Evaluation of phytonutrients composition and nutraceutical potential of tomato by-products

ABSTRACT

This study aims to evaluate the phytonutrient composition, antioxidant activity and nutraceutical potential of peels and seeds of two tomato cultivars. Levels of phytonutrients such as phenolic compounds, carotenoids, chlorophyll, salicylic acid and vitamin C were assessed. Potential in vitro antioxidant activities were evaluated. Tomato has quite interesting levels of phenolic compounds such as total phenols and flavonoids, whose contents varied from 78.41 ± 1.52 to 272.17 ± 53 mg GAE/100 g DM and 13.35 to 139.89 mg QE/100 g DM, respectively. They also contained chlorophyll, which was concentrated in the peels (39 to 78 mg/100 g DM). β-carotene and lycopene contents ranged from 4.63 to 105 mg/100 g DM and 7.51 to 32.45 mg/100 g DM, respectively. Vitamin C level was high in peels with an average content of 27.82 mg/100 g DM. Tomato by-products showed high antioxidant activity with 61% DPPH inhibition and 108.55 to 120.86 µg EAA/g with FRAP method. With this richness in phytonutrients and their strong antioxidant power, tomato by-products have important nutraceutical potentials to be valorized with in vivo experiments.

Resumen

Este estudio tuvo como objetivo evaluar la composición de fitonutrientes, la actividad antioxidante y el potencial nutracéutico de cáscaras y semillas de dos cultivares de tomate. Para este cometido se evaluaron los niveles de fitonutrientes, entre ellos, de compuestos fenólicos, carotenoides, clorofila, ácido salicílico y vitamina C. Asimismo, se valoraron las posibles actividades antioxidantes in vitro. Los tomates presentaron niveles bastante interesantes de compuestos fenólicos, como fenoles totales y flavonoides, cuyos contenidos variaron de 78.41 ± 1.52 a 272.17±53 mg GAE/100 g MS; 13.35 a 139.89 mg QE/100 g MS, respectivamente. Además, contenían clorofila concentrada en las cáscaras (de 39 a 78 mg/100 g MS). Los contenidos de β-caroteno y licopeno oscilaron de 4.63 a 105 mg/100 g MS y de 7.51 a 32.45 mg/100 g MS, respectivamente. El nivel de vitamina C en las cáscaras fue elevado, registrándose un contenido medio de 27.82 mg/100 g MS. Los subproductos del tomate mostraron elevada actividad antioxidante, con 61% de inhibición del DPPH y de 108.55 a 120.86 µg de EAA/g empleando el método FRAP. Esta riqueza en fitonutrientes y su fuerte poder antioxidante hace que los subproductos del tomate posean importantes potenciales nutracéuticos que deben ser valorados mediante experimentos in vivo.

KEYWORDS:

• Tomato
• by-products
• nutraceutical nutraceutical
• phytonutrients
• antioxidant

PALABRAS CLAVE:

• Tomate
• subproductos
• nutracéutico
• fitonutrientes
• antioxidante

1. Introduction

Cultivated tomato (Solanum lycopersicum L.) is among the most consumed fruits in the world certainly as common food ingredient, source of energy, food colorant or its beneficial effects on health (Ali et al., 2021). Being a highly perishable climacteric fruit, the best way to preserve it is its processing. This later is at the origin of appearance of by-products constituted essentially by peels and seeds. Interestingly, studies have shown that these by-products are potential nutritional sources. Indeed, they are rich in lipids, proteins, dietary fibers and minerals (Kaboré et al., 2022). In addition to their richness in macronutrients, they are known to contain phytonutrients such as phenolics (flavonoids), carotenoids, chlorophyll compounds and vitamins (Wu et al., 2022). The existence of a correlation between the consumption of plant foods and the incidence of cancers and chronic pathologies is established in part thanks to phytonutrients. Polyphenols are known as powerful antioxidants, which prevent cell oxidation and fight against premature cell aging. Therefore, they have preventive effects on several diseases that involve a deterioration of cells, whether metabolic, inflammatory or neurodegenerative (Sarkar et al., 2022). Polyphenols may promote good glycemic balance, fight against the oxidation of cholesterol, reduce the obstruction of the arteries, intervene on insulin resistance and on arterial hypertension (Fernandes et al., 2022). Among phenolics, flavonoids as effective antioxidants reduce inflammation and help to prevent chronic diseases (Savych & Milian, 2021). They reduce the risk of asthma and protect the body from certain types of cancer and coronary heart disease (Alzamel, 2022). Tomato contains carotenoids such as lycopene (which gives the fruit its predominantly red colour) and β-Carotene (responsible for orange colour). Carotenoids help to scavenge free radicals that cause oxidative stress, which can damage tissue and accelerate premature aging (Lappi et al., 2021). These carotenoids contribute to smooth communication between cells. β-Carotene is a pro-vitamin A and participates in the maintenance of a healthy immune system and eye health (Anand et al., 2022). Lycopene is a powerful antioxidant, anti-inflammatory and anticancer agent (Madia et al., 2021). Chlorophyll regulates the intestinal transit by restoring the probiotic digestive flora which can be disturbed by candidiasis and mycosis. It contributes to boosting the immune system and helps lower blood pressure (Vaňková et al., 2018). Vitamin C is involved in collagen synthesis, and it is also an antioxidant that helps fight against oxidative stress, in synergy with vitamin E, β-carotene, selenium and zinc that potentiates the effects on free radicals (Milani et al., 2021). Vitamin C is essential to strengthening the immune system. It also increases the assimilation of iron, thus protecting against anemia. Vitamin E as an antioxidant plays an essential role in the protection of the membrane of all the cells of the body. In addition, it reduces the oxidation of low-density lipoproteins (LDL) and protects against cardiovascular diseases (Garg & Lee, 2022).

The nutraceutical potential of tomato by-products depends on the cultivar, the soil and climatic conditions. Thus, it is very difficult to predict the level of secondary metabolites in tomato by-products because the quality and contents of bioactive compounds also vary depending on the type of cultivation (organic, conventional), in soil, etc. (Braglia et al., 2021). Several studies have shown that tomatoes increase the synthesis of phenolic compounds, vitamin C and therefore a higher antioxidant activity, when they are produced in organic culture (Borguini et al., 2013). Also, the type of fertilizer influences the levels of bioactive compounds. Thus, it has been reported that high inputs of phosphorus and nitrogen may increase the levels of carotenoids, notably lycopene (Suhl et al., 2016). The findings above reveal that soil and climatic conditions affect the cultivar metabolism and therefore their nutraceutical quality. The valorization of the by-products of the cultivars used therefore requires prior analysis of their nutritional and nutraceutical potential.

The aim of this study is to evaluate the nutraceutical potential of by-products from two tomato cultivars.

2. Material and methods

2.1. Biological material

The biological material consisted of peels and seeds of tomato (Lycopersicum esculentum) of F1 Mongal and Petomech cultivar collected in the North of Burkina Faso, the most tomato producing region. It is located between 11°35“ and 13°19” North latitude and between 1°30“ and 2°45” West longitude. At least 5 kg of fruits was collected in each of the four collection areas from conventional agriculture. Collection is random in 2019, 2020 and 2021.

2.2. Methods

2.2.1. Quantitative analysis of phytomicronutrients

The analysis of polyphenols was performed with the Folin-Ciocalteu reagent with slight modification nutraceutical (Doka et al., 2004). This method is based on the reduction of the Folin-Ciocalteu reagent, consisting of phosphotungstic and phosphomolybdic acids, by phenolate ions whose absorbance is monitored at 760 nm. Contents are expressed as gallic acid equivalent per 100 g dry matter (mg GAE/100 g DM).

Total flavonoid contents were determined by the colorimetric method of Dowd (Arvouet-Grand et al., 1994). The optical densities were read at 415 nm using quercetin as standard.

Anthocyanins were quantified as described by Silva et al. (2017). The assay is based on the measure of the absorbances of the extracted sample diluted with buffer solutions of pH = 1 and pH = 4.5 and spectrophotometry reading at two wavelengths (510 nm and at 700 nm).

Extraction of salicylic acid was done according to the method described by Yang et al. (2018). Absorbances were measured at 540 nm against a blank and contents were expressed in mg/100 g dry matter (mg/100 g DM)

Lycopene, β-carotene and chlorophyll contents were evaluated by methods adapted according to Nagata and Yamashita (1992). The dry sample (100 mg) is vigorously shaken in 10 mL of acetone-hexane (4:6) solvent mixture for 1 min and filtered through Whatman No. 4 paper. The absorbance of the filtrate was measured at 453, 505, 645 and 663 nm.

The vitamin C content is obtained using the official AOAC titrimetric method using 2,6-dichlorophenol-indophenol (DCPIP) (Cunha-Santos et al., 2018). This method is based on the discoloration of 2,6-dichlorophenolindophenol (DCPIP) by ascorbic acid. This discoloration representing inversely the amount of ascorbic acid is read at 515 nm against a blank and extrapolated to a calibration curve. Equivalent ascorbic acid contents were expressed in mg per 100 mg dry matter (mg EAA/100 g DM)

2.3. Evaluation of the antioxidant activity

Anti-radical activity is evaluated using DPPH method (Brand-Williams et al., 1995). DPPH is reduced, turning the picryl group pale yellow and the intensity of the colour is inversely proportional to the capacity of the antioxidants present in the medium to donate protons. The evaluation of the delocalization was carried out by spectrophotometry at 517 nm.

The determination of antioxidant activity by the iron reduction method was carried out according to Hinneburg et al. (2006). The ferric-reducing antioxidant power (FRAP) method is based on the reduction of ferric ion (Fe³⁺) to ferrous one (Fe²⁺) which is accompanied by the appearance of an intense blue coloration read at 700 nm.

2.4. Statistical analysis

All the measurements were performed in triplicate. The calculations of the means, the analysis of variances ANOVA and plots were performed using the following softwares: Excel, GraphPad Prism 5, XLstat version 2016 and R_studio version 2022.02.01.

3. Result and discussion

Total phenolic compounds (TPC) content varied from 78.41 ± 1.52 to 122.19 ± 2.89 mg GAE/100 g DM for Petomech and F1 Mongal seeds, respectively (Figure 1). For peels levels were 256.74 ± 43.71 mg GAE/100 g DM to 272.17 ± 53.47 mg GAE/100 g DM for F1 Mongal and Petomech, respectively (Figure 2). The TPC varied significantly (p ≤ 0.0001) in seeds. The content of TPC in peels is higher than that obtained by Navarro-González et al. (2011). This difference could be explained by the cultivars studied and the agro-climatic conditions. The TPC of seeds and peels are higher than the values obtained by Fernández et al. (2021). In general, peels have a higher TPC than seeds (Friedman et al., 2021). Tomato by-products are low in energy but rich in bioactive compounds and may be an alternative to fight obesity, hypertension and to treat complications (Kosmalski et al., 2022). Polyphenols are known to be excellent in the prevention of chronic diseases. They regulate metabolism, control the glycemic index and protect against inflammation (Sarkar et al., 2022). They have enormous properties including anti-diabetic, anti-hypertensive and antioxidant properties. These phenolic compounds protect the arteries and prevent coronary diseases (Fernandes et al., 2022).

Figure 1. Proximal phytonutrient composition of tomato seeds. TP: Total polyphenol; T F: Total flavonoid; Antho: anthocyanin; S acid: Salicylic acid; Chl: chlorophyl.

Figura 1. Composición proximal de fitonutrientes encontrados en semillas de tomate. TP: Total polyphenol; TF: Total flavonoid; Antho: anthocyanin; S acid: Salicylic acid; Chl: chlorophyll.

Figure 2. Proximal phytonutrient composition of tomato peels. TP: Total polyphenol; T F: Total flavonoid; Antho: anthocyanin; S acid: Salicylic acid; Chl: chlorophyll.

Figura 2. Composición proximal de fitonutrientes encontrados en cáscaras de tomate. TP: Total polyphenol; TF: Total flavonoid; Antho: anthocyanin; S acid: Salicylic acid; Chl: chlorophyll TP: Polifenol total; TF: Flavonoide total; Antho: antocianina; Ácido S: Ácido salicílico; Chl: clorofila.

The total flavonoid contents varied from 13.35 to 139.89 mg EQ/100 g DM. The lowest contents were found in the seeds of F1 Mongal and the highest in the peels of Petomech. Contents varied significantly in seeds (P ≤ 0.0001) but not in peels (P = 0.2033). These values are lower than those obtained by other authors (Dabiré et al., 2021). This difference is due to the genotype of the cultivar, the type of culture and the part of the fruit used. Flavonoids allow the leaves to protect themselves against senescence. They are responsible for the colouring of leaves and fruits, and protect the plant against stress (Dias et al., 2021). In humans, flavonoids prevent weight increase and are stimulating agents of insulin receptors and reduce insulin resistance. By controlling glucose tolerance, flavonoids reduce the glycemic index and thus prevent diabetes (Savych & Milian, 2021). The lipid levels in the blood are regulated by flavonoids, which gives them the anti-obesity role (Rufino et al., 2021). Thanks to their antioxidant activity, flavonoids manage to scavenge free radicals, and prevent several chronic diseases such as hypertensive diseases and cancers (Maneesai et al., 2021).

Anthocyanins contents ranged from 4.33 ± 0.13 to 7.83 mg/g, with the lowest and highest contents found in Petomech seeds and Petomech peels. The anthocyanins contents did not significantly vary (P = 0.1131) from one variety to another for peels, but significant difference was found in seeds (P ≤ 0.0001). Anthocyanins have a protective role against biotic and abiotic stress in plants (Qiu et al., 2019). The tomato peels have higher anthocyanins content than other parts of the fruit and their levels vary according to the stage of maturity of the fruit (Lim & Li, 2017). In addition to their protective role that contributes greatly to fruit quality, food anthocyanins are important antioxidants that are beneficial to health. Anthocyanins contribute to the regulation of glycemia and may reduce the insulin resistance. They therefore prevent diabetes and protect against chronic inflammation (Khan et al., 2021). They are also known to have antioxidant properties that allow them to scavenge free radicals, precursors of chronic diseases (Bucciantini et al., 2021). Consuming foods rich in anthocyanins such as tomato by-products can reduce the risk of developing type 2 diabetes and hypertensive diseases (Lappi et al., 2021).

Salicylic acid contents ranged from 3.56 ± 0.25 to 5.52 ± 0.23 mg/100 g DM. Petomech peels showed the lowest content and F1 Mongal seeds showed the highest one. The difference in levels was significant in both by-products (P ≤ 0.0166). In general, salicylic acid is more concentrated in seeds than in peels. This could be due in part to its activity as a phytohormone that participates in the regulation. Salicylic acid may be a resistance factor against UV radiation and water stress (Torun et al., 2022). In addition to its protective role in plant physiology, salicylic acid has beneficial effects on human health. It has economic and pharmaceutical importance for humans because of its use in the synthesis of acetylsalicylic acid (aspirin). Foods containing salicylic acid are of nutraceutical potential because it plays an anti-inflammatory role, and prevents and treats obesity (Bucciantini et al., 2021). It also decreases plasma renin activity and induces excretion of catecholamines and cortisol in the urine which prevents hypertension.

Chlorophylls a and b level ranged from 25 to 50.64 mg/100 g DM where the low contents are encountered in seeds and the lowest with peels. For chlorophyll b, the contents ranged from 39 mg/100 g DM to 78 mg/100 g DM. The peels also had the lowest contents and the seeds the highest. The differences were statistically significant (P ≤ 0.0115). These results are different from those obtained with tomato variety “Regosol” from Indonesia (Sakya & Sulandjari, 2019). Bednarczyk et al. (2020) demonstrated that chlorophyll synthesis is photoperiod sensitive (Bednarczyk et al., 2020). Thus, shade would increase chlorophyll content depending on the cultivar. Chlorophyll is responsible for the photosynthesis of the green parts of tomatoes. In addition, it contributes to the development of the fruit and to the reduction of carbon emissions (Yuan et al., 2018). Despite its known role in green plants, dietary chlorophyll could treat obesity by improving intestinal flora (Li et al., 2019). In the same idea, other studies have highlighted the systemic activities of chlorophyll derivatives in the modulation of oxidative stress and regulation of xenobiotic metabolism systems, gene expression for diabetes and cancer prevention (Madia et al., 2021). Chlorophyll also has an antioxidant role coupled to anti-proliferative role that confers its anticancer property (Vaňková et al., 2018).

Lycopene content ranged from 4.63 to 105 mg/100 g DM in seeds and peels. For β-carotene, contents ranged from 7.51 to 32.45 mg/100 g DM for seeds and peels. There was no significant difference in lycopene or β-carotene levels in peels. However, in seeds, these differences were significant. Carotenoids are a large family of fat-soluble substances precursor of vitamin A (retinol), displaying antioxidant activities and preventive properties against chronic diseases (Lappi et al., 2021). β-Carotene is known to be an immune system booster. Other authors have reported that β-carotene is involved in the reproductive function by improving spermatogenesis and in ovarian function (Sabry et al., 2021). The consumption of fruits and vegetables rich in β-carotene would reduce the risk of complications of obesity (Yamada et al., 2020). In-vivo studies have shown that β-carotene protects against toxicity caused by some substances. Interestingly, present data show that these tomato by-products can be used as sources of β-carotene to reduce vitamin A deficiency.

Lycopene levels in peels are higher than previously reported in organic and conventional crops (Borguini et al., 2013). Lycopene is a phytonutrient that has an important role in human health, in particular in the prevention of cancer, cardiovascular diseases and other chronic diseases (Madia et al., 2021). Lycopene content depends on cultivars and other factors such as extraction yield, the cultivation conditions and the climatic conditions. Lycopene is not an essential nutrient, but it is recommended for dietary intake because of its beneficial health properties (Lappi et al., 2021). It is one of the most important antioxidant carotenoids found in abundance in tomatoes and derived products. According to several studies, lycopene, due to its strong antioxidant activity, prevents degenerative, renal and cancerous diseases (Madia et al., 2021). It is also involved in the reproductive system by preventing the oxidation of glutathione S-transferase, glutathione peroxidase, glutathione reductase and 5-aminolevulinic acid dehydratase (Ranjbar Nedamani et al., 2019).

Vitamin C content ranged from 9.62 to 27.82 mg/100 g DM. The peels were the richest in vitamin C. These levels were lower than those reported elsewhere (Cesare et al., 2021). This difference may be linked to the cultural and climatic conditions. Vitamin C plays a role of antioxidant and would prevent certain diseases such as reproductive diseases (Madia et al., 2021). It could prevent certain cancers by intervening in the cell proliferation cycle. It has protective effects against endothelial dysfunction, blood pressure and blood vessel changes that precede cardiovascular disease (Milani et al., 2021). The intake of vitamin C is necessary in order to avoid complications due to the increase in cholesterol and triglycerides in the blood (Milani et al., 2021).

Statistical analysis of phytonutrients in tomato by-products reveals the existence of several clusters (Figure 3). The first cluster in blue is formed by salicylic acid and anthocyanins; the second cluster in yellow is constituted by phenolic compounds, vitamin C, carotenoids and antioxidant activities. The third cluster included chlorophylls a and b. The distribution of phytonutrients by cultivar showed that the main antioxidants in tomato by-products are carotenoids, phenolics and vitamin C regardless of tomato cultivar (Figure 4). However, chlorophylls a and b are more concentrated in Petomech by-products, while salicylic acid and anthocyanins are not directly related to the cultivar but are closer to F1 Mongal than to Petomech. Their contents would thus be linked to the cultivation conditions.

Figure 3. Principal Component Cluster Analysis.

Figura 3. Análisis de Clúster de Componentes Principales.

Figure 4. Distribution of phytonutrients according to cultivars.

Figura 4. Distribución de fitonutrientes según los cultivares.

Oxidative stress is identified as the main cause of several diseases, notably chronic diseases. Oxidative stress consists of an aggression of the cells by free radicals threatening the health of the organism. They are generated by many environmental factors as well as by certain lifestyle habits such as stress, has a deleterious effect on the body and contributes to the development of certain pathologies, overweight and obesity. Chronic diseases such as obesity, hypertension and diabetes are due to an imbalance between the production of free radicals and the antioxidant capacity of the body (Khan et al., 2021). Free radicals are normally taken care by the antioxidant systems of the body, however, when there is a strong accumulation, these systems are no longer able to scavenge oxidants. This insufficiency of the body’s defense must be reinforced by an external contribution of dietary antioxidant compounds. Therefore, it is recommended to consume foods with a high antioxidant capacity, especially those rich in carotenoids, vitamins C and E and polyphenols (Kosmalski et al., 2022). The exploration of natural antioxidant compounds for free radical scavenging is a necessary perspective to prevent these chronic diseases (Sansone & Brunet, 2019). These compounds are mostly found in plants such as tomatoes and tomato products. The tomato by-products inhibited the DPPH radical from 38.51% to 61.38%. The peels showed the best inhibition proportions and the seeds the lowest. There was no significant difference between the inhibition rates of individual by-products. As for the FRAP the seeds showed contents from 70.19 to 73.63 µg EAA/g DM. The peels showed contents from 108.55 to 120.86 µg EAA/g DM without significant differences (P ≤ 0.001). These values are lower than those reported in previous studies on organic and aquaponic culture (Braglia et al., 2021). Tomato peels and seeds have been shown to have a very high antioxidant capacity capable of scavenging free radicals. The highest scavenging of the peels could be due to their role as protective organs as they are more exposed than seeds. The contents found in this study were higher than tomato peels from Egypt (Elbadrawy & Sello, 2016). The scavenging of the DPPH radical increases according to the concentration and the extraction solvent. The antioxidant activity of the FRAP method is similar to the DPPH method with slight differences. Principal component cluster analysis revealed that in tomato by-products the scavenging of DPPH free radicals is governed by lycopene, β-carotene, vitamin C and total flavonoids. However, iron scavenging power is more correlated with total phenolics. This corroborates the idea that carotenoids are the best antioxidant in tomato. Principal component analysis of phytonutrients in peels and seeds showed a positive correlation between chlorophyll a and b on the one hand and phenolic compounds, vitamin C, carotenoids and antioxidant activities on the other hand (Figure 5). However, salicylic acid and anthocyanin showed weakest correlations. The hierarchical classification (Figure 6) showed a link between total polyphenols and FRAP antioxidant activity on one hand and on the other a correlation between carotenoids and vitamin C and between these parameters the DPPH antioxidant activity. In addition, the analysis of phytonutrient distribution by cultivar showed that antioxidant activities, phenolics, carotenoids and vitamin C are common among tomato cultivars (Figure 4). These results demonstrated that tomato by-products are natural sources of bioactive compounds that deserve to be valorized in order to have functional foods accessible at a lower cost and capable of fighting chronic diseases (Wu et al., 2022). Antioxidant reinforces the immunity of the human organism, thus protecting it from cancerous diseases and other diseases caused by oxidative stress. These tomato by-products can therefore contribute to the prevention and treatment of these diseases and therefore are important sources of nutraceuticals. Therefore, as foods rich in antioxidant compounds, their consumption can offer increased protection against reactive oxygen species and the diseases they cause (Severo et al., 2021). In fact, this antioxidant capacity protects the organism from the oxidation of fats and the deposit of cholesterol blood vessels. It controls the glycemic index by regulating the metabolism of carbohydrates (Cannataro et al., 2021). The accumulation of saturated fats and cholesterol is responsible for the narrowing of the arteries diameter and therefore for hypertension. Antioxidants therefore have the role of increasing the fluidity of the blood by preventing the deposit of cholesterol and fats (Fernandes et al., 2022). Tomato peels and seeds are real sources of natural antioxidants to consume for the prevention of chronic diseases (Valle-Castillo et al., 2021). Foods containing antioxidant compounds may be interesting in agro-industry (Shirahigue & Ceccato-Antonini, 2020).

Figure 5. Principal component analysis of phytonutrients in peels and seeds.

Figura 5. Análisis de componentes principales de fitonutrientes encontrados en cáscaras y semillas.

Figure 6. Hierarchical classification of phytonutrients in peels and seeds.

Figura 6. Clasificación jerárquica de fitonutrientes encontrados en cáscaras y semillas.

4. Conclusion

Tomato seeds and peels have different qualitative and quantitative composition in bio-active phytonutrients such as phenolic compounds, chlorophyll, carotenoids and vitamin C. These by-products, in addition to their nutritional potential, would be important nutraceutical sources. Analyses have shown that the levels of polyphenols, carotenoids and vitamin C were positively correlated. This study showed that, β-carotene, vitamin C and lycopene have very important antioxidant activities with respect to their strong correlation with free radical scavenging. These by-products have shown very good nutraceutical potential to be used in the fight against obesity and its complications. These tomato by-products can be valorized in the formulation of bioactive foods or as nutraceuticals.

Author contributions

Conceptualization, K. K. (Kaboré Kabakdé) and K. K. (Konaté Kiessoun); formal analysis, S. B., S. A. and R. D.; investigation, K. K. and S. H.; methodology, K. K. and K. K.; supervision, D. M. H. and K. K.; writing – original draft, K. K.; writing – review and editing, K. K., D. M. H., S. A., D. R. and S. H. All authors have read and agreed to the published version of the manuscript.

Acknowledgement

The African Biotechnology Network (RABIOTECH, ISP/IPICS project N° 172 600 000) is appreciated for supporting publication fees and academic mobilities.

Disclosure statement

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

Data availability statement

Study data are available from the corresponding author for researchers upon request.

Additional information

Funding

Financial support was provided by The West African Biotechnology Network [RABIOTECH, ISP/IPICS Project N°172 600 000].