Sources of Natural Antioxidants

### **Chapter 4**

## Congolese Traditional Foods as Sources of Antioxidant Nutrients for Disease Prevention

*Théophile Mbemba Fundu, Paulin Mutwale Kapepula, Jean Paul Nzundu Mbo, Justin Mboloko Esimo and Nadège Ngombe Kabamba*

### **Abstract**

Oxidative stress, characterized by excessive production of reactive species, is involved in several chronic diseases such as cardiovascular, chronic obstructive pulmonary, sickle cell, chronic kidney, neurodegenerative, and cancer. The negative impact of ROS and RNS, produced by endogenous and exogenous processes, is neutralized by antioxidant defenses. Given the importance of oxidative stress to human health, the use of antioxidants as therapy directs medical research toward the specificity of antioxidants causing each disease. Fruits and vegetables contain antioxidants, such as nutraceuticals, pharmaceuticals, and phytoceuticals, the consumption of which reduces the risk of developing chronic diseases. Flora of African countries is endowed with plant species that would make a putative source for new antioxidants. This article reports antioxidant activities of traditional foods from Democratic Republic of the Congo. Further studies are needed to ensure mechanisms of their functionality in the human body.

**Keywords:** antioxidants, Congolese diet, insects, oxidative stress, phytochemicals, reactive oxygen species, selenium, vegetables

### **1. Introduction**

Oxygen metabolism, physiologically and regularly, produces small amounts of reactive oxygen species (ROS) to serve as an essential signaling mechanism for the maintenance of homeostasis and redox reactions in the cell [1]. Highly reactive ROS, associated with inflammation, cause tissue damage against which the cells of the human body protect themselves by various free radical defense mechanisms. However, when ROS levels are high due to an imbalance between their production and antioxidant defense mechanisms, oxidative stress occurs [2]; a situation where the cell no longer controls the excessive presence of radical's toxic oxygen, responsible for genomic and metabolic modifications, which favor the development of several diseases, in particular diabetes, cardiovascular diseases, cancer, respiratory and rheumatic diseases, and endometriosis [3]. Endogenous antioxidants and the wide

variety of antioxidants in the diet, once present in all compartments of the organism, are involved in the protection of membranes and intra and extracellular environments against free radicals, and therefore against the diseases for which they are responsible. The objective of this review was to provide the therapeutic potential of Congolese traditional foods with antioxidant capacities useful in the management of various pathologies associated with oxidative damage.

### **2. Oxygen and ROS**

Oxygen, essential for life, can also become a source of toxicity and cell degeneration. Indeed, at the level of the electron transport chain, oxygen undergoes a tetravalent reduction, which transforms it into water-generating ATP. During this process, 2% of the oxygen escapes and undergoes a monovalent reduction of one electron at ubiquinone producing the superoxide radical (•O2 – ) with an unpaired electron on the outer shell, which is seeking to return immediately to a stable state by donating an electron or taking one from another molecule, finds itself in an energy instability that gives it its particular reactivity with respect to other atoms or molecules [4]. O2 – can also be produced from NADH-dehydrogenase located in the inner mitochondrial membrane or from NADPH oxidase present in vascular endothelial cells [5]; it can also result from the auto-oxidation of neurotransmitters such as adrenaline, noradrenaline, dopamine, cysteine thiols, and reduced coenzymes, such as FADH2, as well as the detoxification of toxic pollutants and drugs, by the system of cytochromes P450 present in the endoplasmic reticulum [6]. The neutrophil respiratory burst and xanthine oxidase, NO synthase, and eicosanoids are also cellular sources of superoxide anion production [7]. Having a certain toxicity and being at a low concentration, the superoxide radical is eliminated by superoxyde dismutase (SOD), generating hydrogen peroxide (H2O2), which can also be produced by a bielectronic reduction of oxygen in the presence of oxidases of peroxisomes or by oxidative deamination of certain amines of the outer mitochondrial membrane. In the presence of metal cations, such as Fe2+ [8] or Cu [9], hydrogen peroxide generates, through the Fenton reaction, the hydroxyl radical (• OH), which is particularly harmful to biological tissues.

Other oxygen free radicals such as the perhydroxyl radical (HO2), the peroxyl radical (RO), and the alkoxyl radical (RO2) can also be formed during cellular metabolism. Another radical species is nitric oxide, which is produced by the various NO synthases (or NOS) of endothelial cells or macrophages for neuron-mediated purposes [7]. Inflammation is also an important source of oxygenated radicals produced directly by activated phagocytic cells, which are the site of a phenomenon called oxidative explosion consisting of the activation of the NADPH oxidase complex, an enzyme capable of using molecular oxygen to produce large amounts of superoxide anions at the cell membrane. This mechanism, when controlled, is essential in the fight against infection because it allows the phagocytosis of bacteria and foreign bodies. Radiation can generate free radicals, either by splitting the water molecule in the case of ionizing X or γ rays or by activating photosensitizing molecules in the case of ultraviolet rays [10, 11].

In general, ROSs include free radicals of oxygen itself as well as singlet oxygen ( 1 O2) and non-radical reactive oxygen species, such as hydrogen peroxide (H2O2), RO2H, peroxynitrite (ONOO– ), and HOCl, whose toxicity is significant [12].

Due to their reactivity, ROSs participate in phagocytosis, cell signaling, activating fertilization, improving muscle glucose uptake, and replenishing muscle glycogen

*Congolese Traditional Foods as Sources of Antioxidant Nutrients for Disease Prevention DOI: http://dx.doi.org/10.5772/intechopen.109319*

stores [13–15] and have a bactericidal effect [16]. In addition, ROSs regulate most of the physiological functions of the body, in particular transcription factors, which activate protective genes for the cell contributing to the processes of cell repair and regeneration as well as the phenomenon of apoptosis [17].

To have a level of ROS beneficial for cellular life, it is necessary to maintain a balance inside the cell between the systems that generate free radicals and the nonenzymatic antioxidant systems [18, 19].

### **3. Oxidative stress**

Present in excess in the body, ROS create an imbalance between prooxidant sources and antioxidant systems, generating "oxidative stress." This oxidative stress, resulting from the excessive presence of toxic oxygen radicals, causes oxidative damage to lipids, DNA, or proteins, which is the basis of many cellular dysfunctions, and the activation of the expression of genes coding for pro-inflammatory cytokines or adhesion proteins, phenomena that are partly responsible for a large number of diseases such as cancer, cardiovascular disorders, and neurodegenerative diseases [20, 21].

This disruption of the antioxidant/prooxidant balance in favor of the prooxidants can come from heavy metal poisoning; irradiation, a nutritional deficiency in one or more of the antioxidants such as vitamins or trace elements, abnormalities genetics responsible for poor coding of a protein either enzymatically antioxidant, synthesizing an antioxidant, regenerating an antioxidant, coupling defense to energy, or of a promoter of these same genes that the mutation will render unable of reacting to an excess of radicals or ischemia/repercussions following thrombosis [22–24]. In general, oxidative stress is the result of several of these factors and occurs singularly in a specific tissue and cell type, and not throughout the body.

### **4. Physiological and pathological oxidative stress**

Oxidative stress, resulting from high levels of toxic ROS and RNS, while having a physiological role, constitutes a favorable ground for the development of various pathologies. Generated in small quantities under normal conditions, ROSs play a role of capable secondary messengers, especially in regulating the phenomenon of apoptosis or of activating transcription factors as well as in maintaining cellular homeostasis [25]. During the process of fertilization, the sperm cells secrete large amounts of ROS to pierce the membrane wall of the egg [26]. Free radical nitric oxide or NO• , synthesized by endothelial cells, has regulatory effects for the maintenance of vascular tone, neurotransmission, renal function, and other physiological functions.

However, in the event of oxidative stress, the strong reactivity of ROS with respect to biological substrates can induce deleterious oxidative damage, which promotes the appearance of several diseases and the complications associated with them. The oxidation of lipids, for example, is a factor favoring the occurrence of cardiovascular diseases, while that of DNA is found in various stages that lead to the development of cancers [27].

The development of molecular biology has also clarified the important physiological role of ROSs, which, at high levels in the body, activate the expression of genes coding for pro-inflammatory cytokines or proteins adhesion, thus, becoming pathological. By reacting with DNA and the memory of all the biochemical composition of

living beings, ROSs induce five main classes of oxidative damage, namely, oxidized bases, abasic sites, intra-strand adducts, strand breaks, and DNA-protein bridges. If these structural alterations are not "repaired," they will disrupt the DNA replication mechanisms and lead either to reading and synthesis errors by unfaithful translesional DNA polymerases resulting in a point mutation in the genome, or an impossibility of DNA copying, which will result in the initiation of the programmed suicide of the cells by a mechanism called apoptosis [28]. Not only smoking, alcoholism, obesity, and intense physical exercise but also our bad eating habits abnormally increase the production of AOEs in our bodies [29]. A diet low in fruits and vegetables and rich in antioxidants (vitamins C and E, carotenoids, polyphenols) promotes a drop in antioxidant capacity. For the sake of prevention, having effective tools to properly assess the status of oxidative stress, in an individual, in order to make the necessary corrections to their antioxidant defenses and reduce the oxidative damage induced by ROSs at the DNA level, proteins, and lipids is an imperative necessity.

### **5. Oxidative stress and associated diseases**

Oxidative stress is implicated in the occurrence of several acute and chronic pathologies [30]. Under physiological conditions, glucose, in the presence of metallic traces, can oxidize, releasing ketoaldehydes, H2O2, and • OH, which will lead to the cleavage of proteins or their glycation by attachment of the ketoaldehyde, forming an AGE derivative. This phenomenon of glycosylation, very important in diabetics, contributes to the fragility of their vascular walls and their elasticity [31]. Reactive oxygen species also attack mucopolysaccharides and, in particular, cartilage proteoglycans. By altering Krebs cycle enzymes, oxidative stress negatively influences oxidative phosphorylation, promoting acidosis and early fatigue. ROSs readily react with aromatic and sulfur amino acids, altering the functions of proteins that they constitute as well as their ability to properly bind to a receptor or specifically bind a ligand, which alters cell signaling [32]. The attack on membrane lipid double bonds induces peroxidation reactions that alter membrane exchange, barrier, and information functions, modify membrane fluidity and the functioning of numerous receptors and transporters and signal transduction; that of circulating lipids lead to the formation of oxidized LDL, which, captured by specific macrophage receptors, promotes the secretion of pro-inflammatory cytokines [33] and forms the lipid deposit of the atherosclerotic plaque of cardiovascular disease. Damage to lysosome membranes promotes the release of proteases into the cytosol [34], which will aggravate protein destruction and induce muscle catabolism, responsible for the onset of atrophy or even cachexia. The human brain is very sensitive to oxidative damage due to its richness in polyunsaturated fatty acids, its high oxygen consumption, and the presence of metals with active redox potential such as copper and iron [35]. As oxidative stress increases with age, it is considered a primary etiological factor in age-related degenerative pathologies such as Alzheimer's and Parkinson's diseases. Oxidative stress also plays a crucial role in the occurrence of other neurodegenerative pathologies of toxic-nutritional origin such as konzo, tropical ataxic neuropathy, and neurolathyrism [36]. In general, oxidative damage compromises cell viability or induces other cellular responses *via* secondary reactive species leading to apoptosis or cell necrosis. The most concerning pathologies are cardiovascular diseases, cancers, diabetes, neurodegenerative diseases, and endometriosis. The biological consequences of oxidative stress vary according to the dose and the cell type. If light stresses increase cell proliferation and the expression of adhesion proteins, medium stresses facilitate

apoptosis, and strong stresses cause necrosis, while violent stresses disorganize the cell membrane, leading to immediate lysis. The amplitude of oxidative stress promotes the induction of cell death processes: apoptosis and/or necrosis [37].

### **6. Antioxidants**

Antioxidants are molecules capable of neutralizing oxidative species and preventing their oxidative damage. In a healthy individual, reactive species and antioxidant defenses are in balance, although there may be a slow accumulation of oxidative damage with age [38]. This imbalance also occurs when there is a significant decrease in antioxidant levels without necessarily an increase in ROS production. Studies on the involvement of GSH during the aging of human embryo fibroblasts in culture have reported that the activity of the antioxidant enzyme glutathione peroxidase, as well as that of glutathione reductase, constantly decreases during aging cells until reaching a drastic low level in old cells [39]. To counteract the harmful effects of ROS following excessive ROS production, living cells and tissues are equipped with enzymatic systems, endogenous molecules, and antioxidants whose essential role is to destroy these intermediates before their deleterious action and to restore the redox balance [39]. According to their mode of action, we distinguish stoichiometric antioxidants and catalytic antioxidants. The stœchiométric antioxidants are vitamins, reduced glutathione (GSH), uric acid, N-acetylcysteine, nonsteroidal anti-inflammatory drugs, certain antibiotics, polyphenols, etc. capable of neutralizing one or even a few ROSs, mainly free radicals. The catalytic antioxidants have two subgroups [40]. The first are antioxidant enzymes with direct catalytic activity, such as superoxide dismutase (SOD) and glutathione peroxidase (GPx), and the second, with indirect catalytic activity, is represented by cofactors of antioxidant enzymes such as NADPH, GSH, and selenium or reducing enzymes involved in the repair of oxidation processes such as GSH reductase, thioredoxin reductase, and also ferritin, transferrin, and desferrioxamine. By neutralizing an oxidizing enzyme molecule or activating an antioxidant enzyme, hundreds or even thousands of ROS will be eliminated by the action of a single antioxidant molecule, hence their qualification as catalytic antioxidants. According to their nature, antioxidants are enzymatic and nonenzymatic. The enzymatic group includes the primary defense enzymes that directly neutralize free radicals or prevent their formation [38], such as superoxide dismutase, catalase, and glutathione peroxidase, while the secondary are glutathione reductase and glucose-6-phospho-dehydrogenase [41]. Nonenzymatic antioxidants are mainly exogenous molecules of food origins such as polyphenols, vitamins, carotenoids, sulfur molecules, and mineral elements.

### **7. Micronutrients, polyphenols, and phytochemicals as natural plant antioxidants**

Phytochemicals are secondary metabolites, suchas polyphenols, terpenes, nitrogen/sulfur-containing compounds, and alkaloids, found in algae, fungi, plants, and some insects such as caterpillars, not directly involved in basic life processes but constitute compounds with multiple nutritional and therapeutic beneficial effects for humans [42]. During the overflow of the body's defense system following multiple attacks due to a poor lifestyle, there is a loss of activity of antioxidant

enzymes, leading to sometimes irreversible cellular disorganizations going so far as to cause cell death. Under these conditions, the presence of natural antioxidants such as micronutrients, carotenoids, and polyphenols is essential to limit oxidative damage. The best carotenoid known is β-carotene, which is the precursor of vitamin A. Recent studies showed beneficial effects of glucosinolates, including regulatory functions in inflammation, stress response, phase I metabolism, and antioxidant activities [43]. The polyphenols, according to their antioxidant, antimicrobial, and anti-inflammatory properties, have demonstrated remarkable effects in many chronic diseases such as neurodegenerative diseases, diabetes, and cardiovascular diseases. It has been reported that phenolic and flavonoid compounds act as antioxidants to exert antiallergic, anti-inflammatory, antidiabetic, antimicrobial, antipathogenic, antiviral, antithrombotic, immunomodulatory, and vasodilatory effects, and prevent diseases such as cancer, heart problems, cataracts, eye disorders, and Alzheimer's [44].

Currently, a wide variety of polyphenols showed immunomodulatory activity by altering the formation of nitric oxide and eicosanoid proteins and by inhibiting pro-inflammatory cytokines and gene expression [45]. The polyphenols are found in plants, from the roots to the fruits. In this group, we have phenolic acids (caffeic, chrolorogenic acids…), anthocyanins, anthraquinones, catechins, coumarins, flavonoids (quercetin, kaempferol, rutin…), and tannins.

About micronutrients, essential components of the diet, studies on their supplementation that might improve health status have gained immense popularity. Fruits and vegetables, such as grapes, oranges, pomegranates, apples, plums, fresh garlic, carrots, and spinach from nature, have micronutrients and are rich in molecules with high antioxidant power, including tocopherols and polyphenols, which have ammunition to fight against free radicals and stop their chain oxidation reaction [46].

### **8. Traditional foods as potential sources of antioxidants, nutraceuticals, pharmaceuticals, and phytoceuticals**

Traditional foods, eaten and prepared by groups of people who share a common religion, language, culture, or heritage, are an expression of the culture, history, and lifestyle of a people [47, 48]. The Democratic Republic of Congo (DRC) with the largest biodiversity in Africa and a variety of ecosystems: including nearly half the African rainforests, forest-savannah ecotones, savannahs, afro -mountainous forests, large and small lakes, rivers, and swampy forests [49], and lived by most than 450 ethnic groups, has more types of cuisines, rich in traditional dietary diversity from vegetables, fruits, herbal teas, legumes, nuts, seeds, mushrooms, and insects. In three of the twenty-six provinces of the DRC, Mbemba et al. have listed 163 different vegetables, 85 species of mushrooms, 35 kinds of roots and tubers as well as 64 species of fruits, nuts, and seeds, several of which are rich in proteins of good biological value: in lipids with unsaturated fatty acids, in vitamins, and in minerals [41]. The results of our studies on the phytochemicals, micronutrient contents, and antioxidant activities of traditional foods are reported in the table below.

Vegetables represent an important part of the diet of Congolese's population. Apart from conventional vegetables originating from other countries, there are traditional vegetables specific to each ethnic group. These vegetables are rich in nutrients such as proteins, lipids, vitamins, and minerals. Studies on several vegetables have shown their richness in various secondary metabolites (**Table 1**) with therapeutic properties that would justify their use in the management of certain diseases.


*Congolese Traditional Foods as Sources of Antioxidant Nutrients for Disease Prevention DOI: http://dx.doi.org/10.5772/intechopen.109319*


*(\*) Antioxidant activities were evaluated using gallic acid and quercetin as controls. (IC50 Gallic acid: 0.71 ± 0.08 and 1.07 ± 0.10; Quercetin: 1.42 ± 0.04 and 3.21 ± 0.99 in ABTS and DPPH tests, respectively). (-) not determined*

### **Table 1.**

*Antioxidant activities of Congolese traditional vegetables.*

From the results obtained, it appears that traditional vegetables contain polyphenolic compounds and flavonoids, which would give them antioxidant activities that are likely to fight against free radicals to attenuate oxidative damage to cells in the human body and spare it from chronic diseases. In order of importance, we align *Salacia pynaerti, Tetrorchirdium congolense, Manihot glaziovii, Manihot esculenta, Rungia congoensis, Sesamum angustifolium, Phytolacca dodecandra, Entada gigas, Hibiscus acetosella, Ipomoea batatas, Psophocarpus scandens* etc. In addition, the leaves of *Salacia pynaerti* contain calcium, zinc, manganese as well as glutamic, methionine, and cysteine, which participate in the synthesis of glutathione [54].

Spices are an integral part of the Congolese diet. Several traditional spices have been identified in the culinary habits of the Congolese people, often unrecognized and unexploited. Spice plants and vegetables, as well as their essential oils, are important sources of antioxidants phytochemicals and micronutrients including phenolics, terpenoids, and alkaloids. Consumption of these spices in diets would reduce the occurrence of nutritional deficiencies and health problems (**Table 2**).

Spice data indicate high polyphenol content in *Curcuma longa* rhizomes and high antioxidant activity from *Piper nigrum*. Studies have reported that the consumption of turmeric longa, mixed with black pepper, slows down or even decreases the proliferation of cancer cells [57]

Mushrooms are the second most common traditional food available to the Congolese rural population after vegetables. Although they are available periodically, *Congolese Traditional Foods as Sources of Antioxidant Nutrients for Disease Prevention DOI: http://dx.doi.org/10.5772/intechopen.109319*


*(\*) Antioxidant activities were evaluated using gallic acid and quercetin as controls. (IC50 Gallic acid: 0.71 ± 0.08 and 1.07 ± 0.10; Quercetin: 1.42 ± 0.04 and 3.21 ± 0.99 in ABTS and DPPH tests, respectively).*

*(-) not determined*

### **Table 2.**

*Antioxidant activities of Congolese traditional spices.*

some species are sold dried throughout the year, such as *Auricularia delicata, Lactifluus edulis,* and *Schizophyllum commune* (**Table 3**). Mushrooms are a significant source of lipophilic compounds, phenolic and indole derivatives as well as carotenoids, and some vitamins having considerable antioxidant properties.

Despite low levels of polyphenols, mushrooms contain terpenoids as well as trace of elements such as zinc and selenium, and have appreciable antioxidant activity. *Auricularia delicata, Cantharellus symoensii*, *Lactarius ssp, Lactarius tenellus,* and *Marasmius collybia* have the best antioxidant activities.

Yams are an alternative for cereals and tubers with a moderate glycemic index, close to that of corn but lower than that of rice and cassava. Congolese yams are mainly represented by *Dioscorea* species. Numerous studies have reported the high nutritional value of *Diosocorea,* particularly as an alternative source of starch and some important micronutrients. Bioactivities and health benefits of yams such as Dioscorea extracts and other preparations have been related to the presence of phytochemicals, which possess antioxidant properties. Antioxidant activities are related mainly to radical scavenging capacity and positive effects on the cell's endogenous antioxidant system. Bukatuka et al. (2016) studied five Congolese edible Dioscorea and showed that the phytochemical screening revealed the presence of polyphenols, alkaloids, and terpenoids and they have shown a good antioxidant and anti-hyperglycemic activities (55), (**Table 4**).

*Dioscorea alata, Dioscorea praehensilis,* and *Dioscorea bulbifera* are endowed with useful antioxidant activities. Studies have reported that *D. bulbifera* and *D. praehensilis* have a hypoglycemic and antihyperglycemic effects [59].


*(\*) Antioxidant activities were evaluated using gallic acid and quercetin as controls. (IC50 Gallic acid: 0.71 ± 0.08 and 1.07 ± 0.10; Quercetin: 1.42 ± 0.04 and 3.21 ± 0.99 in ABTS and DPPH tests, respectively).*

### **Table 3.**

*Antioxidant activities of Congolese traditional mushrooms.*

The spontaneous flora of the DRC is very rich in food fruits called wild fruits and seeds, which unfortunately are little valued by the population. These fruits are rich in polysaccharides, micronutrients (vitamins, minerals), and secondary metabolites, such as polyphenols, whose therapeutic benefits are well known (**Table 5**).

*Congolese Traditional Foods as Sources of Antioxidant Nutrients for Disease Prevention DOI: http://dx.doi.org/10.5772/intechopen.109319*


*(\*) Antioxidant activities were evaluated using gallic acid and quercetin as controls. (IC50 Gallic acid: 0.71 ± 0.08 and 1.07 ± 0.10; Quercetin: 1.42 ± 0.04 and 3.21 ± 0.99 in ABTS and DPPH tests, respectively).*

*(-) not determined*

### **Table 4.**

*Antioxidant activities of Congolese edible yams.*


### **Table 5.**

*Antioxidant activities of fruits and seeds.*

*Afromum melegueta* contains a high content of polyphenols and the best antioxidant activity. Their content in gingerol, shogaol, paradole, and oleanolic acid would be responsible for their hypocholesterolemic, antitumor, anti-inflammatory, antimicrobial, and antidiabetic properties [60].

Entomophagy is remarkably ingrained in food habits in DRC, seeing that edible insects are considered a valuable traditional food for long and a sustainable source of proteins and vitamins. Study by Nsevolo et al (2021) listed 148 Congolese edible insects identified at species (100 genera, 31 families, and 9 orders dominated by the orders Lepidoptera, Orthoptera, Coleoptera, and Hymenoptera). Insects are part of the regular diet of more than two billion people around the world are delicacies [61]. In the Democratic Republic of the Congo (DRC), caterpillars are the most consumed insects, and they are consumed by more than 70% of the population throughout the year **Table 6**.

Insects are not only valuable sources of lipids, polysaccharides, proteins, and micronutrients but also are sources of bioactive compounds such as phytochemicals with numerous therapeutic properties. Anti-inflammatory, antioxidant, anticancer,


### **Table 6.**

*Antioxidant activities of insects.*

and antimicrobial activities have been reported for the major phenolic compounds found in insects like kaempferol and quercetin when they are directly extracted from plants [62].

### **9. Conclusion**

Oxidative stress, characterized by excessive production of reactive species, is involved in several chronic diseases such as cardiovascular, chronic obstructive pulmonary, sickle cell, chronic kidney, neurodegenerative, and cancer. The data reported in the tables above clearly showed that traditional foods from the biodiversity of the Democratic Republic of Congo are often unvalued, and constitute a potential source of new natural antioxidants. Indeed, the vegetables, mushrooms, yams, nuts, and fruits studied contain polyphenolic compounds, terpenes, and micronutrients, responsible for their antioxidant activities. As Congolese diets, particularly in rural areas, are based on vegetables, such as mushrooms, yams, nuts, and herbs as drinks,

### *Congolese Traditional Foods as Sources of Antioxidant Nutrients for Disease Prevention DOI: http://dx.doi.org/10.5772/intechopen.109319*

there is reason to consider that Congolese traditional foods are a rich source of antioxidant phytonutrients, which brings several health benefits for the population, including the prevention or management of cardiovascular diseases, neurodegenerative disorders, cancer, autoimmune diseases, and diabetes. Considering the importance of oxidative stress on human health, promoting research with a view to valuing the natural antioxidants of biodiversity in Africa, could pave the way toward the discovery of specific natural antioxidant to prevent or treat such and other chronic diseases not transmissible.

### **Author details**

Théophile Mbemba Fundu1 , Paulin Mutwale Kapepula2 \*, Jean Paul Nzundu Mbo1 , Justin Mboloko Esimo3 and Nadège Ngombe Kabamba2

1 Faculty of Sciences, Laboratoire d'analyses et de Recherches sur les Aliments et la Nutrition (LARAN), Department of Biology, University of Kinshasa, Kinshasa, Democratic Republic of Congo

2 Faculty of Pharmaceutical Sciences, Centre d'Etudes des Substances Naturelles d'Origine Végétale (CESNOV), University of Kinshasa, Kinshasa, Democratic Republic of Congo

3 Faculty of Medicine, University of Kinshasa, Democratic Republic of Congo

\*Address all correspondence to: garaphmutwal@yahoo.fr

© 2023 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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### **Chapter 5**

## Recent Development in Antioxidant of Milk and Its Products

*Fouad M.F. Elshaghabee, Ahmed A. Abd El-Maksoud and Gustavo M. Ambrósio F. de Gouveia*

### **Abstract**

Free radicals are produced in humans through natural metabolism or the external environment, such as diet. These free radicals are neutralized by the antioxidant system, whereas enzymes, for example, catalase, superoxide dismutase, and glutathione peroxidase, play an important role in preventing excessive free radicals. Food antioxidants give a good hand in enhancing the human antioxidant system; high consumption of a diet rich in natural antioxidants protects against the risk of diseases such as cardiovascular, cancer, diabetes, and obesity. Milk and its products are popular for a wide range of consumers. Milk contains casein, whey protein, lactoferrin, milk lipid and phospholipids, vitamins, and microelements, for example, selenium (Se), which have antioxidant properties. Furthermore, probiotication of milk either sweet or fermented could enhance the antioxidant capacity of milk. This chapter focuses on presenting recent review data on milk components with antioxidant activity and their health benefits, probiotics as antioxidant agents, and methods for enhancing the antioxidant capacity of dairy products. The key aim of this chapter is to focus on major strategies for enhancing the antioxidant capacity of milk and its products.

**Keywords:** essential oils, plant extracts, probiotication, dietary management, metabolic diseases, antioxidant capacity of milk

### **1. Introduction**

Reactive species are formed during different cellular process, especially during mitochondrial respiratory chain. Reactive oxygen species (ROS) and reactive nitrogen species (RNS) are major reactive species that act as second messengers to regulate biological processes. However, they could cause oxidative stress and protein and DNA damage, which may cause different diseases such as atherosclerosis, diabetes, accelerated aging, and cardiovascular diseases [1].

Milk as a natural product is the first food for humans, and dairy products represent approximately 25–30% of an individual's diet. It also contains different components with antioxidant activity such as casein, whey protein, sulfur-containing amino acids cysteine, conjugated linoleic acid, and catalase that could restore the antioxidant system of the host [2]. Supplementation of milk with natural sources represents a dietary strategy in order to enhance the antioxidant capacity of milk and its products. Essential oils (EO)

are volatile hydrophobic liquids that are extracted from a wide range of plants. They also possess different therapeutic effects, for example, anti-inflammatory and anti-microbial activities [3]. Supplementation of butter oil/ghee with different concentrations of essential oils (glove, garden cress, and jojoba) enhances its antioxidant capacity and shelf life [4, 5]. Furthermore, addition of ethanol extraction of pomegranate peels to ghee enhances the oxidative stability [6].

Probiotication means addition of probiotics (beneficial microbes for the host) to food products. It was considered as a dietary strategy for enhancing the antioxidant capacity of different fermented milk products through the ability of different probiotic strains, for example, *Lb. casei* shirota strain, to produce different metabolites from lactose fermentation or milk protein hydrolysis [7, 8]. This chapter aims to present the recent knowledge on the antioxidant potential of milk and major methods for enhancing the antioxidant capacity of dairy products.

### **2. Milk component with antioxidant activities: an overview**

The antioxidant components in milk could be classified as non-enzymatic compounds, for example, milk proteins, and enzymatic antioxidants, for example, superoxide dismutase (SOD). **Figure 1** shows both selected antioxidant categories in milk. Casein is a major milk protein, accounting for 80% of the total protein in cow milk, and it presents in macromolecule aggregates because of the phosphorus content of casein [9]. Furthermore, the primary structure of casein has free radical scavenging activity [10]. Casein-derived phospho-peptide and phosphoserine residues can bind the non-heme iron [11]. Results obtained by Çekiç et al. [12] showed that β-casein fraction exhibited high antioxidant activity due to the presence of proline residues.

Whey protein as an antioxidant agent was used for inhibiting lipid peroxidation. The antioxidant activity of whey protein is due to its content of sulfur-containing amino acids. Addition of whey protein to soybean and salmon oils increased the oxidative stability of these products [13, 14]. The antioxidant activity of lactoferrin is due to iron-chelating activity and inhibits pro-oxidant effect and release of ROS by leucocytes [15, 16].

### **Figure 1.**

*The major two antioxidant categories in milk. SOD: super oxide dismutase, CAT: catalase, GSHPx: glutathione peroxidase.*

*Recent Development in Antioxidant of Milk and Its Products DOI: http://dx.doi.org/10.5772/intechopen.109441*

Vitamins (soluble in either milk fat or milk serum) and minerals play an essential role as antioxidant factors. The antioxidant capacity of vitamins E (α-tocopherol), A, and C (ascorbic acid) as well as carotenoids is due to their ability to scavenge free radicals (mainly oxygen, hydroxyl, and peroxyl radicals), inhibit lipid peroxidation, and protect DNA from damage [17, 18]. Supplementation of milk with ascorbic acid in light-exposed milk enhanced the antioxidant capacity of milk and inhibited the degradation of riboflavin [19]. Moreover, fortification of cheddar cheese with vitamin E and selenium (Se) enhanced the oxidative stability of cheddar cheese and its shelf life [20].

Feeding strategies of dairy animals has a potential impact on levels of polyphenols, changes in amino/fatty acid composition in milk, and its overall antioxidant capacity [21]. In this respect, feeding dairy cow with carrot results in increased levels of β-carotene and α-tocopherol in milk [22]. Also, supplementation of animal feeds with fish oil and grazing improved the antioxidant capacity of cow and sheep milk, respectively [23, 24]. Recently, supplementation of grazing with tannin for dairy cow has enhanced the status of antioxidant capacity of blood plasma and cheese [25].

Enzymatic antioxidant in milk includes super oxide dismutase (SOD), glutathione peroxidase (GSHPx), and catalase (CAT). SOD safeguards cells from superoxide free radicals and lipid peroxidation [26]. Levels of SOD in cow milk range from 0.15 to 2.4 mg/L. However, the content of SOD in human milk is higher than (2.0–2.3 times) in cow milk [27]. GSHPx (Se encompassing enzyme) plays an important role in protection from lipid peroxidation [28]. Also, human milk has a higher concentration of GSHPx than caprine and cow milk [29]. A decrease in levels of selenium content and antioxidant activity could be detected with the progression of lactation [30]. Catalase (CAT: heme protein with molecular weight = 200KDa) has a dismutation effect against hydrogen peroxide [31]. The concentration of CAT in human milk is 10 times more than in cow milk, whereas the content of CAT in cow milk is approximately 1.95 U/mL [32].

### **3. Natural plant extracts for enhancing the antioxidant capacity of milk and its products**

In recent years, there has been high focus toward the field of antioxidants and the reduction of free radicals. Milk and dairy products are essential components of human nutrition, and they are considered the carriers of several bioactive compounds that are important for a variety of biochemical and physiological functions. Milk and dairy products (yogurt and cheese), accounting for approximately 25–30% of the average human diet, are undoubtedly a rich source of compounds exhibiting antioxidant properties. Additionally, it is worth emphasizing that regular consumption of natural dairy antioxidants minimizes the risk of development of civilization diseases (e.g., cardiovascular disease, cancer, or diabetes). It also slows down the aging process in the organisms [33].

On the other hand, the consumption of natural antioxidant-rich foods improves an organism's antioxidant status by protecting it from oxidative stress and damage. Consumption of food products that are rich in natural antioxidants improves the antioxidant status of an organism through protection against oxidative stress and damage [34]. The antioxidant status of milk and dairy products can be improved with the use of natural additives in animal nutrition or at the stage of milk processing. Herbal mixtures, seeds, fruits, and waste from the fruit and vegetable industry are used most commonly [35]. Commercially, cheddar cheese was fortified by chili and red pepper by Monterey Jack Co., California, USA. Also, Khaled Khoshala for industry and trading Co., Obour city, Egypt, manufactured Egyptian soft cheese (Gebna Bida) and processed cheese fortified with green and red pepper that enhanced the shelf life of final products.

Numerous studies have tried to enhance antioxidant activities of foods by mixing them with phenolic components [36, 37]. Examples constitute the non-covalent complexes of polyphenols and proteins in foods [38, 39]. However, these types of interactions have been shown to alter the structure, function, stability, and nutritional properties of the complex [40, 41]. Though these methods are relatively cheaper, they are largely ineffective due to the reversible nature of the interactions between proteins

### **Figure 2.**

*Individual amino acids consist of a primary amine, a carboxylic acid group, and a unique side-chain structure (R).*

### **Figure 3.**

*Derivatives of carboxylic acids can be interacted through the use of active intermediates that react with target functional groups, NHS: N-hydroxysuccinimide; EDC: N-(3-imethylaminopropyl)-N*′*-ethylcarbodiimide hydrochloride.*

### *Recent Development in Antioxidant of Milk and Its Products DOI: http://dx.doi.org/10.5772/intechopen.109441*

and phenolic acids, which leads to an unstable complex for food processing conditions. Thus, covalently linking phenolic acids to proteins might be a way to generate a more stable antioxidant for food [42].

Bioconjugation involves the linking of two or more molecules to form a novel complex having the combined properties of its individual components. Natural or synthetic compounds with their individual activities can be chemically combined to produce unique substances possessing multifunctional characteristics. A protein that can bind discretely to a target molecule through the functional groups (**Figure 2**) within a complex mixture can thus be crosslinked with another detectable molecule to form a traceable conjugate. The conjugation techniques are dependent on the functional groups present on the target macromolecules to be modified. Protein molecules are the most common targets for modification with natural antioxidants such as phenolic acids (**Figure 3**) [43, 44].

### **4. Dairy products fortified with essential oils as antioxidant promoters**

The control of free radicals, prooxidants, and oxidation intermediates is used to protect the protein and lipid components of food from oxidation [45]. In addition to oxidative damage and death of cells, tissue damage and various pathological conditions may be the consequence of oxidative stress. Deleterious changes in dairy products caused by lipid oxidation include not only flavor loss or the development of off-flavors but also color loss, nutrient value loss, and the accumulation of compounds that may be harmful to consumers' health. One of the most effective ways of reducing the lipid oxidation in dairy products is to incorporate antioxidants [46].

Free radical scavengers (FRS) inhibit lipid oxidation by reacting faster than unsaturated fatty acids with free radicals. Synthetic antioxidants such as butylated hydroxytoluene (BHT) and butylated hydroxyanisole (BHA) are widely used to prevent lipid oxidation (BHA). However, large amounts of these synthetic ingredients have been linked to carcinogenic and cytotoxic effects. Therefore, the focus has shifted toward the use of natural antioxidants such as essential oils and phenolic acids [43]. Essential oils are liquid aromatic substance, and they are extracted from plants that have been proven to be good sources of bioactive compounds with antioxidative and antimicrobial properties. Essential oils play a high role as good free radical scavengers. Also, natural essential oils have to be given a lot of interest for enhancing overall well-being, in the prevention of diseases and in the incorporation of health-promoting substances into the diet [47]. Additionally, the use of essential oils as natural antioxidants in dairy products can reduce the rate of lipid oxidation and hydrolysis and may be beneficial in increasing the shelf life of these products [46]. Marjoram, frankincense, thyme, myrtle, lemon, oregano, and lavender essential oils are commonly used as food additives. These supplementations will move the dairy products into the functional food area as healthy dairy products.

Different essential oils extracted from plant sources such as cumin, rosemary, and thyme and their mixtures have been studied for their effect on physicochemical, microbial, rheological, and sensorial attributes of ultra-filtrated (UF)-soft cheese. The results revealed that the different essential oils had remarkable antimicrobial effect on the growth of pathogenic bacteria (i.e., *Escherichia coli*, *Salmonella typhimurium*, *Staphylococcus aureus*, *Bacillus subtilis*, *Bacillus cereus*, and *Aspergillus niger*) [48].

### **5. Impact of probiotication of dairy foods on enhancement of their antioxidant capacity**

Probiotics are *live microorganisms, which when administered in adequate amounts confer health benefits to the host* [49]. A recent definition of probiotics by Elshaghabee [50] was probiotics are live microbial strains with health impact on host when they consumed daily with enough amounts (not less than 106 –108 CFU/g) and incorporated into the gut micro-biome. The main two genera of probiotics are *Lactobacillus* (*Lb.*) and *Bifidobacterium*. Different studies had led to a renewed interest in probiotics as antioxidant agents. Isolated *Lb. fermentum* from GIT mucosa could scavenge free radicals using *in vitro* model and enhance the antioxidant status and health of pigs [51]. Probiotic yeast *Sacch. cerevisiae* DSMZ strain had higher antioxidant capacity than *Lb. casei* 01 and bifidobacteria B-12 in either viable or non-viable form [52].

A mixture of probiotic bacteria containing *Lb. acidophilus* W70, *Lb. casei* W56, *Lb. salivarius* W24, *Lactococcus lactis* W58, *Bifidobacterium* (Bif.) *bifidum* W23, and *Bif. lactis* W52 enhanced de novo synthesis of GSH under severe acute pancreatitis in a rat model [53]. Furthermore, Spyropoulos et al. [54] reviewed that several probiotic species, for example, *L. lactis* and *Lb. plantarum*, could produce SOD, resulting in a protective effect against radiation-induced enteritis and colitis. Also, some species of probiotic bacteria could produce folate, which could enhance the antioxidant capacity [55].

Feeding mice with engineered *Lb. casei* BL23-producing SOD could significantly decrease the intestinal inflammation in mice with Crohn's disease [56]. Feeding boiler with spore-forming probiotics *Bacillus coagulans* could enhance the antioxidant capacity, immunity, and gut function [57]. In a human experiment, the status of total antioxidant capacity of type 2 diabetic patients was enhanced when they received yogurt containing *Lb. acidophilus* La 5 and *Bif. lactis* Bb-12 [58]. All health benefits of spore-forming probiotics with their future prospects were reviewed by Elshaghabee et al. [59].

Gut microbiota, including probiotics, has a protective effect against pathogens by competitive exclusion [60]. Imbalance in the composition of gut microbiota resulted in increased levels of ROS and could affect redox homeostatic in the host [61]. Probiotics can regulate positively the composition of gut microbiota through different mechanisms, for example, producing a wide range of organic acids, mainly lactic and acetic. Propionic and butyric acids produced from cross feeding of lactate by other gut microbiota resulting in lowered the pH of colon and inhibiting the growth of a wide range of pathogens as well as other harmful bacteria [62, 63].

Probiotic *Lb. johnsonii* BS15 could attenuate high fat diet that induced oxidative stress and modulated the ratio of *Firmicutes*/*Bacteroidetes* in mice model [64]. Also, supplementation of probiotic ABT-fermented milk with heat-treated *Sacch. cerevisiae* could significantly enhance the antioxidant capacity of the product [65]. Recently, lased-treated *Lb. casei* had higher free radical scavenging activity than nontreated cells [66, 67].

*Akkermansia (A.) muciniphila* represents a new generation of probiotics; it is an intestinal mucin-degrading bacterium, and it could regulate blood pressure, and it could release the endogenous hydrogen sulfide (H2S), which has been considered a potential regulator of vascular homeostasis, possibly through the regulation of vascular tone and inflammation, antioxidant mechanism, vascular cell proliferation, and apoptosis [68]. Data in **Figure 4** conclude different possible mechanisms of antioxidant activity of different probiotic genera.

### **Figure 4.**

*Selected different possible mechanisms of probiotics as antioxidant food supplements.*

### **6. Conclusion**

In the past few years, there has been an increasing demand for natural products with antioxidant activity as well as dairy foods. Milk is the first food for mammalians. It contains different antioxidant components that cleared in this chapter. The use of different plants or herbs has been was in practice from the ancient time. Fortification of different dairy products with either plant extracts or essential oils enhanced the antioxidant capacity and quality parameters including shelf life of these products. Recently, different species of probiotics could be used also for enhancing the antioxidant capacity of fermented milks. This chapter reveals that consumers could use different methods for enhancing the antioxidant status of dairy products resulting in an enhancement the health status of consumers which serve the sustainable development goals SDG 3 (good health and wellbeing).

### **Author details**

Fouad M.F. Elshaghabee1 \*, Ahmed A. Abd El-Maksoud1 and Gustavo M. Ambrósio F. de Gouveia<sup>2</sup>

1 Dairy Science Department, Faculty of Agriculture, Cairo University, Giza, Egypt

2 LEAF - Linking Landscape, Environment Agriculture and Food, Instituto Superior de Agronomia da Universidada de Lisboa, Lisboa, Portugal

\*Address all correspondence to: elshaghabee@agr.cu.edu.eg

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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### **Chapter 6**

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

*Dennis R.A. Mans*

### **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.

**Keywords:** reactive oxygen species, antioxidants, fruits, Suriname, anthocyanins, ellagitannins, coumarins

### **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 [5–7]. 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 [5–7]. ROS are able to readily react with and cause damage to biomolecules including proteins, lipids, and nucleic acids, leading to cell and tissue injury [8–10]. 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 [8–10].

ROS are mainly generated in cellular organelles where oxygen consumption is high, such as mitochondria, peroxisomes, and endoplasmic reticulum [11–13]. 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 [18–24].

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

### *Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110078*

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 [29–31, 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 [35–37]. 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 [29–31, 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 [18–22].

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].

The country's land area of roughly 165,000 km<sup>2</sup> 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 *Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110078*

### **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).*

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, 66–68] and/or used as traditional medicines [69–78]. 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 [69–78]. The plants addressed in both parts of this chapter as well as their relevant characteristics are given in **Table 1**.


*Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110078*

### **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 healthpromoting 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 [89–91]. 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 [97–100]. Anthocyanidins exist in a variety of chemical forms depending on the conditions of the medium, which result in differently colored or colorless compounds [97–100]. 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 [97–100].

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

### *Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110078*

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, [103–105]). And in accordance with the apparent antioxidant and antiinflammatory 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, 106–108]).

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 [97–100] 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 [109–112], 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

### **Figure 2.** *Bunch of fruits of the açai* Euterpe oleracea *Mart. (Arecaceae) (from: https://images.app.goo.gl/22sjzvsep94caDv2A).*

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.

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, 116–120]. 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, 119–122]. Particularly, the antioxidant properties of *E. oleracea* fruit preparations have been well investigated, showing an abundance of phenolic compounds with antioxidant activity [123–127], supporting some of their traditional and nutraceutical uses [79, 119–127].

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, 119–122].

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 [97–100, 109–112]. For this reason, the possibility exists that other, more stable phenolic compounds, vitamins, and/or fatty acids [99, 113] in *E. olerace*a 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

### *Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110078*

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, waterinsoluble 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.

*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, 156–158]. 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 [161–164], 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,

### **Figure 3.**

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

*Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110078*

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 viv*o 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 pyronesubstituted 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 systemstimulating, and menopausal distress-preventing effects [180–182]. 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, [184–186]). 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].

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 [180–182]. 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].

### **Figure 4.**

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

*Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110078*

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 phenylpropanoidderived 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) [200–202] might be due to the combined actions of selenium with phenolic compounds, tocopherols, and unsaturated fatty acids [203–206].

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 [97–100, 109–112], 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].

### **Author details**

Dennis R.A. Mans Faculty of Medical Sciences, Department of Pharmacology, Anton de Kom University of Suriname, Paramaribo, Suriname

\*Address all correspondence to: dennismans16@gmail.com; dennis\_mans@yahoo.com

© 2023 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110078*

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### **Chapter 7**

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

*Dennis R.A. Mans*

### **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.

**Keywords:** antioxidants, fruits, Suriname, (pro)vitamin A, vitamin C, vitamin E, selenium

### **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 [5–7]. 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 [5–7]. ROS are able to readily react with and cause damage to biomolecules including proteins, lipids, and nucleic acids, leading to cell and tissue injury [8–10]. 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 [8–10].

ROS are mainly generated in cellular organelles where oxygen consumption is high, such as mitochondria, peroxisomes, and endoplasmic reticulum [11–13]. 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 [18–24].

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

### *Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110079*

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 [29–31, 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 [35–37]. 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 [40–49]. The plants addressed in both parts of this chapter as well as their relevant characteristics are given in **Table 1**.

### **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


### **Table 1.**

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

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].

*Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110079*

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 oxidasereductase 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 [67–71]. Not surprisingly, diets high in carotenoids have been associated with a lower risk of, among others, heart disease, lung cancer, and diabetes mellitus [72–74]. 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].

*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 antiinflammatory 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 [83–85] which have been shown to be partly responsible for the biological properties

*Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110079*

**Figure 1.** *Fruits of the tucumã Astrocaryum vulgare Mart. (Arecaceae) (from: https://images.app.goo.gl/ ohwh8G8BwHZBiUk8A).*

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 [98–101]. 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 (semidehydrovitamin C) with a lifetime of 10–15 s [107, 108]. In a subsequent electrondonating 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].

*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

*Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110079*

**Figure 2.** *Fruit of the acerola Malpighia glabra L. (Malpighiaceae) (from: https://images.app.goo.gl/SXvp1ifwFFRWLm TU7).*

from *M. glabra* fruit extracts showed, among others, anti-inflammatory, antihyperglycemic, antitumor, antigenotoxic, and hepatoprotective activity [115–118].

The beneficial health effects of *M. glabra* fruit have been associated with its powerful antioxidant effects in several *in vitro* assays [119–121] 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, 122–125]. 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, 128–130]. 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 [135–137]; 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].

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 [148–151]. Due to this favorable

*Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110079*

**Figure 3.** *Calyx of the roselle Hibiscus sabdariffa L. (Malvaceae) (from: https://images.app.goo.gl/5M5iBiBb4nHwcTFk6).*

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 [163–165] 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 [166–168]. They can be classified into macroelements, microelements, and trace elements [166–168]. 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 [166–168]. 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 [166–168]. 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 [166–168]. They fulfill more or less the same functions as the macroelements but are required in smaller amounts [166–168].

Trace elements are present in the body at concentrations of much less than 0.1% and are required in parts per million [166–168]. Nevertheless, in these minute amounts, they are vital for proper growth and development and are therefore also referred to as essential minerals [166–168]. They include, among others, iron, copper, zinc, molybdenum, manganese, chromium, cobalt, cadmium, and selenium [166–168]. 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 [166–168].

### *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 [166–168]. 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].

### *Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110079*

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 [188–190]. 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.

*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 [198–200]. It is used in creams, lotions, conditioners, and hair care products, as well

### **Figure 4.**

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

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

*Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110079*

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, 198–200], 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 [204–206] might be due to the combined actions of selenium with phenolic compounds, tocopherols, and unsaturated fatty acids [181, 198–200]. 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, 210–212].

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, 213–218], 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].

### **Author details**

Dennis R.A. Mans Faculty of Medical Sciences, Department of Pharmacology, Anton de Kom University of Suriname, Paramaribo, Suriname

Address all correspondence to: dennismans16@gmail.com; dennis\_mans@yahoo.com

© 2023 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*Naturally Occurring Antioxidants in Seven Well-Known Fruits from the Republic of Suriname… DOI: http://dx.doi.org/10.5772/intechopen.110079*

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### **Chapter 8**

## Antioxidant Activity of *Nigella sativa* Essential Oil

*Kehinde Sowunmi and Zeenat Kaka*

### **Abstract**

*Nigella sativa* oils have anti-inflammatory, antibacterial, antifungal, antiparasitic and antiprotozoal, antiviral, cytotoxic, anticancer, neuro-, gastro-, cardio-, and hepatoprotective properties, making them potential treatments for a wide range of illnesses. *N. sativa* oil also suggests positive benefits on the immunological, respiratory, and reproductive systems in addition to diabetes mellitus (DM), fertility, breast cancer, dyspepsia, osmotic balance, and other conditions. Thymoquinone (TQ ) is a suitable target for its potential antibacterial, antimicrobial, anti-inflammatory, chemopreventive, antitumoral, and other actions among the various isolated chemical moieties. The *N. sativa* oil has been shown in various non-clinical and clinical investigations to benefit health. On the other hand, TQ in several animal experiments is clear to generate no adverse modifications of the body biomarkers; rather, it enhanced health quality. This study presents a more mechanistic review of the constitutions and oil of *N. sativa*. In conclusion, research on Nigella oil may represent a health breakthrough.

**Keywords:** *Nigella sativa*, antioxidant, essential oils, potential treatment, thymoquinone (TQ )

### **1. Introduction**

*Nigella sativa* L. is a short shrub of the Ranunculaceae botanical family. It is native to Southern Europe, North Africa, and Southeast Asia, and it is grown in a variety of nations across the world. Green leaves and 5–10 petalled rosaceous white, yellow, pink, pastel blue, or purple blooms. The mature fruit bears several small dark black seeds. The oil of *N. sativa* was widely utilised in traditional Asian and Middle Eastern medicines [1]. However, *N. sativa* has been used to treat a wide range of ailments affecting the respiratory system, digestive tract, cardiovascular system, kidney, liver, and immunological system. It has long been used to treat weariness and depression. Ailments such as asthma, bronchitis, rheumatism and associated inflammatory illnesses, indigestion, lack of appetite, diarrhoea, dropsy, amenorrhea, dysmenorrhea, worms, and skin eruptions are among the most prevalent traditional applications. It's both an antiseptic and a local anaesthetic [2].

Protein, fat, carbohydrates, crude fibre, total ash, volatile oil, fatty oil, cellulose, and moisture are all present in black seed oil [3]. The oil is also a good source of minerals including Ca, K, Se, Cu, P, Zn, and Fe, as well as several vitamins like A, B1, B2, and C. Additionally, seeds, roots, and shoots contain both carotenes and vanillic acid.

The primary unsaturated fatty acids include linolic acid, oleic acid, diomolinoleic acid, and eicosadienoic acid, which are found in fatty components. The two primary saturated fatty acids that palmitic acid and stearic acid are a part of our -sitosterol and stigmasterol [2]. According to Gharby et al. [4], other fatty acids include myristic acid, palmitoleic acid, linoleic acid, linolenic acid, arachidonic acid, cholesterol, campesterol, β-sitosterol, 5-avenasterol, and 7-avenasterol. The alkaloids in the oil are either imidazole ring-bearing alkaloids, pyrazole alkaloids, or isoquinoline alkaloids. Terpenes and saponins are also found in them. Evidence suggests that the most significant active ingredients in *N. sativa* include thymoquinone (TQ ), thymohydroquinone, dithymoquinone, p-cymene, carvacrol, 4-terpineol, t-anethol, sesquiterpene longifolene, −pinene, and thymol, among others. Carvone, nigellicine, nigellone, citrostradienol,

**Figure 1.** *Some important chemical moieties isolated from* N. sativa*.*

*DOI: http://dx.doi.org/10.5772/intechopen.109086 Antioxidant Activity of* Nigella sativa *Essential Oil*

cycloeucalenol, gramisterol, lophenol, ostusifoliol, stigmastanol, β -amyrin, butyrospermol, and cycloartenol are the other chemical components [2, 5] bitter principle, tannin, resin, reducing sugars, glycosidal saponin, hederagenin glycoside, esters of unsaturated fatty acids with C15 terpenoids, esters of dehydrostearic and linoleic acid, aliphatic alcohol, −unsaturated hydroxyl ketone, 3-O-[12-L-rhamnopyrasyl(12)- D-glucopyranosyl)-L-xylopyranosyl (12)] Stigma-5,22-dien-3-D-glucopyranoside, cycloart-23-methyl-7,20,22-triene-3, 25-diol, nigellidine-4-O-sulphite, 11-methoxy-16, 23-dihydroxy-28-methylolean-12-enoate, N. mines A1, A2, B1, and B2 in addition to A3, A4, and A5 [1, 6–16]. The chemical structures of some important chemical moieties are shown in **Figure 1**.

### **2. Activities of** *N. sativa* **oil**

### **2.1 Antibacterial agent**

According to reports, *N. sativa* has potent antibacterial activity against both gram-positive and gram-negative microorganisms. It has additive effects with spectinomycin, erythromycin, tobramycin, doxycycline, chloramphenicol, nalidixic acid, ampicillin, lincomycin, and co-trimoxazole and exhibits synergistic effects with streptomycin and gentamycin. It also functions similarly to topical mupirocin. It can combat resistant microorganisms, including many gram-positive and gram-negative bacteria that are multi-drug resistant [17]. Manju et al. [18] claim that an oil extract from Nigella can guard against *Vibrio parahaemolyticus* Dahv2 infection in Artemia spp. TQ has demonstrated anti-methicillin-resistant action in *Staphylococcus aureus*, according to Hariharan et al. [19].

### **2.2 Antiviral agent**

It has been demonstrated that *N. sativa* increases the ratio of helper to suppressor T cells in people as well as the activity of natural killer (NK) cells. Otherwise, it is an effective inhibitor of murine CMV and HIV protease. In the latter instance, it was discovered that the generation of interferon-gamma (INF-) led to an increase in the quantity and functionality of M-phi and CD4 + ve T cells [7, 8, 17].

### **2.3 Antifungal activity**

When used against Aspergillus niger, Fusarium solani, and Scopulariopsis brevicaulis, *N. sativa's* isolated chemical, TQ, was shown to be more efficient than griseofulvin and amphotericin-B. It also has antifungal action against *Candida albicans* and Madurella mycetomatis. The TQ also works well against Microsporum spp., Trichophyton spp., and Epidermophyton spp. Additionally, against a variety of clinical isolates, such as dermatophytes, moulds, and yeasts, thymohydroquinone and thymol also displayed an antifungal activity [9, 10, 20]. It is also obvious that black seed oil (10–200 g/mL) acts against *Saccharomyces cerevisiae* and C. utilise [21].

### **2.4 Effects on parasites**

It has been demonstrated that *N. sativa* oil has potential against leishmaniasis, miracidia, cercariae, and *Schistosoma mansoni*. In the latter instance, co-treatment with praziquantel, a well-known anti-schistosomal and anthelmintic medicine for domestic animals, resulted in a potentiating effect from the oil of the black seed, which demonstrated high efficacy [13–16]. According to Simalango [22], ethanol extract of *N. sativa* (0.5–8%) exhibited anti-Ascaris suum action that was noticeably active.

### **2.5 Effect on wound infection**

The ability of *N. sativa* oil to speed up the healing of wounds in mice, farm animals, and human gingival fibroblasts was examined. The accumulation result showed that the absolute difference in WBC counts, local infection and inflammation, bacterial growth and tissue damage, and free radical generation had all decreased. Additionally, transforming growth factor beta and basic fibroblast growth factor levels were found to be higher [17]. Studies using *N. sativa* extracts, seed oil, and TQ have been done on the antioxidant activity of Nigella. The research indicates that oxidative stress may have both potential anti-radical and inhibitory effects. Adenosine deaminase (ADA), catalase (CAT), myeloperoxidase (MPO), lipid peroxidase (LPO), reduced glutathione (GSH), glutathione-S-transferase (GSH-ST), glutathione peroxidase (GPx), superoxide dismutase (SOD), and nitric oxide were among the measures that TQ significantly altered (NO). In addition, it decreased levels of malonilealdehyde (MDA), conjugated diene (CGD), tumour necrosis factor-alpha (TNF-), interferon-gamma (IFN-), and prostaglandin (PGE2) rather than interleukin-10 (IL-10) and other pro-inflammatory mediators [2, 23].

### **2.6 Anti-inflammatory diseases**

*N. sativa* extracts, seed oil, and TQ may have anti-inflammatory properties, according to research using several animal models. The lowering of NO synthesis, interleukin-1 (IL-1), cyclooxygenase-1 (COX-1), cyclooxygenase-2 (COX-2), histone deacetylase (HDAC), and other pro-inflammatory mediators, including IL-1, IL-6, TNF-, IFN-, and PGE2, is a function of this activity [1, 11]. In mice, topical TQ treatments increased the expression of heme oxygenase-1, NAD(P)H-quinone oxidoreductase-1, glutamate cysteine ligase, GSH-ST, and other enzymes, but rat seed oil inhibited COXs and 5-LPO in the pathways of arachidonate metabolism [17]. TQ has also been demonstrated to reduce nuclear translocation and nuclear factor-kappa-B (NF-B) DNA binding in mice by preventing I-phosphorylation Bs and subsequent degradation. TQ also reduced the phosphorylation of p38 mitogen-activated protein kinase, c-Jun-Nterminal kinase (c-JUNK), and protein kinase B (Akt) (MAPK–p38). The inactivation of caspase-1 was followed by the suppression of IL-1 and IL-18 in B16F10 mice whose expression of NLRP3 (NACHT, LRR, and pyrin domain-containing protein 3) was reduced. Additionally, the NLRP3 inflammasome was partially inactivated as a result of TQ's inhibitory action on NF-B and reactive oxygen species (ROS) [17, 23, 24].

### **2.7 Anticancer**

The capacity of black seed oil to boost NK cells makes it potentially useful in immune treatment. Oil's constituents, however, may have a carcinogenic impact due to prooxidant effects caused by antioxidants. TQ was also evaluated on a variety of cancer cells generated from mice, indicating its capacity to stop G0/G1 phases of the cell cycle, which coincided with rapid increases in the expression of the cyclindependent kinase p16 (CDK-p16) and a drop in cyclin-d1 (dcl-1) protein expression

*DOI: http://dx.doi.org/10.5772/intechopen.109086 Antioxidant Activity of* Nigella sativa *Essential Oil*

in papilloma (SP-1) cell line, and G2/M arrest connected with an increase in the production. The chemopreventive potential of TQ may be attributed to its capacity to reduce cyclin-xl (bcl-xl) protein and enhance the ratio of apoptosis regulator (bcl-4)/ cyclin-2 (bax/bcl- 2) expression. Additionally, squamous cell carcinoma (SCC- VII), FsaR, and mouse tumour models of fibrosarcoma and SCC were found to exhibit TQ's anticancer efficacy. TQ significantly increased the sub-G1 population, live/dead cytotoxicity, chromatin condensation, DNA laddering, and Tunel-positive cells in A431 and Hep-2 cells, demonstrating substantial anticancer action through apoptosis. Caspase activation, cell proliferation, cleavage of poly ADP ribose polymerase, and a rise in the bax/bcl-2 ratio were also seen [17]. According to research, TQ caused p53-independent apoptosis in human colon cancer cells, as well as p21 expression, and stopped the S phase of the cell cycle [25]. TQ is a potent down-regulator of NF-B and MMP-9 in Panc-1 cells as well as bcl-2 and an up-regulator of caspase-3 and caspase-9 in gastric cancer cells. It is also an anticancer drug for several cell lines, including MCF-7/Topo breast carcinoma cells. The antitumor action of certain TQ derivatives, including 6-menthoxybutyryl, 6-hencosahexanyl conjugate, 4-acyl hydrazones, and 6-alkyl derivatives, is also visible in cancer cell lines [2].

### **2.8 Effect on diabetes mellitus**

In rats, *N. sativa* was discovered to be crucial in the lowering of blood glucose levels with an increase in insulin and C-peptide levels. TQ lowers tissue MDA levels, DNA damage, mitochondrial vacuolization, and fragmentation, and by acting as an antioxidant, it protects the integrity of pancreatic beta-cells. According to a study, TQ clearly raises insulin and Hb levels while also significantly lowering glucose and HbA1c levels. In T2 D rats, *N. sativa* improved bone mass, connection, biomechanical behaviour, and strength in a synergistic manner with parathyroid hormone [26, 27]. Additionally, it is clear that the black seeds are an effective treatment for those with dyslipidemia and the insulin resistance syndrome. Diabetes patient *Meriones Shawi* treated with *N. sativa* likewise had an insulin-sensitization effect through increased ACC phosphorylation (primarily MAPK signalling pathway) and muscle GLUT4 content as well as gradual restoration of glycemia [1, 28]. In rats with diabetic mellitus (DM) brought on by streptozotocin, lipid and volatile fractions decreased toxicological and unfavourable effects [29]. Additionally, Heshmati et al. [30] reported that therapy with oil at 3 g three times per day might improve glycemic status and lipid profiles in DM patients (n = 72). When TQ was tested in clonal beta-cells and rodent islets, it had a protective effect with normalisation of chronic malonyl CoA accumulation and elevation of acetyl CoA carboxylase (ACC), fatty acid synthase (FAS), and fatty acid binding proteins (FABPs) following chronic glucose overload, suggesting a modification in beta-cell redox circuitry and enhancing the sensitivity of beta-cell metabolic pathways to glucose and glucose-stimulated insulin secretion (GSIS) under both normal conditions and hyperglycemia [31]. Otherwise, MAPK controls several transcriptional variables, the alteration of which disrupts the cell cycle. Therefore, *N. sativa* and TQ may be effective treatments for both type 1 and type 2 DM patients, as maintaining beta-cell integrity and secreting enough insulin to support glycogenesis and the phosphorylation of elevated blood glucose levels are essential in this context. Otherwise, oxidative stress, illness, and trauma are the other variables that raise blood sugar levels in addition to eaten meals. Therefore, the antioxidant, antibacterial, cytotoxic, and anti-inflammatory properties of *N. sativa* and TQ may be related to each other. Otherwise, lowering HbA1c levels is one of the treatments for retinopathy, nephropathy, and cardiovascular disease.

### **2.9 Effect on the immune system**

*N. sativa* is a demodulator of the production of numerous pro-inflammatory mediators, with an increase in the release of Th2 vs. Th1 cytokines in splenocytes, along with NK antitumor activity. Black seed extracts can regain resistance against granulocyte-dependent *C. albicans*. According to research conducted by the oil, the immunosuppressive cytotoxic impact of typhoid immunisation may result in a decrease in antibody production. Additionally, it is clear that the oxytetracycline (OXT)-induced imbalances in leukocyte, lymphocyte, heterophil: lymphocyte, lysosomal enzyme activity, and reticuloendothelial system function need to be addressed. When pigeons received continuous antibiotic therapy, nevertheless, it had an immuno-protective effect. The black seed oil also has radioprotective properties against the oxidative and immunosuppressive effects of ionising radiation. In addition, *N. sativa* oil administration resulted in a rise in IFN- levels and a considerable reduction in the pathological alterations in the guinea pigs' lungs. Additionally, it works well for allergic diarrhoea [1, 23, 24]. Recent research reveals that seed oil can shield the jejunal mucosa from harm caused by -radiation [26]. After 6 weeks of therapy, Nigella EO in hens at doses between 5 and 20 g/kg (oral feed) enhanced FCR, plasma lipid profile, and antibodymediated immunity [32]. Additionally, in individuals with Hashimoto's thyroiditis, nigella oil decreased thyroid stimulating hormone (TSH) and anti-thyroid peroxidase antibodies [12, 33].

### **2.10 Effect on the nervous system (NS)**

The methanolic extract of *N. sativa* is an effective analgesic and antidepressant. Additionally, rat brains showed anxiolytic action by elevating serotonin (5-HT) and lowering hydroxy indole acetic acid (5-HIAA) levels [20]. Rats showed improved learning and memory associated with an increase in 5-HT secretion. It may aid in the treatment of anxiety since it increased the levels of tryptophan [20, 23]. In contrast, TQ decreased the generation of NO and MDA while still having a GABAmediated calming effect in mice [1]. Due to its antioxidant, free radical scavenging, and anti-inflammatory properties, it may have neuroprotective properties.

### **2.11 Effect on the gastrointestinal tract (GIT) system**

TQ is gastroprotective because it increases the quantity and activity of gastric mucin, GSH, total nitric oxide (TNO), and SOD while decreasing stomach acid secretion, acid output (AO), pepsin, mucosal lipid peroxidase (LPO), the proton (H+) pump, MPO, and ulcer index (UI). Prostaglandin (PGD)-mediated and/or via antioxidant and ant secretion pathways were hypothesised to reduce ulcer severity in rats. Rats also showed a decrease in LPO and lactate dehydrogenase (LDH), MPO, MDA, and an increase in GSH, SOD, GPx, and GSH-ST without changing stomach CAT. TQ was discovered to have considerable benefits on inflammatory bowel illnesses, anti-*Helicobacter pylori*, body weight reduction, colitis, and diarrhoea [2].

### **2.12 Effect on the hepatic system**

The hepatoprotective action of *N. sativa* is shown by its effects on the enzymes alanine aminotransferase (ALT), aspartate aminotransferase (AST), LDH, total antioxidant capacity (TAC), CAT, MPO, total oxidative status (TOS), and oxidative *DOI: http://dx.doi.org/10.5772/intechopen.109086 Antioxidant Activity of* Nigella sativa *Essential Oil*

stress index (OSI). Additionally, GSH and TQ enhanced protein carbonyl content, which reduced protein oxidation and improved the cellular fraction's decreased antioxidant levels [1]. Hepatocytes in mouse TIB-73 cells were shielded against N-acetyl-p-aminophenol (APAP)-induced hepatotoxicity and metabolic abnormalities by *N. sativa* oil at a concentration of 25–100 g/mL [34]. With an aqueous extract of *N. sativa*, a comparable activity was also seen by Hamza and Salem Al-Harbi [35]. This activity was assumed to be related to enhancing antioxidant capacity and inhibiting both lipid peroxidation and ROS formation [34]. It is also clear that black seed oil, when administered to rats receiving cisplatin (CP), at a dosage of 2 mg/kg, has hepatoprotective effects via enhancing energy metabolism and fortifying antioxidant defence mechanisms [36].

### **2.13 Effect on the urinary system**

*N. sativa* with ascorbic acid (Vitamin C) reduced serum creatinine (CK), blood urea nitrogen (BUN), and antioxidant activity in rabbits, resulting in a nephroprotective effect. Otherwise, TQ had an impact on the renal expression of organic ion transporters and proteins linked to multidrug resistance in rats. Rats showed lower expression of OAT1, OAT3, OCT1, and OCT2 and increased protein levels of the efflux transporters MRP2 and MRP4. Along with lowering the tubular necrosis score, *N. sativa* is effective at lowering levels of CK, urea, MDA, NO, ROS, OSI, and TOS in kidney tissue and blood while increasing TAC, SOD, and GPx. The gentamicin (GM)-induced change in blood CK, BUN, thiobarbituric acid substances (TBARS), and total bilirubin is reversed by TQ. The black seed ethanol extracts showed considerable nephroprotective effect against paracetamol-induced nephrotoxicity in female Wistar Albino rats at doses of 250-100 mg/kg [37]. Otherwise, Erboga et al. [38] have shown that Cd-induced nephroprotective is also detectable in rats.

### **2.14 Effect on the pulmonary system**

Leukotriene-d4 (LT4) is inhibited by both nigellone and TQ in the trachea, where the activity of the former was determined by mucociliary clearance. The peribronchial inflammatory cell infiltration, alveolar septal infiltration, alveolar edema, alveolar exudates, alveolar macrophages, intestinal fibrosis, granuloma, necrosis formation, NOS, and an increase in surfactant protein D in the pulmonary system were all significantly decreased by *N. sativa*. It is also clear that *N. sativa* protects the lungs from damage brought on by hypoxia and lung injury. *N. sativa* puffs have also been shown to have a bronchodilatory impact on PFT values, frequency of asthma symptoms/weakness, chest wheezing, and asthma symptoms [1].

### **2.15 Effect on the reproductive system**

TQ reduced the levels of TAC and MPO in C57BL/6 male mice. Additionally, TQ warned of methotrexate-related occurrences such as intestinal space enlargement, edema, disruption of the somniferous epithelium, and smaller seminiferous tubule diameter. Treatment of 34 infertile men for two months with 2.5 mL black seed oil enhanced their abnormal semen quality without having any negative effects [39]. Black seed oil is a promising therapy for treating male infertility, according to Mahdavi et al. [28] In Sprague-Dawley male and female rats, *N. sativa* extracts in hexane and methanol significantly reduced fertility. In contrast, *N. sativa* prevented

the contraction of uterine smooth muscle in rats and guinea pigs [1, 28]. TQ reduced the number of polycystic ovaries in rats by reducing their exposure to olive oil [40].

### **2.16 Effect on dyspepsia**

A substantial reduction in dyspepsia was seen in individuals (n = 70) with functional dyspepsia who received treatment with 5 mL of Nigella oil (p.o.) daily for 8 weeks [41]. In osmotic balance: Nigella It was determined that black seed oil (22.6 g/25 l) should be used as an alternate therapy to isotonic sodium chloride (0.9% NaCl) solution for the elderly patients (n = 42) after they received treatment for two weeks (**Table 1**) [43].


### **Table 1.** *Several new research findings on nigella recipes.*

*Antioxidant Activity of* Nigella sativa *Essential Oil DOI: http://dx.doi.org/10.5772/intechopen.109086*

### **3. Conclusion**

One of the potential sources of drugs comes from plants, specifically shrubs. It's interesting to note that people worldwide are paying a lot of attention to herbal medicines today. Otherwise, traditional medicines continue to rule a certain kingdom of remedies. The excitement for drug researchers comes from the possible and varied activities of a trustworthy source. According to earlier research, *N. sativa* generated notable pharmacological actions, mainly through the use of TQ and its derivatives, nigellone, −hederin, and linoleic acid. Additionally, a few human clinical applications imply that *N. sativa* and its genetic makeup have a safety record. *N. sativa* and its derivatives may be chemically modified to produce useful results for the drug library. It is been found to be safe and healthy in several clinical applications, particularly in anti-fertility studies. Fixed oil of black seed was found to have LD50 values of 26.2–31.6 mg/kg in mice when administered intraperitoneally (i.p.) and orally (p.o.). TQ was found to be more tolerable than the *N. sativa* extract. They may be effective sources of cytoprotective agents due to their substantial antioxidant activity through antiradical, including ROS, direct reduction of oxidizable substrates, and stimulation of cellular antioxidant molecules. Antibiotics or radiation therapy can be used in conjunction with *N. sativa* oil to counteract its cytotoxic, immunosuppressive, and carcinogenic effects. TQ fits within this category, while further research is needed to determine its genotoxic and mutagenic potential.

### **Author details**

Kehinde Sowunmi1 \* and Zeenat Kaka<sup>2</sup>

1 Department of Cell Biology and Genetics, University of Lagos, Akoka, Lagos, Nigeria

2 Department of General Education, Government Technical College, Ikorodu, Lagos, Nigeria

\*Address all correspondence to: sowunmikehinde111@gmail.com

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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*Antioxidant Activity of* Nigella sativa *Essential Oil DOI: http://dx.doi.org/10.5772/intechopen.109086*

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### **Chapter 9**

## Bioactive Compounds and Antioxidant Activity of Essential Oil of Species of the Genus Tagetes

*Rosa Huaraca Aparco, María del Carmen Delgado Laime, Fidelia Tapia Tadeo, Henrry Wilfredo Agreda Cerna, Edwin Mescco Cáceres, Juan Alarcón Camacho, Hans Yuri Godoy Medina, Calixto Cañari Otero, Martha Teresa Ecos Ramos, Victor Raul Ochoa Aquije, Rosa Nelida Ascue Ruiz, Grecia Valverde Mamani and Niki Franklin Flores Pacheco*

### **Abstract**

This study investigated the bioactive compounds and antioxidant activity of the essential oil of two species of the genus Tagetes (*Tagetes minuta L*. and *Tagetes elliptica Sm*). The essential oil was obtained by steam distillation, and its extraction performance, relative density, refractive index, and solubility in ethanol (70% v/v) were determined. The chemical components were evaluated by gas chromatography coupled to mass spectrometry (GC-MS). Antioxidant activity was determined by the free radical 2,2-diphenyl-1-picrylhydrocyl (DPPH) method and the trapping capacity of the ABTS\*+ radical cation. In the essential oils of the species Tagetes, it was possible to identify 26 chemical components for the species *Tagetes elliptica* Sm. and 16 for *Tagetes minuta* L., both species presented as main components monoterpenes (61%) and sesquiterpenes (44%). The compounds found were β-myrcene, trans-tagetone, β-trans-ocimene, and β-caryophyllene. Essential oils showed a variation in extraction yields and density. The refractive index was higher in the species *Tagetes elliptica* Sm., finding a high solubility in both species. A variation was found between 1.77 and 2.56 mg/mL of antioxidant activity by the DPPH method and 21.02–41.06 mg/mL for ABTS\*+. The essential oils of the species *Tagetes elliptica* Sm.y and *Tagetes minuta* L. have bioactive components with antimicrobial and antioxidant potentialities for use for food preservatives.

**Keywords:** chromatography, density, monoterpenes, sesquiterpenes, solubility

### **1. Introduction**

Peru is one of the 12 countries with the greatest biological diversity, with approximately 10% of the world's flora, estimated at 25,000 species, 30 of which are endemic [1]. There is a growing interest in bioactive compounds and the antioxidant properties of substances from natural sources that can potentially be used in food industries. Essential oils from aromatic and medicinal plants are known to possess biological activity [2, 3]. Essential oils are natural plant products that contain a complex mixture and therefore have multiple antimicrobial properties [4]. To be the constituents of the most important groups of raw materials for the food, pharmaceutical, perfumery, and related industries [5]. Most of these compounds are derived from oxygenated terpenoids, particularly phenolic terpenes, phenylpropanoids, and alcohols [6, 7]. Tagetes species were originally used as a source of essential oils that were extracted from leaves, stems, and flowers, being applied as flavorings in the food industry; in addition, their pigments have potential as a natural food colorant.

Tagetes is an important genus belonging to the family Asteraceae [8], aromatic, native to Central and South America with a cosmopolitan distribution due to anthropic activities [9]. *Tagetes minuta* L. is an aromatic plant with a broad spectrum of biological activity that has medicinal, antioxidant, and antimicrobial properties [10]. The great importance of Tagetes is due to the presence of essential oil in almost all parts of its plants, except in the stem [11]. It has biological activities such as antibacterial, antifungal, antiviral, antioxidant, anticancer, acaricide, nematicide, insecticidal, and allelopathic activities [12]. The growing interest in the food, flavor, and perfumery industries contributes to the investigation of environmental conditions affecting qualitative composition and yield [13].

*Tagetes minuta* L. is known by the common name of "huacatay" in Peru; in Mexico, it is known as "Mexican marigold" [14]. It is a species that accumulates a long world history of uses such as food, therapeutics, and aromatherapy that are inherent in the unique chemistry of the plant, its composition, and bioactivities. According to the research background review on bioactive metabolites and antioxidant activity of the aromatic species *Tagetes minuta* L. and *Tagetes elliptica* Sm., no publications are reported in our country; however, there are many reports on essential oils of these species in other countries [15].

Despite their importance as food species, research on the species *Tagetes minuta* L. and *Tagetes elliptica* Sm. in terms of chemical composition, genetic diversity, and biological properties is limited. Therefore, the objective was to determine the physical properties and identify the bioactive components and antioxidant activity of the essential oils of both species of the genus Tagetes that grow wild and are adapted to moderate-altitude ecosystems of the Andean region of Peru.

### **2. Materials and methods**

### **2.1 Plant matter and botanical identification**

The sheets of *Tagetes minuta* L. and *Tagetes elliptica* Sm were used. The samples were collected from the high Andean zone of the district of José María Arguedas (13°42 S.73°24 W at an altitude of 2935 m above sea level) belonging to the province of Andahuaylas, Apurimac region. With climate Cwd according to Koppens with average annual rainfall around 1000 mm/year, average relative humidity of 50% and temperature of −5 to 21°C, with moderate incidence of frost. The sample sheets were collected

*Bioactive Compounds and Antioxidant Activity of Essential Oil of Species of the Genus Tagetes DOI: http://dx.doi.org/10.5772/intechopen.109254*

during the months of February to March 2019. The plants were identified and authenticated by Dra. María del Carmen Delgado Laime and deposited in the botany laboratory of the Basic Sciences pavilion of the José María Arguedas National University.

### **2.2 Essential oil extraction**

For the extraction of essential oils, fresh leaves of *Tagetes minuta* L. were selected and *Tagetes elliptica Sm.*; 2.5 kg of fresh leaves of each species were used and subjected to extraction by distillation by dragging water vapor at a pressure of 10 psi. Once distilled, the essential oils were separated by difference in densities using a graduated Florentine decanter. Then dried in anhydrous sodium sulfate and stored at 4°C until the time of analysis, extraction yields were evaluated according to (Eq. 1).

$$9\% P = \frac{\text{Masafinaldeaccite esencial} \left(\text{g}\right)}{\text{Masaimicialdemustraofollaje} \left(\text{g}\right)} \* 100\tag{1}$$

### **2.3 Determination of the physical properties of the essential oil**

In the essential oils obtained from each species, the relative density at 20°C was determined according to the Peruvian technical standard: NTP 3129.081:1974; refractive index in the ABBE refractometer; optical rotation in polarimeter and solubility in ethanol. For the latter, a 70% solution was used taking 100 μL of essential oil.

### **2.4 Determination of chemical compounds by gas chromatography coupled to mass spectrometry (GC-MS)**

The analysis of the chemical composition of essential oils was identified by gas chromatography coupled to mass spectrometry (GC-MS) at the natural products research center of the Universidad Peruana Cayetano Heredia.

For the analysis of each sample, 20μL of essential oil in 980 μL of dichloromethane was used, which was injected into the gas chromatograph coupled to a selective mass detector. The compounds were separated in a mixture by an apolar capillary column DB-5MS (60 m × 250 μm × 0.25 μm) (J and W Scientific of 5% phenyl-polymethylsiloxane).

The temperature of the injector was maintained at 250°C with an injection in Split mode (50:1), the programming of the furnace temperature was: initial temperature 50°C, maintained for 5 mins; then increasing to 10°C/min to reach 100°C and finally to 10°C/min to 270°C, maintaining the final temperature for 1 min. The execution time was 77.8 mins, helium was used as a drag gas at a constant flow of 1 ml/min. The compounds of Tagetes oils *minute* L*.* and *Tagetes elliptica* Sm*.* were identified using software provided by Agilent; MSD chemstation (verse EO2.00.493), by comparing the mass spectra of each peak with those of the mass spectra library of the flavor databases and the National Institute of Standards and Technology (NIST, 08).

### **2.5 Evaluation of the antioxidant activity of essen0tial oils**

For the determination of the antioxidant activity of the essential oils of the species of the genus Tagetes, two methodologies were used:

### *2.5.1 DPPH radical method*

Aqueous ethanol dilutions of hydroalcoholic extracts were prepared to obtain concentrations of 0.0–150.0 μg/mL. About 1.0 mL of each dilution was combined with 0.5 mL of a 0.3 mM solution of DPPH in ethanol and allowed to react at room temperature for 30 mins, then the absorbance of the mixtures at 517 nm was measured in the spectrophotometry equipment. The percentage of antioxidant activity of each sample was calculated according to the following (Eq. 2):

$$Actividad\ A\ \text{ntio}\ \text{xidante}\ \left(\forall\ \mathsf{6}\right) = \frac{\text{MAC} - \text{AM} - \text{AB}\left(\text{g}\right)}{\text{AC}}\ \mathbf{X}\ \mathbf{100}\tag{2}$$

AM: is the absorbance of the sample + DPPH,

AB: is the absorbance of the target (sample + ethanol),

AC: is the absorbance of the reactant target (DPPH + ethanol).

The concentration of the hydroalcoholic extract was neutralized at 50% of the DPPH radicals (EC50, mean effective concentration) and was obtained directly by drawing the line between the percentage of antioxidant activity, compared with the concentration of the sample of essential oils mg/mL.

### *2.5.2 Radical method ABTS\*+*

The ABTS<sup>+</sup> free radical scavenging activity was determined by the method developed by Re et al. (1999), with some modifications.

About 3.5 mM of ABTS was reacted with 1.25 mM of potassium persulfate. The samples were incubated at temperatures of 2–8°C for 16–24 h in darkness. The formed ABTS\*+ radical is diluted with ethanol to an absorbance of 0.7+ minus 0.05 to 734 nm. At a volume of 190 μL dilution of the ABTS\*+ radical A, 10 μL of the AE sample was added and incubated at room temperature for 5 mins. After the time it took to determine by means of the spectrophotometer equipment at 734 nm in the Themoscientific microplate reader. For the positive control of the absorption of A radicals ABTS\*+, ascorbic acid (4 μg/mL) was used.

### **2.6 Statistical analysis**

The analyses were performed in triplicate, for the statistical evaluation, the completely randomized design (DCA) was used; The analysis of variance was worked with 0.05 significance; upon finding a significant difference, the Fisher's mean comparison test (LSD) was performed at a level of α = 0.05. The data were processed with the help of the statistical programs Centurion XVII and the Microsoft Excel 2016 spreadsheet.

### **3. Results**

### **3.1 Performance and physical properties of essential oils**

The determination of the physicochemical properties allows us to know the quality control and purity in essential oils.

*Bioactive Compounds and Antioxidant Activity of Essential Oil of Species of the Genus Tagetes DOI: http://dx.doi.org/10.5772/intechopen.109254*

**Table 1** shows the percentage of extraction yield and the physical properties of the essential oils of both species of the genus Tagetes. Where:, a is different from b.

### **3.2 Chemical composition of essential oils of two species of the genus Tagetes**

The main components of the essential oils of both species of the genus Tagetes are shown in **Table 2**.

Retention time (TR) and relative abundance (%) of essential oils, Not detected (ND).

In the analysis of the chemical composition, a total of 26 chemical compounds were detected and quantified in the essential oil of *Tagetes elliptica* Sm., with main fraction in monoterpenes in (61.00%) and 16 chemical compounds for the essential oil of *Tagetes minuta* L. being found as the main fraction to the monoterpenes (50.0%); between both species, a standard deviation below 5% was obtained between the percentages of each analyte in both columns used. They were identified as bioactive compounds in essential oils in species of the genus Tagetes to β-trans-ocimene, trans-tagelone, cis-tagelone, β-myrcene, and β-caryophyllene.


### **Table 1.**

*Performance and physical properties of the essential oils of* Tagetes minuta *L. and* Tagetes elliptica *Sm.*


### **Table 2.**

*Main components detected in the essential oils of* Tagetes minuta *L. and* Tagetes elliptica *Sm***.**


**Table 3.**

*Antioxidant activity by DPPH and ABTS methods.*

### **3.3. Antioxidant activity of AE of** *Tagetes minuta* **L. and** *Tagetes elliptica* **Sm**

The antioxidant activity of the essential oil, evaluated by the DPPH and ABTS methods, is shown in **Table 3**.

Significant differences were found in the antioxidant activity of both Tagetes samples as shown in **Table 3**. According to the DPPH methodology, CI50 varied from 1.77 to 2.56 mg/mL; however, the CI50 of ABTS\*+ varied from 21.02 to 41.06 mg/mL, finding a higher antioxidant activity the value of CI 50 41.06 mg/mL. *Tagetes* essential oil had a lower CI50 of 1.77 mg/mL, respectively, exhibited considerable DPPH radical scavenging activity compared with ABTS\*+ method A.

### **4. Discussion**

The essential oils of *Tagetes minuta* L*.* and T*agetes elliptica* Sm. did not show significant differences in the percentage of performance. The yield of the essential oil depends on the plant and the district where it is grown [16]. According to the results of the physical properties of the essential oil, the density showed a variation for both species of the genus Tagetes; however, the refractive index did not show a variation between both species. The presence of a lower refractive index and density value is related to an amount of phenols [17].

The refractive index of both species presented high values, which indicate the presence of high-molecular-weight compounds such as sesquiterpenes and diterpenes and eventually oleoresins in high concentrations [18], being also indicative of essential oils of higher quality and purity.

According to the results of specific gravity of the essential oils of both species, significant differences were found with a presence of higher quality (0.945 ± 0.034) in the essential oil of *Tagetes elliptica* Sm., finding similar values obtained according to previous studies [19].

The analysis of the chemical components in the essential oils of the species *Tagetes minuta* L. *and Tagetes elliptica* Sm*.* showed mainly the presence of the following compounds: Trans-Tagetone, β-trans-Ocimene, Cis-Tagetone, β-Caryophyllene, and Apiol.

The essential oils of the species *Tagetes spp*. are rich in monoterpene hydrates (Ocimenes, limonene, terpinene, myrcene, and acyclic monoterpene ketones (tagetone, dihydrotagetone, and tagetenone), which are the main odors in addition to smaller amounts of sesquiterpene hydrocarbons oxygenated compounds [20].

According to the results of the study in species *of Tagetes patula*, strong bioactivity was found in its essential oils against pathogenic test organisms, which is attributed to the presence of terpinolene, E-karyophene, Z-tagetone, E-tagetone, Caryophene oxide, and Germacrene D.

*Bioactive Compounds and Antioxidant Activity of Essential Oil of Species of the Genus Tagetes DOI: http://dx.doi.org/10.5772/intechopen.109254*

Regarding its bioactivities of the species family of the genus Tagetes, strongto-mild antibacterial activity was found against strains of large-positive and largenegative bacteria tested in the study [4].

Regarding its applications of the essential oil according to the presence of metabolites, it was found that the metabolites synthesized by plants of the genus Tagetes show significant effects as antioxidants, enzyme inhibitors, precursors of toxic substances, and pigments. The activity of secondary metabolites in species of the genus Tagetes is thought to be related to their composition, concentration, and environmental conditions affecting their content.

Essential oils obtained from different parts of the plant may show different biological capabilities and can therefore be used in a variety of industries, such as cosmetics, pharmaceuticals, or food production [21].

According to [22], I report the antimicrobial activity of the essential oils of *Tagetes minuta* L. against phytopathogenic bacteria, *Pseudomonas savastanoi* pv, and *Phaseoli axonopodis* pv, which are responsible for different plant diseases.

The results indicated that *Tagetes spp*. plays a role of great importance for the preparation and preservation of food, considered as an excellent source of food spice. Even from a traditional point of view, the nature of *Tagetes spp*. and its composition affect the quantity and quality of extracts [23]. Despite the promising results obtained in vitro, more detailed studies of the mechanisms of action of the extracts and essential oils of *Tagetes spp*. would be beneficial to reach its potential in biotechnology. It was documented that the components of essential oils, especially terpenoids such as dihydrotagetones, tagetones, and ocymenones, were sufficient to explain the observed antimicrobial activity [24].

The difference in antioxidant activity between the two samples could be attributed to the presence of monoterpenes in their polyphenolic compounds, and oxygenated monoterpenes lead to increased antioxidant, antibacterial, and antifungal activities [25–27].

### **5. Conclusions**

In this study, it was possible to determine the bioactive metabolites of the essential oils of the species of *Tagetes minuta* L. and *Tagetes elliptica* Sm., finding greater abundance of the bioactive metabolites: β-trans-ocimene, trans-tagelota, cis-tagelone, β-myrcene, and β-caryophyllene being the monoterpenic acyclicos, with significant effects as antioxidants, enzyme inhibitors, precursors of toxic substances, and pigments beneficial to reach their potential in biotechnology. The abundance in monoterpenes leads to antioxidant activities, being in the study greater presence of antioxidants in the species of *Tagetes elliptica* L. The physical properties of both species of the genus Tagetes were found in the quality ranges of essential oils.

### **Acknowledgements**

The authors thank the Natural Products Research Laboratory of the Universidad Peruana Cayetano Heredia and the Universidad Nacional José María Arguedas.

### **Author details**

Rosa Huaraca Aparco1 \*, María del Carmen Delgado Laime1 , Fidelia Tapia Tadeo1 , Henrry Wilfredo Agreda Cerna1 , Edwin Mescco Cáceres1 , Juan Alarcón Camacho2 , Hans Yuri Godoy Medina2 , Calixto Cañari Otero2 , Martha Teresa Ecos Ramos1 , Victor Raul Ochoa Aquije3 , Rosa Nelida Ascue Ruiz4 , Grecia Valverde Mamani1 and Niki Franklin Flores Pacheco5

1 José María Arguedas National University, Andahuaylas, Apurimac, Perú


\*Address all correspondence to: rhuaraca@unajma.edu.pe

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*Bioactive Compounds and Antioxidant Activity of Essential Oil of Species of the Genus Tagetes DOI: http://dx.doi.org/10.5772/intechopen.109254*

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## Organic Culture Media for Sustainable Carotenoid Production from Microalgae

*Wa Iba, Nur Illyin Akib, Ilham, La Ode Muhammad Jumardin, Bolo Arif, Nursainuddin, Sendry Yosalina and Jumtrisnanda Asmin Andas*

### **Abstract**

Antioxidants, particularly those carotenoid produced in microalgae, can be increased by induced stress, including light, nutrients, and salinity. Nutrient stress can be achieved by using imbalanced nutrients to boost antioxidant production without compromising the growth, that is, biomass. Culture media is an important factor in microalgae production because it is affecting growth and biomass production, as well as the biochemical content of microalgae. Synthetic or conventional culture media is considerably expensive for mass culture and the supply is limited, especially for developing countries. Therefore, there is a need for cheap and easily available culture media. This chapter discusses the use of organic media to culture several species of microalgae and cyanobacteria (*Arthrospira platensis*) for antioxidant production, particularly of those total carotenoids and beta carotene. The antioxidant content data mainly comes from our research with several organic culture media, such as fermented water hyacinth biomass, soybean processing waste, and Acadian Marine Plant Extract Powder (AMPEP). Carotenoid can be used for pharmaceuticals, including for anticancer, anti-inflammatory, and anti-obesity. Also, they can be used in aquaculture to increase cultured animals' health and immunity. Using organic media that may also serve as waste stream microalgae, which is aiding in a sustainable microalgae culture. Additional data presented in this chapter come from literature reviews of similar research topics.

**Keywords:** carotenoid, microalgae, organic, culture media

### **1. Introduction**

Microalgae are microscopic organisms that are known to have very efficient photosynthesis capabilities. These organisms in nature are generally phytoplankton that acts as constituents of secondary metabolites in the form of natural pigments [1]. These natural pigments play an important role in microalgae photosynthesis and growth both for light harvesting and cell protection from stress, thus as an

antioxidant. Antioxidant compounds contained in microalgae can be pigments, such as chlorophyll, phycobilin protein, and carotenoids [2]. Microalgae produce different types of carotenoids, more than 40 carotene and xanthophylls have been isolated and characterized. Carotenoid compounds are natural pigments found in bacteria, algae, fungi, and plants but are not produced by animals.

Carotenoids are formed from eight isoprene molecules, so that they have 40 carbon atoms. In general, carotenoids are grouped into carotene (pure hydrocarbon carotenoids, having no oxygen atoms) and xanthophyll (oxygen atom-carrying carotenoids) [3]. Carotenoids have several types, including α-carotene, β-carotene, astaxanthin, lycopene, lutein, zeaxanthin, β-cryptoxanthin, and fucoxanthin [4–6]. Carotenoids also have perishable or degradable properties caused by light, heat, and oxygen, and prolonged exposure to those factors decreases the content of carotenoids in the biomaterial [7]. Carotenoids are organic pigments found in chloroplasts and chromoplasts of plants and other groups of organisms. Carotenoid compounds provide several health functions for the body, especially as antioxidants, that may protect the body from free radicals. Because of these functions, carotenoids are also applied to nutraceutical products [8]. These pigments are found in almost all classes of microalgae and can be used as pharmaceutical or health products because they can reduce the risk of developing cancer, vitamin A precursor for good vision and eye health, a strong immune system, and the health of the skin and mucus membranes. In the food industry, β-carotene is used as a pigment in food, in the pharmaceutical industry, β-carotene acts as a tablet coloring agent, and in the cosmetic industry, it is used as a bioactive ingredient in creams, which protects the skin from exposure to UV radiation [2–4].

Microalgae can be propagated by culture or cultivation in controlled closed photobioreactors or open ponds and raceways. Algae culture activities are one of the efforts to develop and meet the needs of carotenoid-producing microalgae. Microalgae in the process of their growth require macroelements of N and P and various other microelements to increase the growth rate and produce maximal nutrient content. The complete nutrient composition and proper concentration of nutrients determine biomass production and nutritional content of microalgae [9, 10]. Synthetic culture media commonly used for microalgae culture include Walne, Bold Basalt Medium (BBM), Conway, and F/2 media [9]. Meanwhile, organic media that have been used as microalgae culture media include seaweed waste [11], fermented water hyacinth [12], chicken manure [13], and brown seaweed extract [14]. Conventional culture media tend to be expensive and limited in availability for mass culture of microalgae, especially in developing countries. Using organic media is considered more sustainable and cheaper, particularly for the mass culture of microalgae. Also, culturing microalgae in organic media can be used as a bioremediation strategy and waste stream microalgae. Therefore, alternative culture media continues to be researched and developed. More importantly, organic media is considered as nutrient imbalances media, particularly of those N and P, and therefore may induce nutrient stress in microalgae that may lead to high production of carotenoid. This chapter discussed the use of several organic culture media, such as Acadian Marine Plant Extract Powder (AMPEP), fermented water hyacinth biomass, and soybean processing waste from tempeh production. These media were used to culture several species of microalgae in our lab, such as *Chlorella vulgaris, Dunaliella salina, Nannochloropsis* sp., *Tetraselmis* sp., and *Arthrospira (Spirulina) platensis,* that has been experimented in our lab for carotenoids, including β-carotene production.

### **2. Carotenoid biosynthesis in microalgae**

Microalgae produce a variety of beneficial compounds, such as anticancer, antiinflammatory compounds, antioxidants, vitamins, minerals, omega-3 fatty acids, and pigments [15]. One of the antioxidant compounds in microalgae is carotenoids, including β-carotene. Carotenoids exhibit biological activity as antioxidants, influencing cell growth regulation and modulating gene expression and immune responses. Carotenoids are natural pigments found in plant chloroplasts together with chlorophyll. Carotenoids act as additional pigments that help chlorophyll in absorbing light energy. The formation of carotenoids in microalgae increases in physiological conditions that are not balanced in cells caused by various environmental pressures, including nutrient content in nonoptimal media. This response is modulated by the phytoene synthase (PSY), an enzyme responsible for carotenoid biosynthesis in the photosynthetic organism. It is suggested that different PSY genes family is responsible for microalgae development and cell defense under environmental stress [3, 16]. Also, the composition and combination of nutrient content in the medium (C:N:P ratio) can affect the content of carotenoids in microalgae [17].

Carotenoids are synthesized in plastids through phytoene to lycopene synthesis and resulting in α- and β-carotene. The most common carotenoid used in several industries is β-carotene, which is a yellow, orange, or red organic pigment that occurs naturally in photosynthetic plants. β-Carotene can be fat-soluble, insoluble in water, and easily damaged by oxidizing at high temperatures. β-Carotene can be useful as a natural food coloring, antioxidant, and pro-vitamin A source for humans and can be beneficial in treating and preventing tumors and cancer [2–4]. β-Carotene can be commercially synthesized from natural source extraction. β-Carotene was found to accumulate in oil globules in thylakoids present in chloroplasts and consisted of two isomers, all-trans, and 9-cis β-carotene [18] (**Figure 1**).

β-Carotene biosynthesis begins with head-tail condensation on two molecules of C20 geranylgeranyl pyrophosphate (GGPP), resulting in C40 phytoene catalyzed by phytoene synthase (PSY). Phytoene is further modified gradually into β-carotene, neurosporent, lycopene by phytoene desaturase (PDS), β-carotene desaturase (ZDS), and carotenoid isomerase (CRTISO). There is an increase in the number of conjugated double bonds at each stage. The terminal structure of isoprene on lycopene molecules is further cyclized by lycopene β-cyclase (LCYB) and forms β-carotene (**Figure 2**). GGPP, PDS, ZDS, CRTISO, and LCYB coding genes are found in all terrestrial plants and algae. The path of carotenoid biosynthesis to the β-carotene stage has been conserved in these organisms [4, 19, 20]. Many other important carotenoid types are β-carotene derivatives, such as astaxanthin, zeaxanthin, and dinoxanthin (**Figure 2**).

Almost all types of carotenoids (**Figure 3**) are found in microalgae, but distribution is varied among classes and species. Carotenoids in algae contain allene

**Figure 1.** *Chemical structure of β-carotene [19].*

**Figure 2.** *Carotenoid biosynthesis in microalgae [4].*

**Figure 3.** *Carotenoid structure found in microalgae [4].*

### *Organic Culture Media for Sustainable Carotenoid Production from Microalgae DOI: http://dx.doi.org/10.5772/intechopen.109789*

(C〓C〓C) and acetylene (C≡C) bounds. Allenic carotenoids found in algae include fucoxanthin in brown algae and diatoms, 19′-acyloxyfucoxanthin in Haptophyta and Dinophyta, peridinin only in dinoflagellates, and 9′-cis neoxanthin in green algae. Whereas acetylenic carotenoids, such as alloxanthin, crocoxanthin, and monadoxanthin, are found in Cryptophyta, and diadinoxanthin and diatoxanthin in Heterokontophyta, Haptophyta, Dinophyta, and Euglenophyta. Acetylated carotenoids (-O-CO-CH3), such as fucoxanthin, peridinin, and dinoxanthin, are also mainly found in algae, such as Heterokontophyta, Haptophyta, and Dinophyta. Many cyanobacteria contain β-carotene, zeaxanthin, echinenone, and myxol pentosides (myxoxanthophyll), while some species lack part of these and some contain additional carotenoids, such as nostoxanthin, canthaxanthin, and oscillol dipentoside [4]. Several microalgae species are known to produce abundant carotenoid, and therefore commercially cultured include *Haematococcus pluvialis*, *Dunaliella salina*, *Chlorella vulgaris, Nannochloropsis* sp., and *Arthrospira (Spirulina)* sp.

### **3. Effect of organic culture media on carotenoid production in microalgae**

The growth and carotenoid production in microalgae are affected by culture media through the availability of nutrients. The nutrient ratio of C/N/P is an important regulator in carotenoid production. Different concentrations of N and P are found in organic media as shown in our studies. This concentration was higher compared to Walne, a commercially available culture media commonly used for culturing microalgae and cyanobacteria (**Table 1**).

Optimal utilization of nutrients produces maximum growth indicated by high cell number and biomass one culture cycle, thus may affect carotenoid content. Media composition plays a role in nutrient utilization and pigment production of microalgae [25], including carotenoids [26]. A growth medium depleted in phosphorus content has a positive effect on the synthesis of β-carotene. The P element has a role in the process of energy metabolism, but the response to P stress in culture media is different for each microalgae species. Depleted P content in the microalgae growth medium of *Tetraselmis marina* increases its carotenoid content [27]. Conversely, the β-carotene content in *Oocystis* sp. can be improved by giving excess P nutrients. The highest β-carotene content in the microalgae *Oocystis* sp. was detected in induction treatment with a fivefold addition of KH2PO4 [28].

Some organic media that have been successfully used as microalgae culture media for carotenoid production are green bean sprouts extract for growth and carotenoid content of *D. salina* [29], lamtoro leaf extract medium for growth and contains carotenoids *Dunaliella* sp. [30] and fermented water hyacinth for the growth and carotenoids of *C. vulgaris*. We found that organic media from fermented hyacinths with a concentration of 0.1% was able to produce maximum *C. vulgaris* growth on the sixth day with a culture volume of 150 mL with a density value of 66.7 × 104 sel mL−1 with the highest carotenoid content of *C. vulgaris* obtained at a 1% organic media concentration of 0.545 μg mL−1 [31].

Other organic culture media that was experimented in our lab is brown seaweed extract or commercially sold as AMPEP. This is derived from extracts of brown algae (*Ascophyllum nodosum*), which have been used to increase the productivity of agricultural crops and have the potential to be used as a microalgae culture medium for the production of carotenoids. The experiment of microalgae grown for 7 days without the addition of *A. nodosum* extract was able to increase the cell density of *C. vulgaris*


### **Table 1.**

*N and P concentration in organic and synthetic culture media.*

and *Scenedesmus* sp., whereas the addition of *A. nodosum* extract at concentrations of 3 and 4% inhibited the growth and antioxidant activity of *C. vulgaris* and *Scenedesmus sp*., although it was able to improve protein synthesis. Conversely, the addition of *A. nodosum* extract at low concentrations (1 and 2%) was able to increase the growth and antioxidant activity of *C. vulgaris* and *Scenedesmus* sp. [14]. Therefore, low doses of *A. nodosum* extract can be applied for the acceleration of microalgae cultivation and the production of antioxidants, particularly of those carotenoids. The use of AMPEP in low concentrations will be very profitable in terms of the cost and productivity of microalgae cultures for carotenoid production.

Our studies with 10 ppm AMPEP concentration for culturing *D. salina,* resulting in high biomass and *β-carotene* production at 418.1 × 104 cells mL−1 and 0.3545 μg mL−1, respectively. Similar trends were found in our experiment when *Spirulina* sp. was cultured in the same AMPEP concentration, although the growth and carotenoid content were lower compared to *D. salina*. The growth and carotenoid content of *Arthrospira* (*Spirulina*) was also the highest in 0.1% of tempeh processing waste and 25% of moringa leaf extract [32]. Conversely, the lowest growth of *C. vulgaris* was found at 10 ppm AMPEP culture media but with the highest carotenoid content at 0.267 μg mL−1. Our study indicated that different species responded differently in terms of growth and carotenoid content when using the same concentration of AMPEP (**Tables 2** and **3**). It seems that cyanobacteria *Arthrospira* sp. adapted well in different organic culture media except for AMPEP with good growth and considerably high carotenoid content (**Table 4**).


*Notes: S = salinity (ppt), L = light intensity (μmoles m−2 s−1), T = temperature (°C), D = cells density (cells mL−1), and C = β-carotene (carotenoid) = μg mL−1.*

### **Table 2.**

*β-Carotene and carotenoid content of D. salina cultured in various organic culture media.*

*Organic Culture Media for Sustainable Carotenoid Production from Microalgae DOI: http://dx.doi.org/10.5772/intechopen.109789*


*Notes: V = culture volume (mL), P = photoperiod (dark: light), S = salinity (psu), and I = light intensity (μmol photon m−1 s−2).*

### **Table 3.**

*Carotenoid content of C. vulgaris cultured in various organic media.*


*S = salinitas (psu/ppt), Sh = Suhu (°C), C = karotenoid (μg mL−1).*

### **Table 4.**

*Carotenoid content of* A. platensis *cultured in various media.*

The content of carotenoids in microalgae is highly dependent on the species cultured and the media used. In addition, cell density, culture volume, bioreactor, light intensity, salinity, and temperature also affect the carotenoid content (**Tables 3** and **4**). The difference in carotenoid content from each study is thought to be due to differences in nutrient content in each medium used as well as supporting factors that affect such as light, salinity, pH, and temperature. All such factors must be in optimum conditions for maximum microalgae cell growth and carotenoid content.

In our lab, the standard culture condition for carotenoid production in microalgae is 28–30°C, salinity of 29–30 psu, pH 7–8, and light intensity of 16.2 μmoles m−2 s−1 [31]. Besides organic culture media, these conditions have been proven to induce stress during microalgae culture, thus the carotenoid content in cultured species.

### **4. Conclusion**

Organic culture media, such as fermented water hyacinth, tempeh processing waste, and AMPEP, can be used to culture several microalgae species, including D. salina and C. vulgaris, and cyanobacteria *A. platensis*. However, AMPEP is not ideal for culture *A. platensis* for carotenoid production and may need some adjustment to its N and P content.

### **Author details**

Wa Iba1 \*, Nur Illyin Akib2 , Ilham3 , La Ode Muhammad Jumardin4 , Bolo Arif4 , Nursainuddin4 , Sendry Yosalina4 and Jumtrisnanda Asmin Andas4

1 Faculty of Fisheries and Marine Sciences, Aquaculture Department, University of Halu Oleo, Kendari, South East Sulawesi, Indonesia

2 Faculty of Pharmacy, Pharmacy Department, University of Halu Oleo, Kendari, South East Sulawesi, Indonesia

3 Fisheries Resources Section, Directorate General of Capture Fisheries, Ministry of Marine Affairs and Fisheries, Jakarta, Indonesia

4 Faculty of Mathematics and Life Sciences, Biotechnology Department, University of Halu Oleo, Kendari, South East Sulawesi, Indonesia

\*Address all correspondence to: wa.iba@uho.ac.id

© 2023 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*Organic Culture Media for Sustainable Carotenoid Production from Microalgae DOI: http://dx.doi.org/10.5772/intechopen.109789*

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Section 3
