Review: phytochemistry and medicinal properties of Solanum torvum fruits

Abstract

Background: Most plants have medicinal properties, which they achieve from certain secondary metabolites. Phytochemicals are compounds produced by plants. They may affect health but are not-essential nutrients as our diet does not require them to sustain life in the same way as vitamins and minerals.

Objectives: The study reports the phytochemistry and medicinal properties of Solanum torvum fruits.

Methods: A search of database sites such as PUBMED, Google Scholar, and Web of Science as well as other sources of literature available across public libraries was conducted to obtain information related to the topic.

Results: Here, we review the numerous medicinal properties of S. torvum (cardio and nephro protection, anti-hypertensive, analgesic, anti-inflammatory, anti-ulcer, anti-microbial activities) and relate them to the underlying phytochemicals and their biological actions.

Conclusion: This exposure is expected to provide researchers with updated information on S. torvum health benefit properties and related phytochemicals, which merit future research for developing pharmacological drugs aimed at curing ailments or diseases, and for possible use in preventive medicine.

KEYWORDS:

• Phytochemistry
• cardio-protection & treatment of heart related diseases
• anti-oxidant
• anti-microbial
• Solanum torvum fruits

Introduction

Most plants have medicinal properties due to the presence in their tissues of simple chemical elements like selenium or chromium, or of phytochemicals, thousands of which have been isolated and characterized. Some of these phytochemicals have no effect on human health, others can be dangerous. But for most of them, many beneficial biological activities such as anti-cancer, antimicrobial, anti-oxidant, anti-diarrheal, analgesic and wound healing activities have been reported (Jaiswal and Mohan 2012).

Phytochemicals are found in all foods of plant origin, especially whole grains, broccoli, brussels sprouts, cauliflower, citrus fruits, dark green leafy vegetables, garlic, tea, herbs and spices, onions, tomatoes, soya beans, wine, etc. (Biney et al. 2019). We focus here on Solanum torvum Sw., commonly known as Turkey berry, a member of the family Solanaceae, which contains about 3000 species (Fui 2012; Darkwah and Nkoom 2019). S. torvum originates from central and South America, and is now widespread as a wild plant in all tropics (Schippers 2004). It is cultivated in Africa, the West Indies (Adjanohoun et al. 1996) and Asia (Schippers 2004). Commonly available in the markets, the fruits are utilized as a vegetable and regarded as an essential diet ingredient of most Africans and Indians (Siemonsma et al. 2005). In Indonesia, S. torvum is considered as one of the best vegetable side-dish (Boonkerd et al. 1994).

However, S. torvum is not only used as food. It is also widely used in traditional medicine in Africa and Asia for preventing and curing a range of ailments (Chah et al. 2000; Kala 2005). Various preparations based on S. torvum fruits, seeds or vegetative parts are indeed reported to be effective medicines against fever, cough, wounds, pain, liver troubles, tooth decay, reproductive problems, arterial hypertension and also poisoning (use as antidote) (Ndebia et al. 2007; Kamble et al. 2009). S. torvum properties include sedative, diuretic, hemostatic, haemopoietic, anti-microbial effects (Chah et al. 2000; Fui 2012; Kamble et al. 2009; Biney et al. 2020) as well as free radicals scavenging thanks to its antioxidant effect (Sivapriya and Srinivas 2007). Phytochemical studies indicate that S. torvum fruits have sufficient concentrations of various alkaloids, flavonoids, saponins, tannins, and glycosides for explaining these pharmacological effects (Fui 2012). Vitamins, essential organic nutrients which are necessary for smooth metabolism in the body, can also be found in S. torvum (Levine 1986; Rath 1993; Levine et al. 1995; Sies and Stahl 1995; Biswas and Mannan 1996).

We categorized S. torvum medicinal properties as follow: cardio protection and heart related diseases treatment, nephro-protection, anti-inflammatory and analgesic action, anti-ulcers and anti-microbial activities. The objective of this paper is to provide an updated review of the biological mechanisms and phytochemicals lying at the basis of S. torvum numerous and outstanding medicinal properties.

Review

Physical characteristics and phytochemical analysis of S. torvum

S. torvum is annual or perennial depending on the conditions (Hasan and Jansen 1994). Plants grow best in full sunlight and do well in light shade or shade for part of the day but cannot survive under a closed forest canopy (Little et al. 2012). The erect spiny shrub or small tree is usually 2–5 m in height and 2–8 cm in basal diameter (Howard 1989). Plants are unarmed or prickly, usually pubescent with simple, branched, glandular or stellate hairs. The leaves are variable, usually alternate, simple and entire, or lobed, pinnatisect or imparipinnate (Kris-Etherton et al. 2002; Surh 2003; Konczak et al. 2010; Darkwah and Nkoom 2019). Fruits (Figure 1) are thin-fleshed berries, with a pepper-like odor and a bitter and acrid taste. They become yellow when fully ripe and contain numerous flat, round, brown seeds.

Figure 1. A photograph of Solanum torvum Fruit. Picture taken by Williams Kweku Darkwah (author).

Phytochemical analysis of methanolic extracts of sun-dried S. torvum fruits revealed the presence of alkaloids, flavonoids, tannins, saponins, glycosides, oil, tocopherol / Vitamins E, B and C, as well as iron salts (Sivapriya and Srinivas 2007; Amarowicz et al. 2010; George et al. 2011). Another study (Chah et al. 2000) pointed out S. torvum as a rich source of alkaloids, flavonoids, tannins, saponins, and glycosides. Total alkaloid content (0.12%), total glycoalkaloids (0.038%), and glycosylated compounds derived from solasodine, namely solasonine (0.0043%) and solamargine (0.0028%) were quantified by Pérez-Amador et al. (2007). Polyphenolic compounds (phenols, flavonoids and tannins) concentrations were recorded as 160.30, 104.36, and 65.91 mg/g, respectively (Kusirisin et al. 2009). Alkaloids, total saponins, total flavonoids and vitamin C contents of ethanolic extracts of immature and mature fruits were compared (Koomson et al. 2018) and found significantly different for alkaloids only (respectively 16.94 ± 2.3 mg/g in the immature fruits, and 6.32 ± 0.12 mg/g in mature fruits). This study confirmed that the extracts contained appreciable amounts of all these phytochemicals. The therapeutic interest of S. torvum major phytochemicals is given in Table 1 except for iron salts, saponins, and vitamins B (lack of data).

Table 1. S. torvum fruits phytochemicals and their therapeutic use.

Phytochemicals	Therapeutics
Alkaloids	Keep the body against oxidative stress. ii. Chemotherapeutic treatment. iii. Used as chemo preventive agents. iv. Constrain, reverse, or delay tumorigenesis
Flavonoids	Prevention of heart-related disease ii. Possess anti-ulcer properties.
Tannins	Prevention of heart-related disease. ii. Analgesic and anti-inflammatory effects. iii. Lower and maintain the systolic and diastolic Blood Pressure.
Glycosides	Nutritive purposes. ii. Effective for cough ailments. iii. Treatment of liver and spleen enlargement
Tocopherols / vitamin E	Sustain metabolism and boost immune system. ii. Inhibit the formation of carcinogens in the stomach. iii. Prevent the growth of cataracts in the eyes.
Phenols	Lower blood cholesterol. ii. Prevention of breast, colon and prostate cancers iii. Used in cancer therapy.
Oils	Optimal performance of the brain, ii. regulate reproductive function iii. Enhance bone health. iv. Treatment of pains associated with rheumatoid arthritis Dermatology disease therapy.
Vitamin C	Keeps the body against oxidative stress.

The absence of anthraquinones and cyanides in methanol, petroleum and chloroform extracts of fruits, leaves and roots of S. torvum, as well as, unexpectedly, the absence of glycosides and flavonoids was reported by Lakshmi et al. (2013). One new isoflavonoid sulfate named as torvanol A, and a new steroidal glycoside, named torvoside H, together with the already-known glycoside, torvoside A were detected in methanolic extracts of S. torvum fruits (Arthan et al. 2002). Torvanol A was also isolated from the leaves (Mahmood et al. 1983). Nine new compounds namely neochlorogenin 6-O-β-D-quinovopyranoside, neochlorogenin 6-O-β-D-xylopyranosyl-(1→3)-β-D-quinovopyranoside, neochlorogenin 6-O-α-L-rhamnopyranosyl-(1→3)-β-D-quinovopyranoside, solagenin 6-O-β-D-quinovopyranoside, solagenin 6-O-α-L-rhamnopyranosyl-(1→3)-β-D-quinovopyranoside, isoquercetin, rutin, kaempferol and quercetin were isolated (Yuan-Yuan et al. 2011). Furostanol glycoside 26-O-β-glucosidase was found as an important part of leaves methanolic extracts (Iida et al. 2005). Non-alkaloidal compounds, namely, 3, 4-trimethyltriacontane, octacosanyltriacontanoate and 5 hexatriacontanone, were identified by spectral and chemical analyses (Mahmood et al. 1983).

Medicinal properties of S. torvum

Medicinal properties of S. torvum, the mechanisms and the phyto-chemicals involved are summarized in Table 2. Alkaloids, saponins and glycosides are not mentioned in Table 2 as phytochemicals involved in the mechanisms listed due to lack of data on these phytochemicals.

Table 2. Summary of the medicinal properties of S. torvum fruits, underlying mechanisms and phytochemicals involved.

Medicinal properties	Mechanisms	Phytochemicals Involved	Reference
Cardio-protection & treatment of heart related diseases	Inhibition enzymes activities. Prevention and reversion of hyper-insulinemia	Flavonoids, and polyphenols	Fui (2012); Jaiswal and Mohan (2012); Kamble et al. (2009); Liu et al. (1977)
Nephro-Protective and Anti-Oxidant Activity	Chelation of free iron Reduction of DOX toxicity.	Flavonoids, and phenols	Abas et al. (2006); Loganayaki et al. (2010); Vaclavıkova et al. (2008); Waghulde et al. (2011).
Analgesic and Anti-inflammatory Activity	Inhibition of production of inflammatory mediators.	Tannins, and phenols	Ndebia et al. (2007); Vaclavıkova et al. (2008)
Anti-Ulcer Activity	Enhancement of gastric mucosal defense.	Flavonoids, sterols and triterpenes	Antonio et al. (2004); Nguelefack et al. (2008); Telesphore et al. (2008)
Anti-Microbial Activity	Inhibition of nucleic acid synthesis. Inhibition of cytoplasmic membrane function Inhibition of energy metabolism	Flavonoids	Chah et al. (2000); Travis et al. (2002); Xie et al. (2015); Cushnie and Lamb (2005); Xiao et al. (2013); Ulanowska et al. (2006).

Cardio-protection and treatment of heart-related diseases

People who take in a diet rich in fruits and vegetables, and therefore in phytochemicals, have a lower occurrence of various ailments, including cardiovascular diseases (Jaiswal and Mohan 2012). Many studies highlight a positive correlation between a reduced incidence of coronary heart disease and an increased dietary intake of natural phenolic antioxidants (Darkwah et al. 2018a). S. torvum fruit extracts display anti-oxidant properties (Rhee et al. 1972; Re et al. 1999) that are associated to their cardio-protective effect and prevention of heart-related diseases such as hypertension, strokes, coronary troubles. Several phytochemicals present in S. torvum (Table 1), in particular polyphenols, flavonoids and tannins display such anti-oxidative and free radical scavenging properties (Yeboah and Darkwah 2017), given their capacity to stabilize highly reactive free radicals, via electron(s) exchange with them.

Phenolic compounds are characterized by one or more hydroxyl substitution(s) on their aromatic ring (Figure 2). Cinnamic acid esters, such as caffeic acid phenethyl and benzyl esters, display selective cardiovascular protecting activity. Flavonoids, ubiquitously present in plants, are synthesized from the phenylpropanoid pathway, and consist of a large group of polyphenolic compounds with a benzo-γ-pyrone structure. The cardio-protective action of S. torvum has been assessed by recording changes in Echo Cardiograph (ECG), heart rate and measuring the levels of cardiac marker enzymes-lactic acid dehydrogenase (LDH) and creatine phosphokinase (CK-MB) (Van Acker et al. 2006; Yeh 2006; Kamble et al. 2009). The antioxidant defense enzymes superoxide dismutase (SOD) (Liu et al. 1977) and catalase (CAT) for heart tissue were also measured. These analyses demonstrated that the cardio-protective activity of S. torvum fruit extract is mainly due to its potent antioxidant properties.

Figure 2. Chemical structure of phenol derivative. The figure was obtained from (Asim et al. 2018) with permission from Bentham Science Publishers.

The effects of S. torvum on blood pressure and metabolic alterations were studied in male Wistar rats (Nguelefack et al. 2008; Mohan et al. 2009; Mohan et al. 2010), submitted to hypertensive conditions induced by a high-fructose diet (fructose 10%, w/v) ad libitum for six weeks. Systolic blood pressure was measured with non-invasive (indirect) and invasive (direct) methods. Ethanolic extracts of S. torvum were demonstrated to be effective in preventing high systolic blood pressure (BP). The efficacy of this plant for maintaining the systolic and diastolic BP (normal BP∼110/80) is due to the presence of phenols, flavonoids and tannins. These results, comparable to those obtained with the standard drug Nifedipine (10 mg/kg/day, p.o.), indicate that S. torvum has a clear anti-hypertensive activity (Nguelefack et al. 2008). Further, the hypotensive effect of aqueous and methanolic extract of S. torvum may partially result from their bradycardic (slow heart rate) effect (Nguelefack et al. 2008). In traditional medicine, S. torvum fruits are commonly used as anti-hypertensive (Fui 2012).

Other modes of action of torvum on heart and heart-related diseases have been identified, such as the inhibition of various enzymes such as the phospho-diesterase-5 (PDE-5) (Nguelefack et al. 2008), anti-platelet aggregation effect (Surh 2003) and repair capability on DNA damaged by free radicals (Abas et al. 2006).

Nephro-protection

Nephro-protective action of S. torvum fruits has been demonstrated on Doxorubicin (DOX)-induced nephrotoxicity in rats (Waghulde et al. 2011). DOX induces kidney cells destruction both in rats and humans by overproduction of semiquinone type free radicals (Olson et al. 1981; Olson and Mushlin 1990; Sharma et al. 2001). The antioxidant and nephro-protective properties of S. torvum flavonoids (Haenen et al. 1993), and their ability to chelate free iron, are involved in the reduction of DOX39-induced toxicity (Vaclavıkova et al. 2008). Kidneys histopathological analysis revealed that S. torvum reverses DOX-caused structural damage such as tubular necrosis, renal lesions and glomerular congestion (Mohan et al. 2009). The nephro-protective action of phenolic compounds extracted from different parts of S. torvum was also mentioned by Loganayaki et al. (2010).

Novel proteins, with effective nephro-protective activity (Darkwah and Nkoom 2019), even at low doses when compared to well-known synthetic standards (Sivapriya and Srinivas 2007), have been isolated from water extracts of S. torvum seeds.

The nephro-protective action of vitamins C & E present in S. torvum, is due to their antioxidant power which protects molecules from oxidation, i.e. from electron loss. Indeed, their chemical and molecular structure (see Figure 3 for vitamin E) facilitates electron(s) exchange with oxidative compounds that are consequently stabilized. The effectiveness of different vitamins C & E structures can be measured by measuring their nephro-protective potential.

Figure 3. chemical structure of the simplified Vitamin E derivatives from S. torvum. The figure was obtained from (Anna et al. 2016) with permission from springer nature.

Anti-inflammatory and analgesic activity

S. torvum is used in Cameroonian traditional medicine for the management of pain and inflammation (Atta and Alkofahi 1997). It is also used for the treatment of inflammatory related disease such as fever, wounds and tooth decay. Its analgesic activity against writhing and mechanically induced pain has been shown in rats (Atta and Alkofahi 1997; Ndebia et al. 2007). The anti-inflammatory and analgesic properties of aqueous extracts of tannins and phenols are associated to various mechanisms such as inhibition of production of inflammatory mediators like Prostaglandin and Cyclooxygenase, and also the production of Prostaglandin E2 (PGE2) through the arachidonic acid cascade for a critical inflammatory mediation (Ndebia et al. 2007).

Anti-ulcer activity

Anti-ulcer activity of S. torvum leaves was investigated against ethanol, indomethacin, pylorus ligation and cold-restraint stress-induced gastric ulcer in rat (Telesphore et al. 2008). The gastric mucosal protection of S. torvum is mediated through a number of mechanisms that include enhancement of the gastric mucosal defense through increase in mucus and/or bicarbonate production, reduction of the volume of gastric acid secretion or by simply neutralization of the gastric acidity. Flavonoids, sterols and triterpenes have been shown to promote production of bicarbonate which may be responsible for the anti-ulcer properties (Antonio et al. 2004). Fractions of methanolic extracts significantly inhibited ulcer formation (Nguelefack et al. 2008), those containing flavonoids (see Figure 4), and triterpenes being the most active with an inhibitory percentage of 84.7.

Figure 4. Chemical structure of flavonoid derivative. The figure was obtained from (Anna et al. 2012) with permission from springer nature.

Flavonoid derivatives (Figure 4) of S. torvum display anti-ulcer properties, through increase in mucus and neutralization of the acidic content (Anna et al. 2012).

Anti-microbial activity

Several in-vitro studies have described extracts of S. torvum as good sources of anti-microbial, agents (David et al. 1998; Ajaiyeoba 1999; Darkwah 2018). These results confirm the consistency of the medicinal use of this species. Flavonoids, that S. torvum is rich of, have direct anti-bacterial effects due to three mechanisms: (i) Inhibition of nucleic acid synthesis, (ii) inhibition of cytoplasmic membrane function and (iii) Inhibition of energy metabolism (Cushnie and Lamb 2005; Xiao et al. 2013; Xie et al. 2015).

The global anti-viral properties of methanolic extracts of sun-dried fruit of S. torvum, containing alkaloids, flavonoids, saponins, tannins, and glycosides, was demonstrated on human and animal clinical isolates of Herpes Simplex Virus (Travis et al. 2002), however without specifying the respective role of each phytochemical type. Methanolic extracts of S. torvum, tested with the disc diffusion method, have also a significant growth-inhibiting activity against bacteria (Actinomyces pyogenes, Bacillus subtilis, Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, Salmonella species, Staphylococcus aureus, Streptococcus pyogenes) and fungi (Aspergillus niger, Candida albicans) commonly associated with pyogenic infections, and isolated from clinical isolates of humans and animals (Chah et al. 2000; Yousaf et al. 2013; Darkwah 2018; Kaunda and Zhang 2019; Sima Obiang et al. 2019). The minimum extract concentration that inhibited bacterial and fungal activity was 0.31 and 1.25 mg/ml respectively (Wiart et al. 2004). The extract activity is more or less effective depending on the microbes. Tested against Bacillus cereus, B.subtilis, Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus and the fungus Candida albicans, the highest activity was detected against B. cereus (Wiart et al. 2004). The flavonoids and polyphenolic tannins are the phyto-chemicals responsible of the high anti-bacterial and anti-fungal activity of the extracts. The comparison of methanolic extracts of different plant parts has led to the conclusion that the chemical compounds inhibiting microbial activities are more concentrated in the leaves and fruits (Tania et al. 2007).

In addition to the anti-bacterial, anti-viral and anti-fungal activity of S. torvum bioactive compounds, their immuno-modulatory action is also suggested (Kannan et al. 2012). On the whole, it is clear that further studies are needed in order to better determine the metabolites involved, their exact mode of action, including their antioxidant capacity (Arif and Fareed 2011; Kannan et al. 2012; Wannasiri et al. 2017; Innih et al. 2018).

Conclusion

S. torvum phytochemicals display a wide range of biological properties, among which the anti-oxidant capability appears to be central, thus, common to most of them. Reactive oxygen and nitrogen species (ROS/RNS) are central to biochemical processes and represent an essential part of aerobic life and metabolism (Darkwah et al. 2018b). Biological systems are protected from free radical induced cell damage by antioxidants which may be enzymes or non-enzymatic compounds. Most human cells, unlike plant cells, do not generate adequate amounts of antioxidants to be protected against oxidative stress/damage (Harborne 1998; Meda et al. 2005; Pisoschi et al. 2009). Hence antioxidants should be given as supplements, and there is a growing interest for alternative natural and safer sources of antioxidants (Oyaizu 1986; Pavithra and Vadivukkarasi 2015). Plant-sourced natural antioxidants such as vitamins C & E, carotenes, phenolics, flavonoids, phytates and phytoestrogens are believed to interfere with the oxidation process by reacting with free radicals, chelating catalytic metals and scavenging oxygen in biological systems (Boham and Kocipai-Abyazan 1974; Prasad et al. 2010). The interest for phenolics is growing because of their high antioxidant capacity due to ability to pass hydrogen on to extremely reactive radicals, therefore preventing further radical formation (Lapornik et al. 2005; Xu et al. 2007). The wide traditional medicinal use of S. torvum fruits is nowadays explained by the production of many phytochemicals by this species. Alkaloids, flavonoids, tannins, saponins, and glycosides present in S. torvum extracts in sufficient concentrations for protecting the body against oxidative stresses. S. torvum can therefore be considered as a promising natural source of phytochemicals displaying a range of medicinal properties, ranging from cardio-protection & treatment of heart related diseases, nephro-protection, to analgesic, anti-inflammatory, anti-ulcer, and anti-microbial activities. However, the relatively scarce information concerning S. torvum phytochemicals points out the need of acquiring a deeper understanding of their kinds and structures, of their biological actions and of their relations to the medicinal properties of the fruits.

Disclosure statement

No potential conflict of interest was reported by the author(s).