Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname (South America): Part 2

Abstract

The dependence of humans on oxygen for their metabolism, together with their uninterrupted exposure to a wide variety of hazardous environmental chemicals, leads to the continuous formation of reactive oxygen-derived species (ROS) in the body such as superoxide radical anion, hydrogen peroxide, peroxyl radicals, and hydroxyl radical. When in excess, ROS can damage cellular constituents such as DNA and membrane lipids causing oxidative stress, cellular injury, and eventually, inflammatory, neoplastic, diabetic, cardiovascular, neurodegenerative, and age-related diseases. Fortunately, the body has a multitude of naturally occurring antioxidants in dietary fruits and vegetables to its disposal, including polyphenolic compounds, vitamins, and essential minerals. These antioxidants eliminate ROS by acting as reducing agents, hydrogen donors, quenchers of singlet oxygen, or chelators of metal ions that catalyze oxidation reactions, thus decreasing the risk of the above-mentioned diseases. Part 1 of this chapter has comprehensively addressed three representative examples of fruits from the Republic of Suriname (South America) that are rich in the polyphenolics anthocyanins, ellagitannins, and coumarins and has highlighted their antioxidant activity and beneficial and health-promoting effects. This second part deals with four Surinamese fruits with an abundance of (pro)vitamins A, C, and E and selenium in light of their antioxidant activities.

1. Introduction

There is ample evidence that life on our planet has developed under anaerobic conditions [1, 2]. Most organisms that evolved from these primordial predecessors have dealt with the increasing atmospheric levels of oxygen by adapting to oxygen and its derivatives and creating antioxidant defense systems to protect themselves against the toxic effects of these compounds [3, 4]. The most notable toxic byproducts of metabolic reactions involving oxygen are reactive oxygen-derived species (ROS) such as superoxide radical anion, hydrogen peroxide, peroxyl radicals, and hydroxyl radical, as well as non-radical species such as hydrogen peroxide, peroxynitrite, hypochlorous acid, and ozone [5, 6, 7]. Reactive nitrogen species (RNS) such as nitric oxide, peroxynitrite, and nitrogen dioxide radical, as well as reactive chlorine species (RCS) such as hypochlorous acid, are also classified as ROS [5, 6, 7]. ROS are able to readily react with and cause damage to biomolecules including proteins, lipids, and nucleic acids, leading to cell and tissue injury [8, 9, 10]. The high reactivity of ROS derives from the presence of a single unpaired electron in their outer orbit formed as a result of incomplete reduction of the oxygen metabolites [8, 9, 10].

ROS are mainly generated in cellular organelles where oxygen consumption is high, such as mitochondria, peroxisomes, and endoplasmic reticulum [11, 12, 13]. In addition to these endogenous sources, ROS are produced from exogenous sources such as car exhaust, cigarette smoke, and industrial contaminants; peroxides, aldehydes, oxidized fatty acids, and transition metals in foods; a large variety of xenobiotics including toxins, pesticides, and herbicides; as well as various medical drugs such as narcotics, anesthetizing gases, and antineoplastic agents [5, 14, 15]. For example, γ-radiation interacts with water molecules to form water radical cations and free electrons which react with other water molecules to form highly active hydroxyl radical, superoxides, and organic radicals as well as organic hydroperoxides and hydrogen peroxide [16]. And the antitumor antibiotic doxorubicin generates a semiquinone derivative that can autoxidize in the presence of oxygen, producing superoxide anions following electron donation by oxidases such as mitochondrial NADPH and nitric oxide synthases [17]. In all cases, the ROS-induced oxidative stress results in massive damage to cellular macromolecules such as DNA, critical proteins, and membrane lipids, eventually causing, among others, neoplastic, neurodegenerative, cardiovascular, age-related, cerebrovascular, diabetic, and inflammatory diseases [18, 19, 20, 21, 22, 23, 24].

However, as mentioned above, aerobic organisms have developed mechanisms to adapt to and cope with ROS. Major adaptation mechanisms involve the utilization of oxygen and ROS as relay elements in pathways of cell signaling and homeostasis, for various metabolic reactions, to eliminate xenobiotics from the body, and to help destroy phagocytized harmful particles. For instance, ROS, in particular hydrogen peroxide, can act as messengers in the transduction of metabolic and environmental signals which affect diverse intracellular pathways, culminating in the activation of transcription factors and other proteins, controlling their biological activities [9]. A well-investigated example is redox signaling involving the oxidation of cysteine residues of proteins by hydrogen peroxide, converting a thiolate anion in cysteine (Cys-S-) into the sulfenic form (Cys-SOH), causing the protein to undergo allosteric changes that alter its function [25]. Furthermore, the formation of ATP during oxidative phosphorylation in the mitochondria is accompanied by the production of electrons in the electron transport chain for the reduction of molecular oxygen into superoxides which are subsequently transformed into the much less reactive hydrogen peroxide by superoxide dismutase [26]. As well, the addition of oxygen atoms to xenobiotics by cytochrome P450 enzymes increases their water solubility, facilitating their removal from the body [27]. And phagocytized bacteria, bits of necrotic tissue, and foreign particles are intracellularly destroyed by macrophages and neutrophils by the so-called respiratory burst (or oxidative burst), involving the rapid release of superoxides and hydrogen peroxide following the supply of electrons by NADPH [28].

Critical mechanisms of aerobic organisms to cope with ROS involve the use of endogenous and exogenous defense systems that counter their detrimental effects. The endogenous defenses comprise enzymatic antioxidant systems such as superoxide dismutase, catalase, and glutathione peroxidase [29] and nonenzymatic mechanisms such as bilirubin and albumin [30]. The exogenous defenses complement the endogenous mechanisms and consist of antioxidants in fruits and vegetables provided through the diet [31] and include, among others, various phenolic compounds, vitamins, essential minerals, small peptides, and fatty acids [32, 33]. Like the exogenous mechanisms, the endogenous defenses prevent the formation of ROS through various mechanmsm [29, 30, 31, 33, 34]. A multitude of studies have validated the critical role of exogenous dietary antioxidants in our well-being (see, for instance, references [31, 32]). This has resulted in the recommendation of diets high in fruits and vegetables that are rich in these compounds to decrease the risk of developing the above-mentioned degenerative diseases [35, 36, 37]. The first part of this chapter provided some background information about the role of naturally occurring antioxidants as exogenous antioxidant defenses, gave some background on the Republic of Suriname, then comprehensively addressed three representative examples of well-known Surinamese fruits that are rich in the polyphenolic compounds anthocyanins, ellagitannins, and coumarins, highlighting the involvement of these naturally occurring antioxidants in the beneficial and health-promoting effects of the fruits. This second part of the chapter continues with a comprehensive overview of four additional popular Surinamese plants with an abundance of (pro)vitamins A, C, or E, or selenium, and equally extensively addresses the contribution of these antioxidants to the favorable effects of the fruits on human health.

2. (Pro)vitamins A, C, and/or E, and selenium in four well-known Surinamese fruits

Like the three Surinamese fruits that have in detail been addressed in the first part of this chapter, the four fruits dealt with in this part are abundantly cultivated and traded in Suriname [38], consumed as foods and/or nutritional supplements [38], and/or used as traditional cosmeceuticals [39] and/or medicines [40, 41, 42, 43, 44, 45, 46, 47, 48, 49]. The plants addressed in both parts of this chapter as well as their relevant characteristics are given in Table 1.

Main antioxidants	Plant family	Plant species (common vernacular; Surinamese vernacular)	Main traditional uses	Main commercialized products
Phenolic compounds—anthocyanins	Arecaceae	Euterpe oleracea Mart. (açai; podosiri)	Anemia; hypotension; wounds; as an external contraceptive	Health-promoting supplements and nutraceuticals
Phenolic compounds—ellagitannins	Lythraceae	Punica granatum L. (pomegranate; granaatappel)	Sore throat; respiratory afflictions; wounds and hemorrhages; gastrointestinal disorders; menstrual problems	Ellagitannin-enriched dietary supplements
Phenolic compounds—coumarins	Fabaceae	Dipteryx odorata (Aubl.) Willd (tonka bean; tonkaboon)	Hair conditions; colds and fever; respiratory disorders; gastrointestinal disorders; menstrual problems; as an aphrodisiac	Hair care
Vitamins—vitamin A	Arecaceae	Astrocaryum vulgare Mart. (tucuma; awara)	Colicky babies; respiratory diseases; gastrointestinal disorders; rheumatism; pains; skin and hair problems; wounds; fractured bones; sexual underperformance and infertility	Skin and hair care
Vitamins—vitamin C	Malpighiaceae	Malpighia glabra L. (acerola; West-Indische kers)	Respiratory diseases; maladies of the oral cavity; cardiovascular ailments; wounds; gastrointestinal disorders; depression; cancer	Vitamin C-enriched dietary supplements and other health products
Vitamins—vitamin E	Malvaceae	Hibiscus sabdariffa L. (roselle; syuru)	Microbial infections; respiratory diseases; kidney problems; gastrointestinal disorders; hypertension	Skin and hair care; wound healing
Antioxidant minerals—selenium	Lecythidaceae	Bertholletia excelsa Humb. & Bonpl. (Brazil nut; paranoto)	Gastrointestinal disorders; burns	Skin and hair care

Table 1.

Main antioxidant compounds, traditional uses, and commercialized products of seven Surinamese types of fruits.

2.1 Antioxidant vitamins

Vitamins are essential organic compounds that must be obtained from the diet and are required in minute amounts for: supporting normal growth, development, and reproduction; fortifying the immune system and fighting infections; proper wound healing; strengthening bones, ligaments, muscles, teeth, and nails; regulating hormones; and processing of energy in cells [50]. Insufficient intake of vitamins may cause deficiency diseases such as xerophthalmia, scurvy, beri-beri, and pellagra (particularly in developing countries [50]), but resupplying these nutrients can help ease the symptoms of these conditions [50].

Vitamins can be divided into fat-soluble compounds (vitamins A, D, E, and K) [50, 51] and water-soluble compounds such as vitamins of the B complex (vitamins B₁, B₂, B₃, B₅, B₆, B₉, B₁₂, and biotin) as well as vitamin C [50, 52]. The fat-soluble vitamins dissolve in fat before they are absorbed in the bloodstream to carry out their functions [50, 51]. Excesses of these vitamins are stored in the liver and fatty tissues; for this reason, they are not needed in the daily diet [50, 51]. Notably, excessive intake of fat-soluble vitamins may lead to toxicity and potential health problems [50, 51]. Water-soluble vitamins dissolve in water and are not stored in the body and must therefore be acquired via the daily diet [50, 52]. Unlike the fat-soluble vitamins, excessive intake of water-soluble vitamins is readily eliminated in the urine and does not cause health problems [50, 52].

Apart from the functions mentioned in the preceding paragraph, vitamins function as antioxidants [53, 54]. The best studied antioxidant vitamins are (pro)vitamin A, vitamin C, and vitamin E; other vitamins such as vitamin K, vitamin D, vitamin B₂, vitamin B₃, and vitamin B₆ have not adequately been evaluated for their antioxidant potential [54]. Vitamin C is able to quench ROS by donating electrons to them; vitamin D inhibits ROS generation, preventing lipid peroxidation of cellular membranes; and vitamin A reacts with peroxyl, hydroxyl, and superoxide radicals [53, 54].

2.1.1 Antioxidant vitamins: Vitamin A: Astrocaryum vulgare Mart. (Arecaceae)

Vitamin A is the collective name of a group of fat-soluble organic compounds which are essential for humans (and other vertebrates) and comprise vitamin A alcohols (retinols), vitamin A aldehydes (retinals), retinyl acids (retinoic acids), and retinyl esters [55, 56]. All-trans-retinol is the primary homeostatically regulated vitamin A species in the body, all-trans-retinal and 11-cis-retinal are vitamin A derivatives involved in photoperception, and retinyl esters like retinyl palmitate are the storage form of vitamin A in mainly the liver [55, 56]. Preformed vitamins A are provided by consuming animal products such as meat, fish, poultry, and dairy foods, either as retinol or bound to a fatty acid to become a retinyl ester [57]. The body can also synthesize the preformed vitamins A from provitamin A carotenoids including carotenes such as α- and β-carotene and the xanthophyll β-cryptoxanthin [58]. This mainly occurs in the mucosa of the terminal small intestine using the enzyme β-carotene 15-15′-oxygenase [58]. Conversely, non-provitamin A carotenoids such as the carotene lycopene and the xanthophylls lutein and zeaxanthin cannot be converted into retinol and other preformed vitamins A [55, 56]. Carotenoids are bright yellow-, red-, or orange-colored and are found in, among others, mango, grapefruit, watermelon, papaya, tomato, tangerine, and guava, as well as carrot and yellow corn [57]. The recommended dietary allowance for men and women is 900 and 700 μg retinol activity equivalents, respectively, per day [59].

Vitamins A are involved, among others, in cell growth and fetal development; male and female reproductive health; the condition of surface tissues such as skin, intestines, lungs, bladder, and inner ear; the growth and distribution of T cells and in this way, immune function; and the health of cornea and conjunctiva as well as the capacity of both low-light vision and color vision [55, 56]. These functions and most of vitamins A’s biological effects are carried out following its binding to and activation of the nuclear retinoic acid receptors RARα, RARβ, and RARγ [60]. Chronic shortages of vitamins A and/or carotenoids in the diet result in vitamin A deficiency that typically manifests as night blindness and dry skin, and if prolonged and severe, can even lead to total and irreversible blindness [56].

Vitamins A may also help protect the body from oxidative stress. This is supported by the results from in vitro studies indicating that retinoic acid inhibited the activity of thioredoxin-interacting protein [61], an enyme known to bind to and inhibit the activity of ubiquitous cytosolic and mitochondrial antioxidant oxidase-reductase enzymes called thioredoxins [62]. Furthermore, retinoic acid upregulated the expression of antioxidant-related genes [63] and increased superoxide dismutase and glutathione transferase activities while decreasing those of malondialdehyde and ROS [64].

Experimental data on the antioxidant properties of carotenoids—both carotenes and xanthophylls—are more compelling [65, 66], showing that these compounds efficiently quenched singlet molecular oxygen and potently scavenged other ROS such as peroxyl radicals [67, 68, 69, 70, 71]. Not surprisingly, diets high in carotenoids have been associated with a lower risk of, among others, heart disease, lung cancer, and diabetes mellitus [72, 73, 74]. However, it should be taken into account that the elimination of ROS by carotenoids may be accompanied by the formation of several potentially harmful pro-oxidant carotenoid radical derivatives [75]. For instance, carotenoid radical cations may oxidize the tyrosine and cysteine moieties of cellular proteins, damaging their structure and impairing their function [76].

A well-known source of vitamin A in Suriname is the fruit of the tucuma or awara Astrocaryum vulgare Mart. (Arecaceae). A. vulgare is a multi-stemmed, spiny, evergreen, feather palm that can be found in the forested parts, savannas, and lowlands of the country but is also cultivated for its edible fruit that is produced in clusters on the tree. A. vulgare grows in a small bunch of unbranched stems of 10–20 cm in diameter which can reach a height of 4–10 m and are covered with black spines of about 2 cm long. The fruit is globose to ovoid, 35–45 mm long and 25–35 mm wide, and consists of a fleshy orange-red, fatty mesocarp (pulp) that covers a single large seed (Figure 1). The mesocarp is slightly sweet and has a flavor reminiscent of apricots and is very nutritious, containing a relatively high concentration of carotenoids with a very high concentration of β-carotene (about 52 mg per 100 g), in addition to appreciable amounts of vitamin E, vitamin B₂ (riboflavin), as well as carbohydrates, proteins, and saturated fatty acids (such as oleic acid and palmitic acid), and polyunsaturated fatty acids (such as omega-3, omega-6, and omega-9 fatty acids) [77, 78].

Figure 1.

Fruits of the tucumã Astrocaryum vulgare Mart. (Arecaceae) (from: https://images.app.goo.gl/ohwh8G8BwHZBiUk8A).

A. vulgare fruit is eaten raw, prepared into juices, and used as an indispensable ingredient of the very popular French Guianan dish “bouillon d’awara” that is traditionally eaten during Easter. Cold-pressing of the mesocarp gives tucuma oil, and cold-pressing of the hard, white endosperm from the rigid, black seed gives tucuma butter that has an unusually high concentration of the fatty acid lauric acid in addition to myristic acid and oleic acid [79, 80]. Both tucuma oil and tucuma butter are edible and suitable for cooking and also for preparing nourishing and moisturizing beauty products, anti-aging creams, soaps, body lotions, and products for damaged hair [80, 81]. And the immature endosperm gives a juice called vino de tucuma that is used for preparing tasty beverages and culinary delicacies.

Preparations from the mesocarp of A. vulgare fruit are traditionally used to replenish vitamin A deficiency in individuals suffering from xerophthalmia, to calm colicky babies, and to treat coughs and as a breath freshener [78, 82]. The seed oil is used as a laxative, for treating rheumatism, pain, earache, as a topical diaphoretic to stimulate perspiration in patients with fever, and as an ingredient of treatments of furuncles [78, 82]. In Suriname’s traditional medicine, preparations from several parts of the fruit are used for skin care, to repair damaged hair, against coughing, as an ingredient of dressings for open wounds and fractured bones, against fleas and lice, for treating impotence, and to prevent miscarriage and increase fertility [43, 49].

Some of these uses may be related to the antioxidant activities of the constituents of A. vulgare mesocarp including β-carotene. This could be derived from the anti-inflammatory properties of the pulp oil in both acute and chronic in vivo models of inflammation which could be localized to an unsaponifiable fraction [83, 84] that displayed antioxidant effects in cultured J774 macrophages activated by lipopolysaccharide plus interferon-γ, as well as an animal model of endotoxic shock resulting from the systemic release of inflammatory mediators [83, 84]. However, this fraction contained not only carotenoids but also phytosterols as well as vitamin E derivatives [83, 84, 85] which have been shown to be partly responsible for the biological properties of vegetable oils [86]. This suggests that the beneficial effects and traditional uses of A. vulgare should be credited to its contents of other antioxidant compounds in addition to provitamins A and/or vitamins A.

2.1.2 Antioxidant vitamins: vitamin C: Malpighia glabra L. (Malpighiaceae)

Ascorbic acid, more precisely, L-ascorbic acid, also known as vitamin C, is a water-soluble vitamin that is essential for: the formation and repair of collagen required for, among others, skin, tendons, ligaments, and blood vessels; the healing of wounds and the formation of scar tissue; the repair and maintenance of cartilage, bones, and teeth; carnitine and catecholamine metabolism; the maintenance of a healthy immune system; and the resorption of dietary iron into the body [87, 88]. As a result, vitamin C deficiency leads to impaired collagen synthesis, scurvy, impaired healing of wounds and fractured bones, bleeding gums, achy joints, tiredness, an increased susceptibility to viral infections, skin issues, an increased risk of soft tissue infections with potentially lethal complications, and a decline of general health [87, 88].

Humans as well as primates and a few other animals such as guinea pigs lack the ability to synthesize vitamin C due to the absence of L-gulono-1,4-lactone oxidase, the enzyme that catalyzes the conversion of L-gulonolactone into vitamin C [89]. For this reason, humans depend on the regular intake of vitamin C through the diet in sufficient amounts to prevent the above-mentioned diseases [90]. This is readily achieved by consuming fruits that contain relatively high levels of vitamin C such as strawberries, citrus fruits, watermelon, berries, pineapple, kiwi fruits, mangoes, and tomatoes as well as cherries [91, 92].

Many of the health-promoting effects of vitamin C have been attributed—directly or indirectly—to its notable antioxidant activity. This held true for, for instance, its strong anti-inflammatory and antihistaminic activity and its ability to inhibit several types of inflammatory mediators such as tumor necrosis factor-α [93]; its inhibitory effects on signaling for lipopolysaccharide formation and ROS production during infection [94]; its anti-aging effect due to the stimulation of collagen formation and the protection of particularly elastin from ROS-mediated damage [95]; and its cytotoxicity (in mega-doses) against cancer [96, 97], and perhaps also against diabetes mellitus, cardiovascular ailments, metabolic syndrome, and ocular diseases [98, 99, 100, 101]. All these beneficial effects have been associated with vitamin C’s capacity to generate cytotoxic ascorbyl radicals which do not harm normal cells [102], its antibacterial effects due to its ability to neutralize bacterial endotoxins [102] and impede bacterial replication [103]; and its immune-stimulatory properties by promoting the phagocytic properties of neutrophils and macrophages, the production and titer of antibodies, and the activity of lymphocytes [104].

Vitamin C elicits its antioxidant effects by acting as a reducing agent, donating an electron to potentially harmful ROS such as hydroxyl radical, hydrogen peroxide, and singlet oxygen, and scavenging these species and preventing them from inflicting oxidative damage to lipids and other macromolecules [105, 106]. At the same time, vitamin C is oxidized to a relatively stable, unreactive ascorbyl-free radical (semi-dehydrovitamin C) with a lifetime of 10–15 s [107, 108]. In a subsequent electron-donating reaction, semi-dehydroascorbic acid is transformed into a dehydroascorbic acid that is also relatively stable and lasts for a few minutes [87, 107, 108]. These properties of the vitamin C metabolites render them harmless to surrounding cells [87, 107, 108]. Apart from eliminating ROS, vitamin C protects cells from oxidative stress-induced damage by vitamin E-dependent neutralization of lipid hydroperoxyl radicals in a one-electron reduction reaction via the vitamin E redox cycle, regenerating the antioxidant form of vitamin E (α-tocopherol) by reducing tocopheroxyl radicals [109, 110]. However, there are reports mentioning that vitamin C can also act as a pro-oxidant at relatively low doses [111].

The acerola, also known as Barbados cherry and West Indian cherry (or West-Indische kers in Suriname), with the scientific names M. glabra L., Malpighia punicifolia L., and Malpighia emarginata DC. (Malpighiaceae), is a small tree with spreading, somewhat drooping branches on a short trunk that usually grows to a height of 2–3 m. It is indigenous to the area ranging from Central America and Mexico to the Caribbean and the northern parts of South America including Suriname. M. glabra fruit is ovoid, bright red-colored, sweet- to somewhat acid-tasting, has a diameter of 10–35 mm (Figure 2), and can be eaten raw, cooked, stewed, and made into juices, sauces, jellies, jams, wines, or purees. Because the fruit rapidly deteriorates, it is immediately after harvesting processed into pulp and clarified juice which are frozen and stored for later use. The global market for these products is enormous and is estimated to reach USD 17.5 billion by 2026, with Brazil as the major producer and exporter [112].

Figure 2.

Fruit of the acerola Malpighia glabra L. (Malpighiaceae) (from: https://images.app.goo.gl/SXvp1ifwFFRWLmTU7).

M. glabra fruit is also traditionally used against flu, colds, sore throat, coughing, and hay fever; to prevent scurvy and treat gum infections as well as tooth decay; to avert heart disease and treat atherosclerosis and blood clots; against various types of wounds ranging from pimples to pressure sores; for remedying gastrointestinal problems; as an antidepressant; and for treating cancer [49, 113]. M. glabra fruit has been used to produce vitamin C concentrates, dietary supplements, and in the enrichment of other processed health products [114]. Pharmacological studies with preparations from M. glabra fruit extracts showed, among others, anti-inflammatory, antihyperglycemic, antitumor, antigenotoxic, and hepatoprotective activity [115, 116, 117, 118].

The beneficial health effects of M. glabra fruit have been associated with its powerful antioxidant effects in several in vitro assays [119, 120, 121] which, in their turn, have been attributed to its abundant amount of vitamin C as well as phenolic compounds (including benzoic acid derivatives, phenylpropanoid derivatives, flavonoids, and anthocyanins) and carotenoids [114, 122, 123, 124, 125]. Notably, the vitamin C content of M. glabra fruit is 1000–4500 mg per 100 g, which is 50–100 times that of an orange or a lemon [125]. When considering that the recommended dietary allowances of vitamin C are 75 mg/day for women and 90 mg/day for men [126], the consumption of three M. glabra fruits per day would satisfy the required daily vitamin C intake for an adult [127].

Several investigators also reported that M. glabra fruit extracts displayed a relatively high total phenolic content and in vitro antioxidant activity which correlated well with each other [114, 125, 128, 129, 130]. Thus, the remarkable antioxidant activity of M. glabra fruit is most probably not only attributable to its relatively high content of vitamin C but also to phenolic phytonutrients with antioxidant activity which may act synergistically with vitamin C [123]. Indeed, the contribution of vitamin C to the hydrophilic antioxidant activity in M. glabra fruit, commercial pulps, and juices ranged from 40 to 83%, while the remaining activity was due to phenolic compounds, mainly phenolic acids [123]. And the antioxidant activity of M. glabra fruit juices depended on the synergistic action of the constituents of different fractions, with most significant components being phenolic compounds and vitamin C [122].

2.1.3 Antioxidant vitamins: vitamin E: Hibiscus sabdariffa L. (Malvaceae)

In its broadest sense, vitamin E is a collective term of a group of lipid-soluble compounds called tocochromanols which are present in fat-containing foods [131]. Vitamins E can be divided into tocopherols and tocotrienols, which in their turn, can be subdivided into eight naturally occurring forms, namely the α, β, γ, and δ classes of tocopherol and tocotrienol [131, 132]. All these derivatives are synthesized by plants from the phenolic acid homogentisic acid [131]. The major form of vitamin E used by the human body is α-tocopherol [132]. The richest dietary sources of α-tocopherol are nuts and seeds such as dry roasted peanuts, almonds, and hazelnuts (2.2–6.8 mg per serving); green leafy vegetables such as spinach (0.6 mg per serving); fruits such as mango, tomato, and kiwi (0.7–1.1 mg per serving); as well as edible vegetable oils such as sunflower oil and wheat germ oil (5.6–20.3 mg per serving) [133]. The recommended dietary allowance for α-tocopherol for individuals aged 14 years and older including pregnant women is 15 mg per day [134]. Breast feeding women need slightly more of this compound, namely 19 mg or 28 IU daily [134].

α-Tocopherol is involved in various important functions in the body, including maintaining the proper organization of and repairing damage to cellular membranes [135, 136, 137]; the inhibition of platelet aggregation by promoting the release of prostacyclin from the endothelium, decreasing the adhesion of blood cell components to the endothelium [138], stimulating phospholipase A2 and cyclooxygenase-1 activities and the subsequent release of prostacyclin [139]; and inhibiting nitric oxide synthase activation [140].

These properties of α-tocopherol are for an important part attributable to its potent activity against ROS-mediated lipid peroxidation [141]. Indeed, α-tocopherol appeared to be a powerful chain-breaking antioxidant that inhibits the production of ROS when lipids undergo oxidation and during the propagation of free radical reactions [142]. Not surprisingly, it is primarily located in cellular membranes (such as the membranes of the mitochondria and endoplasmic reticulum in heart and lungs) where it acts as the first line of defense against lipid peroxidation [141]. Due to its peroxyl radical-scavenging activity, α-tocopherol also protects the polyunsaturated fatty acids in membrane phospholipids and plasma lipoproteins [143]. As a result, α-tocopherol has been associated with the prevention of, among others, neurological disorders, cardiovascular diseases, cancer, aging, arthritis, age-related eye and skin damage, and infertility [144, 145]. Because it is able to inhibit air oxidation, it is also used to fortify and extend the lifetime of foods, oils, and industrial materials [146].

The roselle or syuru H. sabdariffa L. (Malvaceae) is an erect, branched, annual to perennial plant with a woody stem that grows to an average height of 2–2.5 m. It probably originates from India and the adjoining regions and has been introduced into Africa, from where enslaved Africans have brought it to the new World including Suriname [147]. H. sabdariffa is now cultivated in many tropical countries, mostly for its conspicuously crimson red-colored fleshy calyces (Figure 3), which develop from white to pale yellow flowers, each petal of which has a dark red spot at the base. The dried calyces taste like cranberry and are used to prepare a variety of teas, jams, sauces, and even beer [41, 45, 46].

Figure 3.

Calyx of the roselle Hibiscus sabdariffa L. (Malvaceae) (from: https://images.app.goo.gl/5M5iBiBb4nHwcTFk6).

The calyx contains a number of constituents with known antioxidant activity, including phenolic acids, a number of anthocyanins, β-carotene, ascorbic acid, as well as α-tocopherol and other tocopherols [148, 149, 150, 151]. Due to this favorable phytochemical composition, extracts from H. sabdariffa calyx have been included in skin care products, skin-protecting agents, anti-aging creams, and hair care products [152]. Furthermore, a polysaccharide-enriched crude extract from H. sabdariffa flower potently stimulated the proliferation of cultured keratinocytes [153], which may explain the addition of these preparations to H. sabdariffa skin care products. As well, a water in oil cream of the methanol extract of the calyces has been prepared as a potential commercial wound healing substance [154, 155]. Preparations from H. sabdariffa calyx are also traditionally used in various countries including Suriname, for treating a broad range of conditions such as microbial infections, cough and bronchitis, kidney problems, various gastrointestinal conditions, and hypertension [49, 151, 156, 157].

It is likely that some of these uses can be attributed to the antioxidant activity of H. sabdariffa calyx [158, 159]. For instance, the antioxidant activity of calyx preparations has been held responsible for their efficacy against bacterial infections [149, 151, 158, 160]. And the regular use of H. sabdariffa calyx preparations would decrease the oxidative stress involved in the development of atherosclerosis, lipid disorders, and hypertension [161]. Indeed, aqueous and alcoholic extracts of the (dried) calyx elicited appreciable antioxidant activities in various in vitro assays [158, 159, 162, 163]. However, the antioxidant activity has not only been associated with α-tocopherol [163] but also with various types of phenolic compounds such as anthocyanins [163, 164, 165] and phenolic acids such as protocatechuic acid [160]. Thus, as may hold true for A. vulgare and M. glabra fruit, the benefical effcts of H. sabdariffa calyx preparations also seem attributable to multiple bioactive phytochemicals rather than only one compound, in the present case, vitamin E.

2.2 Antioxidant minerals

Minerals are inorganic substances that are present in all body tissues and fluids, and although not yielding energy, are necessary for the maintenance and the progression of many physicochemical processes which are essential to life [166, 167, 168]. They can be classified into macroelements, microelements, and trace elements [166, 167, 168]. The macroelements comprise elements which are abundantly found in nature and which the body needs in relatively large amounts (in excess of 100 mg/dL), and they include hydrogen, oxygen, carbon, nitrogen, calcium, and phosphorus [166, 167, 168]. These compounds comprise together about 99% of the body mass, are present in most tissues and organs, represent the most important constituents of DNA, enzymes, cellular membranes, as well as inter- and intracellular liquids, and are essential for almost all metabolic processes [166, 167, 168]. Microelements are required in the body in relatively modest amounts (less than 100 mg/dL), only comprise 0.85% of the body mass, and include potassium, sulfur, sodium, chlorine, and magnesium [166, 167, 168]. They fulfill more or less the same functions as the macroelements but are required in smaller amounts [166, 167, 168].

Trace elements are present in the body at concentrations of much less than 0.1% and are required in parts per million [166, 167, 168]. Nevertheless, in these minute amounts, they are vital for proper growth and development and are therefore also referred to as essential minerals [166, 167, 168]. They include, among others, iron, copper, zinc, molybdenum, manganese, chromium, cobalt, cadmium, and selenium [166, 167, 168]. Iron, copper, zinc, manganese, and selenium are indirectly involved in the body’s antioxidant defenses by enhancing the activities of antioxidant enzymes (see, for instance, reference [169]). And copper, zinc, and manganese are cofactors of superoxide dismutase [170]. Similarly to vitamins, essential minerals must be acquired through the diet, and deficiencies may occur because of inadequate diets [166, 167, 168].

2.2.1 Antioxidant minerals: selenium: Bertholletia excelsa Humb. and Bonpl. (Lecythidaceae)

Selenium is a trace element that is essential for many functions in humans, particularly as part of innate antioxidant defense mechanisms [166, 167, 168]. It is present in soils as inorganic selenites and selenates which are accumulated and converted by plants into the amino acids selenocysteine and selenomethionine and their methylated derivatives [171, 172]. On the basis of the amount of selenium plants accumulate inside their cells, they can be classified as hyperaccumulators, secondary accumulators, and non-accumulators [173]. These groups of plants accumulate selenium at concentrations in excess of 1000 mg, 100–1000 mg, and less than 100 mg, respectively, per kilogram dry weight [173]. The precise functions of selenium in plants is still controversial, but at low doses it seems to protect plants from a variety of abiotic stresses such as cold, drought, desiccation, and metal stress [174].

Humans do not synthesize selenocysteine and selenomethionine de novo but obtain them from dietary sources such as the Brazil nut Bertholletia excelsa Humb. & Bonpl. (Lecythidaceae), grains, wheat, and corn used for bread and cereals, as well as poultry, eggs, animal meats, sea food, and dairy products [175, 176]. These amino acids are, in their turn, constituents of selenoproteins such as glutathione peroxidases, thyroid hormone deiodinases, and thioredoxin reductases, in which selelenium acts as the catalytic center (see, for instance, references [177, 178]). Skeletal muscle is the major site of selenium storage, accounting for approximately 28–46% of the total selenium pool in the body [179]. There are more than two dozen selenoproteins, and they play vital roles in reproduction, thyroid hormone metabolism, DNA synthesis, and protection from oxidative damage and infection [180].

The recommended dietary allowance for selenium for adult men and women is 55 μg daily [181]. The amount of selenium in soil and groundwater is a major determinant of the amount of selenium in plant-based foods (as well sources of foods from animals feeding on these plants [176, 182]). As a result, selenium concentrations in plant-based foods often vary widely by geographic location [183], which may lead to either deficiencies or toxicities. Severe selenium deficiency (7–11 μg/dL) may occur in areas with soils poor in selenium and can lead to a congestive cardiac myopathy called Keshan disease after Keshan County in north-eastern China where it was first described [184]; Kashin-Beck disease, a chronic, endemic osteochondropathy with joint necrosis that has mainly been seen in some Eastern parts of Eurasia [185]; and myxedematous endemic cretinism and mental retardation caused by thyroid atrophy that is highly prevalent in Central Africa [186]. On the other hand, excess selenium (>100μg/dL) may cause selenosis, manifesting as hair loss, white blotchy nails, a garlic breath, gastrointestinal disorders, fatigue, irritability, and neurological damage [187].

The selenium taken up in the body—in the form of organic selenium (as selenocysteine and selenomethionine) and inorganic selenium (in general as selenite and selenite)—is used for the biosynthesis of selenium-containing proteins [188, 189, 190]. As mentioned above, selenoproteins are crucial to, among others, reproduction, thyroid hormone metabolism, DNA synthesis, immune function, and the protection of cells from oxidative damage, inflammation, and cancer [169, 182, 191, 192]. Particularly the critical association of glutathione peroxidases with the innate antioxidant defense mechanisms has meticulously been investigated, and the involvement of these enzymes in the protection against oxidative stress has now been well established [178, 192, 193]. These cytosolic enzymes appeared to catalyze the reduction of hydrogen peroxide to water and oxygen and that of peroxide radicals to alcohols and oxygen, inhibiting DNA damage and the development of cancer [178, 192, 193]. Notably, the beneficial health effects of selenium (as part of selenoproteins) because of its notable antioxidant activity have been supported by the results from varous clinical studies with patients suffering from coronary heart disease [194], cancer [195], and cognitive disorders [196].

The Brazil nut (or paranoto in Surinamese) B. excelsa is native to the northern parts of South America and is one of the largest and longest-living trees in the Amazon rainforest, reaching ages of 500 years or more. It can achieve a height of 50 m and a trunk diameter of 1–2 m and has grayish and smooth bark. It produces small, greenish-white flowers in panicles which must be pollinated by specific bee genera in order to develop into fruits. B. excelsa fruit is rigid and heavy, weighing as much as 2 kg (Figure 4), and contains 8–24 wedge-shaped edible seeds of 4–5 cm long (the so-called “Brazil nuts”) which are packed like the segments of an orange and are encapsulated by a woody shell of 8–12 mm thickness.

Figure 4.

Fruit of the Brazil nut Bertholletia excelsa Humb. & Bonpl. (Lecythidaceae) (from: https://images.app.goo.gl/Ju62ZypEttADRQVH8).

B. excelsa fruit is rich in dietary fiber, vitamins, and dietary minerals and has been a staple diet of the natives residing in the Amazon forest since the Upper Paleolithic era, 11,000 years ago [197]. It also has a long history of traditional use. For instance, a tea prepared of the seed husks would alleviate stomach aches and other gastrointestinal complaints, the oil from the seed is applied to burns, and a decoction of the stembark would cure liver disorders [48]. Currently, the seeds are commercially harvested from the wild for inclusion into mixed nuts and confections coated with chocolate [197]. The oil extracted from the seeds contains 75% unsaturated fatty acids mainly composed of oleic and linoleic acids, as well as phytosterols, several phenolic compounds such as gallic acid and ellagic acid, tocopherols, and selenium [198, 199, 200]. It is used in creams, lotions, conditioners, and hair care products, as well as formulations for alleviating dry, flaky skin, aging skin, acne, and skin inflammation. These applications may be supported by the moisturizing effects of the fatty acids [200, 201].

As a selenium hyperaccumulator [173], selenium levels of B. excelsa seed are remarkably high, with one nut of on average 5 g containing on average 96 μg selenium, i.e., more than the recommended dietary allowance of 55 μg daily [181]. In fact, despite considerable variations within batches of the amount of selenium [202], the Brazil nut is considered one of the richest natural sources of selenium [203]. Not surprisingly, many of the positive effects of B. excelsa fruit preparations have been attributed to its high selenium content and antioxiodant activity. Indeed, the consumption of B. excelsa fruit would improve antioxidant status in humans through increased levels of selenium and/or glutathione peroxidase activity in plasma, serum, whole blood, and/or erythrocytes [204] and would decrease the risk of overweight/obesity and various degenerative diseases such as cardiovascular, neoplastic, and cognitive disorders [205, 206]. However, several studies with the whole fruit of B. excelsa, parts of the fruit, and products derived from the fruit such as “Brazil nut milk,” a cake fraction, and a fat fraction, showed appreciable antioxidant activity in various in vitro assays, as well as the presence of phenolic compounds, tocopherols, and a high level of selenium [200, 207]. Thus, when considering all the phytochemical constituents with antioxidant properties identified in B. excelsa seed [181, 198, 199, 200], its beneficial health effects may also be attributable to the combined effects of selenium, phenolic compounds, tocopherols, and unsaturated fatty acids.

3. Concluding remarks

Naturally occurring antioxidants in fruits and vegetables provided through the diet represent vital components of the exogenous defense mechanisms of the body to manage oxidative stress caused by ROS, minimizing the chances of developing, among others, inflammatory disorders, cancer, diabetes mellitus, cardiovascular diseases, and cognitive ailments. Important classes of such naturally occurring antioxidants are anthocyanins, ellagitannins, coumarins, (pro)vitamins A, C, and E, as well as selenium. In this chapter, seven well-known Surinamese fruits, each of which known to contain one of these compounds at appreciably high concentrations, have elaborately been dealt with. The fruits were those from the açai palm E. oleracea, the pomegranate Punica granatum, the tonka bean D. odorata, the tucumã A. vulgare, the acerola M. glabra, the roselle H. sabdariffa, and the Brazil nut B. excelsa, respectively. These fruits are widely consumed in Suriname and various other countries throughout the world, either raw or incorporated into dishes, or prepared into traditional medicines, food additives, nutraceuticals, or cosmeceuticals. Numerous pharmacological studies with a wide range of assays have provided support that these beneficial health effects are associated with the powerful antioxiodant activities of one or more of the phytochemical classes mentioned above.

However, many studies have also suggested that the antioxidant activities of the fruits must probably be attributed to the combined effects of several classes of biologically active compounds rather than to one specific phytochemical. For instance, the antioxidant activity of A. vulgare mesocarp [83, 84] may be partly ascribed to phytosterols and vitamin E derivatives in addition to its high content of carotenoids [83, 84]. And those of B. excelsa seed preparations [204, 205, 206] might be due to the combined actions of selenium with phenolic compounds, tocopherols, and unsaturated fatty acids [181, 198, 199, 200]. And as mentioned in part 1 of this chapter, the antioxidant activities of products from the fruit pulp of the açai or podosiri Euterpe oleracea Mart. (Arecaceae) [208, 209] is presumably not only due to its high content of mainly the anthocyanin cyanidin-3-glucoside, but also to other phenolic compounds, vitamins, and/or fatty acids [208, 210, 211, 212].

These considerations indicate the need to more precisely identify the pharmacologically active phytochemicals, particularly those with antioxidant activity, in raw natural products, traditional medicines, and commercial plant-based products with purported health benefical properties. This is the more important in the case of substances containing chemically instable ingredients such as anthocyanins [209, 213, 214, 215, 216, 217, 218], and those that may generate pro-oxidant radical species such as carotenoids [75, 76] or display pro-oxidant properties at, for instance, relatively low concentration such as vitamin C [111].