demonstrated hypolipidemic, anti-diabetic, anti-carcinogenic, antioxidant, gastroprotective and analgesic activities in various scientific studies⁹⁰. Fruits of Capparis decidua (Fig. 12) are used to prepare the famous traditional Rajasthani cuisine ‘Panchkuta’ and are also used to make pickle. Interestingly, a methanolic extract of its fruits has shown a 32.39% clot lysis potential (Table 3). This is an important addition to its pharmacological profile besides anti-atherosclerotic, hypolipidemic, antioxidant, and anti-inflammatory properties⁹¹. Therefore, it could be used in dietary modification for therapeutic benefits.

Fruits of Solanum torvum are used as vegetable and also to prepare chutney in eastern India. Ethnic communities of the Mayurbhanj district of Odisha utilize its fruits for the treatment of heart disease⁶. Fruits are rich in steroidal glycosides, phenolic compounds, isoflavonoids, etc. Interestingly, its fruits have shown a 31.51% clot lysis potential (Table 3). Besides, thrombolytic potential, fruits of S. torvum have also demonstrated anti-inflammatory, antidiabetic, anti-ulcerogenic, anti-hypertensive and anticancer activities in scientific studies⁹². Fruits of Luffa cylindrica have exhibited 45% clot lysis potential (Table 3) and used as vegetable in Rajasthan, Kerala and Sikkim⁶. Its fruits possess vitamin A, B5, B6, C, and dietary fibers as well as phyto-constituents such as gallic acid, caffeic acid, cinnamic acid, ferulic acid, ellagic acid, rutin, quercetin, luteolin, bobin, vitexin, myrecetin, catechin, noctacosane, n-heptacosan, n-hexacosane, n-tetracosane, n-tricosane, etc. Many pharmacological activities have also been demonstrated by fruits of L. cylindrica such as antioxidant, anti-inflammatory, hypoglycemic, antimicrobial and sedative which potentiate its use in daily diet⁹³.

Fruits of Averrhoa bilimbi are rich in ascorbic and oxalic acids and possess carbohydrates, proteins, amino acids, coumarin, flavonoids, tannins, essential oils, terpenes, and valepotriates. Besides, many phytochemicals such as hexadecanoic acid, butyl nicotinate, (Z)-9-octadecenoic acid, nonanoic acid, nonanal, (Z)-9-pentacosene, (Z)-3-hexenol, (Z)-9-tricosene, octane, tricosane, (E)-2-decenal, 2-furfural, 2,4-dihydroxy-6-((4-methylpentyloxy) methyl) benzaldehyde etc. have been isolated from its fruits⁹⁴. Interestingly, anticoagulant activity of ethanol extracts of leaves and fruitsof A. bilimbi has been demonstrated in normal and alloxan-induced diabetic rats after oral administration at a dose of 250 mg/kg for 14 days, which has significantly increased prothrombin time⁹⁵. This further validates the results obtained through in vitro clot lysis activity (Table 4). Seeds of Tribulus terrestris (Fig. 13) are consumed as famine food in Rajasthan⁶ and have shown to possess 33% in vitro thrombolytic activity. T. terrestris possesses various phytochemicals such as quercetin, kaempferol, isorhamnetin, rutin, tribuloside, tribulusamide C, tribulusterine, tribulusin A, harmine, benzoic acid, vanillic acid, 2-methyl benzoic acid, and ferulic acid. Moreover, it has also demonstrated antioxidant, hypoglycemic, antimicrobial, anti-inflammatory, cardio-protective, anticancer, anti-ageing and hepatoprotective properties^41,96.

Figure 12: Capparis decidua Click here to view Figure

Figure 13: Tribulus terrestris Click here to view Figure

Edible plants having thrombolytic and platelet aggregation inhibition activities

Inhibition of platelet aggregation is another important mechanism for maintaining the patency of blood vessels. Many of the phyto-constituents such as caffeic acid, epigallocatechin, catechin, quercetin, kaempferol, apigenin, gallic acid present in the plants listed in this paper have also shown platelet aggregation inhibition activity⁹⁷. Likewise, some other compounds, such as Piperin, isolated from Piper nigrum have shown inhibition of platelet aggregation through attenuation of cytosolic phospholipase A₂ and thromboxane A₂ synthase involving arachidonic acid (AA) metabolism⁹⁸. Curcumin; a polyphenol isolated from Curcuma longa, also demonstrated platelet aggregation inhibition by activating adenosine A_2A receptor-stimulated protein kinase A activation and phosphorylation of vasodilator-stimulated phosphoprotein⁹⁹. Gingerol, shogaol, paradol, and gingerol analogues isolated from Zingiber officinale have also demonstrated anti-platelet function¹⁰⁰. Similarly, (+)-nootkatone isolated from Cyperus rotundus has also shown significant in vitro collagen-, thrombin-, and AA-induced platelet aggregation inhibition in a dose-dependent manner as well as ex vivo platelet aggregation inhibition in mice blood by increasing tail bleeding time¹⁰¹. Sesamum indicum also possesses many bioactive molecules such as sesamin, epi-sesamin, sesamol, γ-tocopherol, and sesamolin. Among these, epi-sesamin has shown a strong anti-thrombotic effect by preventing thrombin and activated blood coagulation factor X production, prolonging activated partial thromboplastin time and prothrombin time, reducing thrombin-catalyzed platelet aggregation in mice as well as inhibiting TNFα-induced secretion of plasminogen activator inhibitor type 1 in human umbilical vein endothelial cells¹⁰².

Cuscutaroside A and its acetyl derivative, as well as scrophenoside B; isolated from whole plants of Cuscuta reflexa (Fig. 14), have demonstrated a weak platelet aggregation inhibitory activity induced by collagen with IC₅₀ values of 291.4 ± 47.9 μg/ml, 63.8 ± 4.4 μg/ml, and 180.5 ± 6.7 μg/ml, respectively. However, an acetylated derivative of Cuscutaroside A has shown strong platelet aggregation inhibition induced by AA with an IC₅₀ value of 72.6 ± 10.5 μg/ml¹⁰³. A dose-dependent adenosine diphosphate induced platelet aggregation inhibition has been demonstrated by 70% ethanolic extract of Eclipta prostrata leaves with 74.55%; 65.60%; 48.00% and 39.08% inhibition at the concentration of 100, 80, 60 and 40 mg/ml respectively with an IC₅₀ value of 59.02 mg/ml¹⁰⁴. The mechanism behind the anti-platelet property of E. prostrata and the corresponding bioactive molecules needs to be researched. However, all these studies indirectly support the anti-thrombotic potential of these edible plant species and provide motivation for initiating further research in this direction.

Figure 14: Cuscuta reflexa Click here to view Figure

Figure 15: Boerhavia diffusa Click here to view Figure

COVID-19 treatment potential of edible thrombolytic plants

Recent pandemic of COVID-19 has hugely affected the human population and thrombotic complications are one of the major causes of morbidity and mortality associated with this infectious viral disease¹⁰⁵. COVID-19-related coagulation disorders were associated with an increase in D-Dimer, fibrin degradation products, prothrombin time, activated partial thromboplastin time, and a decrease in antithrombin¹⁰⁶. Interestingly, herbal medicine was also employed to combat this virus and several in vitro, in vivo, and clinical trials have been carried out and are currently underway¹⁰⁷. Plants like Curcuma longa, Nigella sativa, Zingiber officinale, Piper nigrum, Ocimum tenuiflorum, Cuscuta reflexa, Moringa oleifera, etc. were used in herbal treatment and prevention of COVID-19. Some of the isolated phytochemicals such as quercetin, piperin, curcumin, apigenin, kaempferol, luteolin, thymol, rutin, eugenol, ursolic acid, caffeic acid, and oleanolic acid have also shown their potential against the SARS-CoV-2 virus and exhibited anticoagulant activity¹⁰⁶. In view of their thrombolytic potential, the addition of these plants to the diet for treatment or for prevention purposes seems quite relevant because this has been proven in scientific research related to the efficacy of these plants in COVID-19^65,107.

The present article has compiled the Indian edible plants having thrombolytic potential which are commonly used in the diets of various ethnic groups without knowing their multifarious beneficial effects on human health. Theoretically, it is possible to get benefit from these plants in the situation of altered thrombolytic states. In this context, the work of Sarkar¹⁶ is worth quoting, who has advised that few of the plants, for example, Boerhavia diffusa (Fig. 15), Chenopodium album, etc., should be used during the acute stage of heart disease such as acute myocardial infarction. He has stressed that during the acute stage, the diet should preferably include these vegetables. The rationale behind it could be their thrombolytic potential, antioxidant property, anti-platelet and hypolipidemic effect. Moreover, these vegetables are easily digestible without posing undue stress on the heart, which requires rest during the recovery period, and the gut favorable because of high fiber content, which does not allow constipation. Because straining on defecation during this crucial time is also hazardous and can cause arrhythmia and sudden death. Scientific studies have also shown that the intake of dietary fibers can reduce the risk of CVD through various means¹⁰⁸. For example, a recent cohort study in South Korea has also indicated the role of quality plant food in the prevention of metabolic syndrome¹⁰⁹. Therefore, dietary selection of plants with the above-mentioned properties could be helpful for management of CVD.

Safety issues

Though the edible plants mentioned in this article have thrombolytic activity, they should be consumed with caution. Over-consumption of the plants may cause adverse effects. For example, studies have shown that intake of curcumin in doses of 500-12000 mg produced symptoms like diarrhea, yellow stool, headache, and rashes¹¹⁰. Similarly, heartburn, nausea, abdominal pain, gas, bloating, etc. are some of the reported side effects of consumption of Z. officinale (750-2000mg)¹¹¹. Fruits of A. bilimbi can cause nephro- and neurotoxicity¹¹² and consumption of 80% fresh plants of T. terrestris has shown harmful effects on cardiac muscle, liver and kidney of goats and sheep¹¹³. In various animal studies, after consumption of M. oleifera, genotoxicity, kidney and liver damage, necrosis of splenic blood vessels, and neuronal glial cells have been reported¹¹⁴. Hepatotoxicity and gastrointestinal disorders after consumption of C. sinensis on empty stomach have been reported¹¹⁵. S. oleracea grown in heavy metal polluted sites can create risk for cancer¹¹⁶. Likewise, nitrate poisoning has been observed after ingestion of Brassica oleracea var. capitata¹¹⁷. Some of these plants such as T. domingensis¹¹⁸, B. purpurea¹¹⁹, O. tenuiflorum¹²⁰, S. torvum¹²¹, P. granatum¹²², B. monnieri¹²³ and M. koenigii¹²⁴ have yet to be tested for significant toxicity. However, plants having higher thrombolytic activity should be recommended cautiously to patients already taking anti-platelet and fibrinolysis enhancing drugs and supplements because there is a possibility of bleeding.

Conclusion

 The present article provides an overview of 43 plants which have demonstrated thrombolytic potential and are also being utilized by ethnic communities for edible purposes. If these species could be added as a supplement to the diets of people who are predisposed / susceptible to cardio-vascular diseases, they may serve the role of preventive agents. Addition of these plant species to the diet, both before and after the development of disease, could be beneficial in myriad ways due to the multifarious therapeutic potential of plants, which mostly act in a synergistic manner. However, large scale clinical studies could be executed for scientific evaluation of the effect of the addition of these plant species in the diet on the prevention or betterment of CVD. In this regard, the two edible plants with the highest clot lysis potential, namely, Baccaurea ramiflora and Bauhinia purpurea, should be screened for their in vivo thrombolytic potential on a priority basis.

Conflict of Interest

Authors declare that there is no conflict of interest.

Funding sources

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