Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname (South America): Part 1

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 abovementioned diseases. This first part of the current chapter comprehensively addresses three representative examples of fruits from the Republic of Suriname (South America) that are rich in anthocyanins, ellagitannins, and coumarins and highlights their antioxidant activity and beneficial and health-promoting effects. In part 2, four Surinamese fruits with an abundance of (pro)vitamins A, C, and E and selenium are equally extensively dealt with 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, as well as nonradical 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 radicals, 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 nicotinamide adenine dinucleotide phosphate (NADPH) and nitric oxide synthases [17]. In all the 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 adenosine triphosphate (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 that are subsequently transformed into the much less reactive hydrogen peroxide by superoxide dismutase [26]. In addition, 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 mechanisms [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, [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 abovementioned degenerative diseases [35, 36, 37]. The first part of this chapter provides some information about the role of naturally occurring antioxidants as exogenous antioxidant defenses, gives some background on the Republic of Suriname, and then comprehensively addresses three representative examples of well-known Surinamese fruits that are rich in the polyphenolic compounds, such as anthocyanins, ellagitannins, and coumarins, highlighting the involvement of these naturally occurring antioxidants in the beneficial and health-promoting effects of the fruits. The 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. Exogenous antioxidant defenses: naturally occurring antioxidants

As mentioned in the previous section, whether oxidative stress and cellular damage occurs is determined by the net result of the production of ROS and their elimination by antioxidant defenses. Indeed, oxidative stress is a consequence of “a disturbance in the pro-oxidant to antioxidant balance in favor of the former, leading to potential damage” [15]. Both the endogenous and the exogenous antioxidant defenses prevent ROS from overwhelming the intracellular environment by interrupting their propagation, scavenging them, removing their intermediates in redox reactions, inhibiting oxidation reactions that generate them, and repairing oxidized molecules [29, 30, 31, 33, 34, 38]. Exogenous antioxidants are substances in the diet—particularly in fruits and vegetables—that are able to retard or prevent the oxidation of oxidizable substrates in the body at concentrations that are relatively low when compared to the substrates [32, 33]. As also mentioned before, these dietary compounds include, among others, a variety of phenolic compounds, vitamins, and essential minerals, as well as small peptides such as glutathione, and fatty acids [32, 33]. The health-promoting and preventive effects of these substances against diseases associated with oxidative stress have been well-established [18, 19, 20, 21, 22].

Dietary phenolic compounds acting as antioxidants mainly include phenolic acids, flavonoids, and tannins [39]. Owing to their redox properties, these compounds are able to act as antioxidants and adsorb and neutralize free radicals, quench singlet and triplet oxygen, or decompose peroxides [40, 41]. These processes are accomplished by hydrogen atom transfer, transfer of a single electron, sequential proton loss electron transfer, or chelation of transition metals [40, 41]. In addition, phenolic compounds act synergistically with other antioxidants such as (pro)vitamins A, C, and E [42] and are presumably also involved in the regulation of intracellular glutathione levels [43].

Antioxidant vitamins such as (pro)vitamins A react with peroxyl, hydroxyl, and superoxide radicals; vitamin C is able to quench ROS by donating electrons to them; and vitamins E inhibit ROS generation, preventing lipid peroxidation of cellular membranes [44, 45]. The essential minerals, such as copper, zinc, manganese, and selenium, are indirectly involved in the body’s antioxidant defenses by enhancing the activities of antioxidant enzymes. Copper, zinc, and manganese are cofactors of superoxide dismutase [46], and selenium is a cofactor of glutathione transferase and other selenoproteins [47]. It has notable antioxidant activity [48] and may be beneficial in chronic conditions such as cancer [49], heart disease [50], and cognitive disorders [51]. The common dietary small peptide glutathione is able to directly scavenge ROS [52]. And polyunsaturated fatty acids in, for instance, fish oil are able to eliminate ROS and inhibit cellular processes that generate ROS, decreasing the risk of cardiovascular diseases by reducing triacylglycerol production in the plasma [53].

3. Background on Suriname

The Republic of Suriname is situated in the north-eastern part of South America at the Atlantic Ocean, just north of the Amazon delta in Brazil, and between French Guiana and Guyana (Figure 1). Although located in South America, Suriname is culturally considered a Caribbean rather than a Latin American country and is a member of the Caribbean Community [54]. The climate is tropical with abundant rainfall, a uniform temperature of on average 27°C, and a relatively high humidity of 81% in the capital city of Paramaribo [55]. There are four seasons, namely the long rainy season (April–July), the long dry season (August–November), the short rainy season (December–January), and the short dry season (February–March) [55].

Figure 1.

Map of the Republic of Suriname (from: https://images.app.goo.gl/GrjsLhm6NEaZiDeE7). Insert: Position of Suriname in South America (from: https://images.app.goo.gl/VcvhN76aaKhkegELA).

The country’s land area of roughly 165,000 km² can be distinguished into northern urban-coastal and rural-coastal areas as well as a southern area [55]. The urban-coastal area includes Paramaribo and the district of Wanica, and harbors approximately 80% of the population of over 600,000 [55, 56]. The rural-coastal and rural-interior areas are referred to as the hinterland, are home to the remaining 20% of Suriname’s inhabitants, and encompass more than three-quarters of the country’s land surface [55, 56]. These parts of the country largely consist of sparsely inhabited savanna and dense, pristine, and highly biodiverse tropical rain forest [55], making Suriname comparatively one of the most forested countries in the world [55, 57].

The urban area is characterized by a “western” lifestyle, modern health-care facilities, and an economy that is mainly based on commerce, services, and industry [58]. The hinterland societies have a more traditional way of living, lack comprehensive public health services, and have agriculture, forestry, crude oil drilling, gold mining, as well as ecotourism as major economic activities [58]. These activities have been growing in scale and economic importance in recent years and are, together with agriculture and fisheries, the country’s most important means of support, contributing substantially to the gross domestic income in 2020 of USD 2.88 billion and an average per capita income of about USD 4900 [59]. This positions Suriname on the World Bank’s list of upper-middle income economies [59].

Suriname’s population is among the most varied in the world, comprising the Indigenous Amerindians, the original inhabitants; descendants from enslaved Africans imported between the seventeenth and the nineteenth century (called Maroons and Creoles); descendants from contract workers from China, India (called Hindustanis), and the island of Java, Indonesia (called Javanese) attracted between the second half of the nineteenth century and the first half of the twentieth century; descendants from settlers from a number of European and Middle Eastern countries; and, more recently, immigrants from various Latin American and Caribbean countries including Brazil, Guyana, French Guiana, Haiti, and Cuba [54, 56]. Each of these groups has largely adhered to its original language, religion, and culture, including its ethnopharmacological tradition(s) [60]. This has resulted in a large array of traditional forms of medicine in the country, including those derived from traditional Indigenous, African, Chinese, Indian, Indonesian, and European origin [60].

Suriname is situated on the Guiana Shield, a 1.7-billion-year-old Precambrian geological formation in north-eastern South America that is among the regions of the highest biodiversity in the world [57, 61, 62]. This geographical location, together with the tropical climatic conditions and the variety of habitats, has substantially contributed to the country’s rich fauna and flora that includes many endemic species [61, 62]. There are approximately 192 species of mammals including monkeys such as the howler monkey, predators such as the jaguar and the puma, bloodsucking vampires, anteaters, sloths, armadillos, as well as the unique South American tapir and sea cow. The bird world is very rich and includes 715 species such as the harpy eagle, the scarlet ibis, the black vulture, as well as several species of toucans and parrots. The 102 species of amphibians and the 175 species of reptiles include amphibian salamanders, the unique Surinamese toad, and poison dart frogs; caimans, iguanas, boa constrictors, anacondas, venomous bush masters, and rattlesnakes; and various terrestrial tortoises as well as aquatic and semiaquatic freshwater and sea turtles. There are 360 species of marine fish and 318 freshwater species including 61 endemic freshwater fish such as the carp salmon, the viviparous tooth carp, piranhas, electric eels, stingrays, four-eyed fish, cichlids, and many species of catfish. Lower animals are represented by giant centipedes, tarantulas, land snails that grow to over 13 cm long, and an innumerable insect world, including the intriguing lantern bearer and a variety of butterflies.

Suriname’s flora roughly comprises 5100 species [63], including many species of palms, spurges, peas and beans, madders, citruses, cactuses, orchids, grasses, and bromeliads. Characteristic of Suriname’s 386-km-long coastline is the presence of pristine mangrove forests, which help purify the brackish water, give protection against the sea, and provide shelter and food for many animals. The national flower of the country is the palulu Heliconia bihai (L.) L. (Heliconiaceae), and the national tree is the royal palm Roystonea regia (Kunth) O.F.Cook (Arecaceae). Popular fruit species are avocado, banana, some types of berry and cherry, a variety of citrus fruits, mango, several types of palm fruits and nuts, papaya, passion fruit, pineapple, pomegranate, tomato, and watermelon. Among the most cultivated and consumed produce items are leafy vegetables such as tannia and spinach, a number of cabbage types; various edible nightshades; legume vegetables such as black-eyed pea, lima bean, string bean, and yard-long bean; and fruiting vegetables such as bitter melon, eggplant, habanero pepper, and okra [62, 64, 65].

4. Naturally occurring antioxidants in a few well-known Surinamese fruits

Several of the plant species mentioned in the preceding paragraph are renowned for their high nutritious content and are regarded as nutraceuticals, functional food ingredients, or adaptogens [35, 66, 67, 68] and/or used as traditional medicines [69, 70, 71, 72, 73, 74, 75, 76, 77, 78]. In some cases, these qualifications are attributable to an exceptionally high content of phytochemicals with antioxidant activity, including phenolic compounds such as flavonoids, lignans, and coumarins; vitamins such as (pro)vitamins A, C, and E; and trace elements such as selenium. Hereunder, each of these classes of antioxidant phytochemicals is addressed in detail, and one Surinamese fruit species representative of each class is comprehensively dealt with. All the fruits are abundantly cultivated and traded in Suriname [64] and consumed as foods and/or nutritional supplements [64] and/or used as traditional cosmeceuticals [79] and/or medicines [69, 70, 71, 72, 73, 74, 75, 76, 77, 78]. 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; gastro-intestinal 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.

4.1 Antioxidant phenolic compounds

Phenolic compounds are secondary metabolites of plants that contain at least one functional phenol group [34]. These compounds are abundantly present in, among others, berries, grapes, apples, tomatoes, and apricots; artichokes, chicory, red onions, and spinach; as well as a wide diversity of beverages, food additives, and health-promoting products prepared from these fruits and vegetables [80, 81]. So far, more than 8000 phenolic compounds have been identified in natural sources, and they can be classified into flavonoids including anthocyanins, as well as tannins, coumarins, lignans, stilbenes, and phenolic acids [82]. Some of these compounds help protect plants against predators by acting as toxicants and pesticides against herbivores, nematodes, phytophagous insects, and fungal and bacterial pathogens [83, 84]. Others emanate an appealing scent and/or advertise an eye-catching pigmentation, which attracts pollinators, animals that disperse fruits, symbiotic microbes, and predators of the herbivores that act as bodyguards of the plants [85]. Still others are involved in allelopathic interactions, that is, they are released as volatiles in the air or as root exudates and affect the growth, survival, development, and reproduction of neighboring plants in the soil [86] or in water [87]. And some phenolic compounds, particularly flavonoids and isoflavonoids, are presumably involved in endomycorrhizae formation, that is, the establishment of mutually symbiotic relationship between fungi and plant roots where the roots provide carbohydrates for the fungi and the fungi transfer nutrients and water to the plant roots [88].

A high dietary intake of phenolic compounds by consuming sufficient fruits and vegetables has been related to a decreased rate of chronic diseases [89, 90, 91]. This has, for an important part, been associated with the redox properties of these compounds, which enable them to act as antioxidants, adsorbing and neutralizing free radicals, quenching singlet and triplet oxygen, and decomposing peroxides [40, 41]. These processes are accomplished by hydrogen atom transfer, transfer of a single electron, sequential proton loss electron transfer, or chelation of transition metals [40, 41]. Phenolic compounds are also able to act synergistically with the antioxidant (pro)vitamins A, C, and E [42] and are presumably also involved in the regulation of intracellular glutathione levels [43].

4.1.1 Antioxidant phenolic compounds: anthocyanins: Euterpe oleracea Mart. (Arecaceae)

Anthocyanins are water-soluble phenolic pigments belonging to the subgroup of flavonoids, and they are responsible for the red, violet, purple, and blue colors of fruits and vegetables [92]. These compounds are considered the most important group of phenolic compounds in foods [92] and are found, among others, in flower, fruit, and tuber of red and purple grapes, apples, strawberry, raspberry, blackberry, cranberry, acerola, purple potatoes, cush-cush yam, eggplant, and red cabbage [93, 94]. Anthocyanins help defend plants against attacks by microorganisms and phytopathogens; attract insects, birds, and small mammals for pollination and seed dispersal; and protect plants from the detrimental effects of ultraviolet radiation, high light intensity, drought, low temperatures, water stress, high salinity, and wounding [95, 96].

Important anthocyanins in the plant kingdom are cyanidin-3-rutinoside and cyanidin-3-glucoside [97, 98], along with pelargonidin-3-glucoside, peonidin-3-glucoside, cyanidin-3-sambubioside, and peonidin-3-rutinoside [99, 100]. These phytochemicals basically consist of an anthocyanidin (the aglycon) composed of a flavylium cation (2-phenyl-1-benzopyrilium) linked to one or more sugars such as glucose, xylose, galactose, arabinose, rhamnose, or rutinose through hydroxyl and/or methoxy groups [97, 98, 99, 100]. Anthocyanidins exist in a variety of chemical forms depending on the conditions of the medium, which result in differently colored or colorless compounds [97, 98, 99, 100]. For instance, at pH values less than 3, they are reddish; in the pH range of 4–5, they become colorless; and at pH values greater than 6, they have a purple, blue, bluish-green or blue/lilac coloration [97, 98, 99, 100].

Biochemically, the flavylium moiety has an electron deficiency, which makes anthocyanins highly reactive toward ROS, rendering them powerful natural antioxidants [101, 102]. As a result, anthocyanins have the capacity to potently and readily neutralize ROS by transferring a single electron or by removing the hydrogen atom from their phenolic groups [102]. Indeed, anthocyanins obtained from various sources, including plasma from individuals who had consumed anthocyanin-rich diets, elicited substantial antioxidant effects in various in vitro assays (see, for instance, [103, 104, 105]). And in accordance with the apparent antioxidant and anti-inflammatory properties of anthocyanin-rich diets, the presence of these compounds in fruits and vegetables has been reported to elicit beneficial effects on human health (see, for instance, [92, 102, 106, 107, 108]).

However, there are some doubts as to whether the results from studies showing antioxidant activity of the plasma of individuals who had consumed anthocyanins must be taken as evidence of a beneficial physiological effect of these compounds in humans [105]. It is also not sure whether the plasma concentrations of anthocyanin concentrations were sufficiently high to counteract ROS in vivo [105]. Moreover, the instability of anthocyanins depending on the pH [97, 98, 99, 100] as well as on temperature, light, oxygen, the presence of co-pigments, metallic ions, ascorbic acid, sugar, as well as glycosidases, peroxidases, and phenolases in the medium [109, 110, 111, 112], also cast some uncertainty on the health-promoting effects of the abovementioned fruits and vegetables. Despite these and other reservations, the antioxidant activities of anthocyanins seem undisputable.

The açai palm E. oleracea Mart. (Arecaceae) is a tall, slender, multistemmed evergreen palm tree that can reach a height of 25 m, carries pinnate leaves with a length of up to 3 m, and bears 500–900 small, round, black-purple fruits of about 2.5 cm in diameter in branched, drooping panicles (Figure 2). The plant is indigenous to the northern, tropical parts of South America including Suriname, where it is mainly found along river edges, near swamps, and in seasonal floodplains. E. oleracea is also grown as an ornamental, but more often for its fruit that is commonly known as açaí berry and in Suriname as podosiri. E. oleracea fruit is made up of a hard endocarp that contains a single large seed of 7–10 mm in diameter, a fibrous, purple-colored, pulpy mesocarp of about 1 mm thick, and a deeply purple-colored exocarp or skin.

Figure 2.

Bunch of fruits of the açai Euterpe oleracea Mart. (Arecaceae) (from: https://images.app.goo.gl/22sjzvsep94caDv2A).

The pulp prepared from the mesocarp and the exocarp from E. oleracea fruit has a high nutritional density, containing, among others, appreciable amounts of carbohydrates, proteins, vitamin C, calcium, iron, mono- and polyunsaturated fatty acids, as well as phenolic compounds including five different types of anthocyanins with cyanidin 3-glycoside and cyanidin 3-rutinoside being the most predominant anthocyanins [99, 113]. For this reason, it has been a staple food for the Amazon indigenous peoples for centuries, either raw, prepared as a beverage, or cooked, in the latter case often together with cassava and fish [99, 114]. More recently, a multitude of commercialized E. oleracea fruit pulp products has entered the market, including health-promoting supplements and nutraceuticals formulated as beverages, frozen pulp, powders, tablets, and capsules, as well as ready-prepared healthy food items such as jams, ice creams and other frozen treats, as well as mousses, cakes, porridges, and bonbons [99, 101, 115].

Preparations from the fruit and other parts of E. oleracea are also abundantly used in various traditional medical practices in different parts of the world including Suriname. A few indications are anemia, hypotension, various types of wounds including open cuts, scorpion stings, and shot wounds; and as an external contraceptive [77, 78, 116, 117, 118, 119, 120]. Pharmacological studies with particularly the fruit juice have shown a wide range of activities, including antidiarrheal, anti-inflammatory, antinociceptive, antiangiogenic, antimicrobial, antileishmanial, skin regenerating and antiageing, cosmeceutical, neuroprotective, anticancer, and antioxidant effects [79, 119, 120, 121, 122]. Particularly, the antioxidant properties of E. oleracea fruit preparations have been well investigated, showing an abundance of phenolic compounds with antioxidant activity [123, 124, 125, 126, 127], supporting some of their traditional and nutraceutical uses [79, 119, 120, 121, 122, 123, 124, 125, 126, 127].

Indeed, the phenolic compounds and anthocyanins in E. oleracea fruit pulp have been shown to very efficiently scavenge superoxide and peroxyl radicals [102]. And E. oleracea fruit pulp seemed to elicit a greater antioxidant power than other anthocyanin-rich fruits such as blueberries and black berries [128]. The results from clinical studies also supported the antioxidant benefits of E. oleracea fruit juice and related products. For instance, total anthocyanin levels in volunteers who had consumed E. oleracea fruit pulp and clarified fruit juice led to substantially increased plasma antioxidant capacity [129] as well as an increased catalase activity, total antioxidant capacity, and reduced ROS production in total serum of healthy women [130]. These observations support, at least partly, some of the pharmacological activities and cosmeceutical applications of E. oleracea fruit preparations [79, 119, 120, 121, 122].

As indicated above, the commercial success of E. oleracea fruit pulp products [115] has particularly been attributed to its high content of anthocyanins—mainly cyanidin-3-glucoside [128]—with superior antioxidant activity [99, 101]. However, as also mentioned before, the chemical instability of anthocyanins may well affect their antioxidant properties [97, 98, 99, 100, 109, 110, 111, 112]. For this reason, the possibility exists that other, more stable phenolic compounds, vitamins, and/or fatty acids [99, 113] in E. oleracea fruit pulp may substantially contribute to its antioxidant activity [131].

4.1.2 Antioxidant phenolic compounds—Tannins: Punica granatum L. (Lythraceae)

Tannins are a class of astringent, water-soluble phenolic compounds that form strong complexes with macromolecules and precipitate proteins and various other organic compounds including amino acids and alkaloids [132, 133]. They occur abundantly in particularly bark, leaves, buds, unripe fruits, and seeds of many plants and play important roles in the protection of plants from predation by making them unpalatable, dissuading animals from predation [132, 133]. These compounds are responsible for the astringency, color, and some of the flavor in black and green teas [132]. The name of this group is derived from their centuries-old use for tanning animal hides in the leather processing industry [134]. Tannins are also used for dyeing fabric and making ink, as well as in the clarification of wine and beer [134]. Owing to their styptic and astringent properties, tannins have medicinally been used to treat tonsillitis, pharyngitis, hemorrhoids, and skin eruptions [135], and internally to control diarrhea, against intestinal bleeding, and to bind to and eliminate metallic, alkaloidal, and glycosidic poisons [135].

Tannins can chemically be distinguished in two major groups, namely hydrolyzable tannins and condensed tannins [136]. Hydrolyzable tannins break down in water, yielding various water-soluble products, and are subdivided in gallotannins and ellagitannins [136]. The gallotannins release gallic acid and glucose by hydrolysis at low ambient pH and can be encountered in, among others, the pods of the tara Tara spinosa (Feuillée ex Molina) Britton & Rose (Fabaceae) [137] and the gallnuts of the Aleppo oak Quercus infectoria Oliv. (Fagaceae) [138]. The ellagitannins are made up of ellagic acid glycosides, and are ingredients of the wood of several species of oak in the family Fagaceae such as that of the common oak Quercus robur L and the white oak Quercus alba L. [139], as well as the gallnuts of the myrobalan Terminalia chebula Retz. (Combretaceae) [140].

Condensed tannins are the larger group of tannins, form reddish-colored, water-insoluble phenolic precipitates called tanner’s reds or phlobaphenes, and are less astringent when compared to hydrolysable tannins [136]. They are polymers of monomeric flavonoids, are also called proanthocyanidins because they yield anthocyanidins when depolymerized under oxidative conditions, and include, among others, the procyanidins, propelargonidins, prodelphinidins, profisetinidins, proteracacinidins, proguibourtinidins or prorobinetidins [136]. Some of these compounds are naturally present in the skin and seed of the red grape Vitis vinifera L. (Vitaceae) and are, therefore, present in red wines [141]. Other important sources of condensed tannins are the extracts from various genera and species of mangrove [142] and acacia [143].

With more than 1000 natural ellagitannins identified to date, this subgroup constitutes the largest among the hydrolyzable tannins [144, 145]. Examples of these compounds are punicalagin, sanguiin H6, lambertianin C, pedunculagin, vescalagin, castalagin, casuarictin, and potentillin [146] in, among others, walnuts and almonds in the genera Juglans (Juglandaceae) and Prunus (Rosaceae), respectively; oak-aged wines; berries in the genera Rubus and Fragaria (Rosaceae); and the pomegranate P. granatum L. (Lythraceae) [147, 148]. Like other tannins [135], ellagitannins, along with some of its metabolites, have been reported to exhibit various beneficial effects on human health including anti-inflammatory, anticancer, prebiotic, cardioprotective, as well as antioxidant properties [149, 150]. After ingestion, ellagitannins are hydrolytically fractionated in the stomach and the duodenum, yielding ellagic acids [132, 133, 151], which are partially metabolized to urolithins by gut microbiota [149, 151]. Both the ellagic acids and the urolithins elicited in vitro antioxidant activity [152, 153] and might be responsible for (some of) the pharmacological activities of ellagitannins [154]. These findings are consistent with the assumption that the potential health benefits of ellagitannins could not solely be attributed to these compounds themselves [155].

The pomegranate P. granatum L. (Lythraceae) is a long-lived, deciduous shrub or small tree with multiple spiny branches that grows between 5 and 10 m tall. The plant originates from the Mediterranean region and has been introduced into the New World in the late sixteenth century by Spanish colonizers. It is now widely cultivated for its edible fruit in various countries in the Americas as well as in parts of the Mediterranean Basin, north and tropical Africa, Iran, Armenia, the Middle East and Caucasus region, the Indian subcontinent, and the drier parts of Southeast Asia. The rounded fruit measures 5–12 cm in diameter, develops from bright red flowers, and is made up of a red-purpled colored husk consisting of an outer, hard exocarp, and an inner, white, spongy mesocarp that forms chambers that contain 200–1400 seeds inside pulpy, succulent sarcotestas (Figure 3). The juice obtained from the sarcotesta is sweet-sour-tasting and is used in baking, cooking, juice blends, meal garnishes, smoothies, and alcoholic beverages such as cocktails and wines.

Figure 3.

Open fruit of the pomegranate Punica granatum L. (Lythraceae) showing seeds inside sarcotestas (from: https://images.app.goo.gl/zyYerutR5BTYZ87f8).

P. granatum is much appreciated in many parts of the world including Suriname, where the fresh fruit is recommended for the promotion of general health and as a remedy for bleeding gums, lung afflictions, and tuberculosis [70, 156], while preparations from various parts of the fruit are used against small wounds in the oral cavity; hemorrhage; sore throat; shortness of breath; ulcers, diarrhea, and dysentery; menstrual pain, and tapeworm infection [69, 70, 75, 78, 156, 157, 158]. These uses are partially supported by the many pharmacological activities of this plant including antidiabetic, antitumor, anti-inflammatory, antimicrobial, antiparasitic, antiviral, antifibrotic, and other effects [156, 159, 160]. And several of these activities have been associated with the antioxidant activities of the many bioactive compounds in the plant including the ellagitannins [156].

Notably, P. granatum sarcotesta juice has a relatively high content of ellagitannins [161, 162, 163, 164], in addition to anthocyanins which give the juice its red color [164, 165]. In fact, ellagitannins, particularly punicalagin isomers, are presumably the major phenolics in pomegranate fruit and juice [163]. These compounds probably account for more than 90% of the antioxidant activity of the juice, exceeding that of other red-purple fruits, red wine, and green tea [161, 162]. Indeed, ellagitannins from various sources including P. granatum fruit as well as their metabolites such as urolithin, elicited substantial antioxidant effects in several in vitro assays [166] and in vivo models [167]. Of note, the plasma of individuals given a P. granatum ellagitannin-enriched polyphenolic dietary supplement also elicited meaningful in vitro antioxidant activity [168]. These observations support the use of P. granatum fruit preparations as health-promoting substances.

4.1.3 Antioxidant phenolic compounds: coumarins: Dipteryx odorata (Aubl.) Willd (Fabaceae)

Coumarins, including the type compound coumarin, also known as 2H-chromen-2-one, 2H-1-benzopyran-2-one, 1,2-benzopyrone, and o-hydroxycinnamic acid lactone, are phenolic compounds that were first isolated from the seed of the tonka bean D. odorata Willd. (Fabaceae) [169]. Subsequently, these compounds appeared to be present in many other plants including species of cinnamon, strawberries, black currants, apricots, and cherries [170]. They have a bitter taste that helps protect the plants from herbivory by acting as appetite suppressants [171]. To date, about 800 naturally occurring coumarins have been identified in about 600 genera of 100 families of plants [172]. Coumarins can be distinguished into simple coumarins (e.g., coumarin, as well as umbelliferone, also known as 7-hydroxycoumarin, in Apiaceae members such as carrot and coriander), furanocoumarines (e.g., psoralen in the seed of the Indian medicinal plant Psoralea corylifolia L. (Fabaceae), pyranocoumarins (e.g., the natural vasodilator visnadin in the bishop’s weed Visnaga daucoides Gaertn. (Apiaceae), and pyrone-substituted coumarins (e.g., the 4-hydroxycoumarin dicoumarol, a naturally occurring anticoagulant that depletes vitamin K stores similarly to warfarin) [172]. Warfarin is a synthetic anticoagulant produced on the basis of dicoumarol’s structure [173].

Coumarin itself is of relatively low toxicity to humans when consumed in moderation [174]. However, at large (infused) doses, it may cause liver damage, hemorrhages, and paralysis of the heart [174]. It is, therefore, controlled as a food additive by many governments [175] and has even been banned in the USA [176]. Warfarin, acenocoumarol, and phenprocoumon are commonly prescribed to patients suffering from atrial fibrillation, deep venous thrombosis, or pulmonary embolism, or to individuals with artificial heart valves, in order to prevent the formation of blood clots and reduce the risk of embolism [177, 178]. Warfarin is also widely used as a rat poison [179]. Other well-known industrial applications of coumarins are their use as agrochemicals, materials for food processing, optical brighteners, and dispersed fluorescent and laser dyes (see, for instance, [40, 179]).

Besides anticoagulant activity, coumarins have been found to elicit a host of other pharmacological activities including antitumor, photochemotherapeutic, anti-HIV, antimicrobial, anti-inflammatory, triglyceride-lowering, central nervous system-stimulating, and menopausal distress-preventing effects [180, 181, 182]. These beneficial health effects are believed to be mainly related to their antioxidant activities, providing protection against oxidative stress by scavenging ROS such as superoxide, hypochlorous acid, and hydroxyl radicals [183]. Indeed, numerous studies with natural and synthetic coumarins using a variety of assays have shown strong in vitro antioxidant effects (see, for instance, [184, 185, 186]). At least one of the mechanisms involved in the antioxidant activity of coumarins is the donation of hydrogen to ROS in its reduction to nonreactive species, removing the odd electron responsible for radical reactivity [187, 188].

The tonka bean D. odorata (Aubl.) Willd., called “tonkaboon” in Suriname, is a large semideciduous evergreen tree with a small, rounded crown that can reach a height of 30 m. The plant is native to Central America and the northern parts of South America. It is sometimes cultivated but is mostly harvested from the wild for its seed that becomes black and wrinkled with a smooth, brown interior after steeping for 24 hours in alcohol and drying (Figure 4). As mentioned above, the seed is rich in phenolic compounds including coumarin and several of its derivatives [169]. These compounds have a strong sweet and spicy fragrance that is reminiscent of new mown hay, vanilla, and almond [189]. For this reason, they are abundantly used as key fragrances of fougère perfumes, as a substitute for vanilla, and as flavoring agents for desserts and stews as well as tobacco and whisky [175]—in addition to the applications mentioned above—despite the safety concerns [174]. Besides coumarins, D. odorata seed contains various other bioactive phenolic compounds, particularly isoflavones, mostly in the endocarp [190] but also in some of its other parts [191, 192].

Figure 4.

Dried fruits of the Tonka bean Dipteryx odorata (Aubl.) Willd (Fabaceae) (from: https://images.app.goo.gl/Jw7f48V1kARX9vgE9).

Preparations from D. odorata seed have many traditional uses, among others, to fortify the scalp and improve hair growth; as a remedy for colds, fever, coughing, asthma, and tuberculosis; for treating stomach pain and diarrhea; against dysentery and schistosomiasis; as an emmenagogue, and as an aphrodisiac [117, 193, 194]. In Suriname, D. odorata seed is mainly used as an ingredient of products to treat hair loss, dandruff, and an itching scalp; against colds; and to command luck [78, 195].

Some of these traditional uses are in accordance with the results from the abovementioned pharmacological studies with coumarin analogues—from the seed as well as other parts of the plant—showing a wide range of pharmacological activities [180, 181, 182]. This suggests that at least some of the traditional uses of D. odorata seed preparations are also attributable to antioxidant activities. Indeed, the coumarin-rich oil from D. odorata seed displayed meaningful antioxidant activity in several in vitro free radical scavenging assays but also had a substantial total phenolic content [196]. And raw, roasted, and boiled D. odorata seeds had a considerable coumarin, total phenolic, and total flavonoid contents and displayed meaningful free radical scavenging activity, superoxide dismutase activity, as well as ferric reducing antioxidant power [197]. However, both coumarins and flavonoids in D. odorata seed preparations elicited antioxidant activities [180, 184, 185] and can be classified as phenylpropanoid-derived natural products. This makes it difficult to determine whether and to which extent the traditional and pharmacological activities of D. odorata seed preparations can only be associated with antioxidant activities due to coumarins.

5. 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 P. granatum, the tonka bean D. odorata, the tucumã Astrocaryum vulgare, the acerola Malpighia glabra, the roselle Hibiscus sabdariffa, and the Brazil nut Bertholletia excelsa. 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 antioxidant 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 activities of E. oleracea fruit pulp products [99, 101] are presumably not only due to their high content of mainly the anthocyanin cyanidin-3-glucoside, but also due to other phenolic compounds, vitamins, and/or fatty acids [99, 113, 128, 131]. Similarly, as mentioned in part 2 of this chapter, the antioxidant activity of the mesocarp of the tucumã or awara Astrocaryum vulgare Mart. (Arecaceae) A. vulgare [198, 199] may be partly ascribed to phytosterols and vitamin E derivatives in addition to its high content of carotenoids [198, 199]. And those of preparations from the seed of the Brazil nut or paranoto Bertholletia excelsa Humb. & Bonpl. (Lecythidaceae) [200, 201, 202] might be due to the combined actions of selenium with phenolic compounds, tocopherols, and unsaturated fatty acids [203, 204, 205, 206].

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 beneficial properties. This is the more important in the case of substances containing chemically instable ingredients such as anthocyanins [97, 98, 99, 100, 109, 110, 111, 112], and those that may generate pro-oxidant radical species such as carotenoids [207, 208], or display pro-oxidant properties at, for instance, relatively low concentration such as vitamin C [209].