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Article

Comparison in Content of Total Polyphenol, Flavonoid, and Antioxidant Capacity from Different Organs and Extruded Condition of Moringa oleifera Lam

by
Min-Ook Park
1,2,
Choon-Il Park
2,
Se-Jong Jin
2,
Mi-Ri Park
3,
Ik-Young Choi
1,
Cheol-Ho Park
2,4 and
Md. Adnan
4,*
1
Department of Agro-Industry, Kangwon National University, Chuncheon 24341, Korea
2
Cheorwon Cosmetic Agricultural Cooperation, Cheorwon 24047, Korea
3
Cheorwon Plasma Research Institute, Cheorwon 24047, Korea
4
Department of Bio-Health Convergence, Kangwon National University, Chuncheon 24341, Korea
*
Author to whom correspondence should be addressed.
Processes 2022, 10(5), 819; https://doi.org/10.3390/pr10050819
Submission received: 28 March 2022 / Revised: 16 April 2022 / Accepted: 18 April 2022 / Published: 21 April 2022
(This article belongs to the Special Issue Advances in Food Processes Modeling)
Browse Figures
Versions Notes

Abstract

:
Recently, interest in exploring phytochemicals with health benefits has grown significantly. In this research, we aimed to develop the processing profile and functionality of Moringa oleifera Lam. Here, we implemented biopolymer-mediated extrudate formulations of M. oleifera (leaves, seed, and husk) in order to enhance the phenolic, flavonoid, and antioxidant capacity. The formulation-1 (F1) was prepared for leaves, seed, and husk using biopolymers (10% w/w), namely: whey protein isolate (10% w/w) and lecithin (5% w/w) with vitamin E (2% w/w). The formulation-2 (F2) was composed of lecithin (5% w/w) with ascorbyl palmitate (10% w/w) and vitamin E (2% w/w), processed by hot-melt extrusion (HME). It was observed that the total phenol and flavonoid contents were persistent in the lecithin-mediated F2 formulation of leaves, seed, and husk. Likewise, antioxidant capacity was significantly stayed in the F2 formulation of all organs, compared to the extrudate and control. The IC50 values revealed that the leaves of the F2 formulation showed strong free radical scavenging capacity compared to the F2 formulation of seed and husk. It was concluded that the F2 formulation could be used in the different parts of M. oleifera processing to boost functionality.

1. Introduction

Antioxidant therapy regulates the metabolic process and maintains our health status by controlling various risk factors of diseases. The cellular metabolism or biological dysfunction of living cells causes an inordinate number of reactive oxygen species (ROS) to be produced, which induces oxidative damage throughout the organs [1]. Several life-threatening diseases, including neurodegenerative disease, cancer, diabetes mellitus, ischemic heart disease, and many other chronic diseases, are also responsible for such free radicals [2,3]. Hence, ROS neutralization with appropriate antioxidant supplementation is necessary to detoxify organisms. Mechanistically, antioxidants reduce the harmful effects of autoxidation by inhibiting free radical formation or preventing their propagation [4]. In many food industries, several synthetic antioxidants (tert-butyl hydroquinone, butylated hydroxytoluene, propyl gallate, and butylated hydroxyanisole) have indispensable roles in the processing of food products [5]. However, due to their suspected side effects as promoters of various life-threatening diseases, food industries are refocusing on excellent sources of natural antioxidants. In this regard, plant materials (leaves, seeds, fruits, and husk) possessing abundant polyphenols have drawn significant attention in food science and nutrition [6,7].
To ensure optimum nutritional efficacy, bioactive compounds or therapeutic moieties should be protected from autoxidation [8]. Therefore, an effective encapsulation system through biopolymers provides hydrogels, layer–layer films, emulsions, micro- and nano-encapsulation, bio-macromolecule structure, or through forming composite films of active compounds [9]. An imperative biopolymer, “lecithin”, forms phospholipid vesicles in an aqueous medium, providing a liposomal delivery system that can overcome the pharmacokinetic limitations of bioactive compounds. Lecithin has an intrinsic duality (amphiphilic) nature, acting as both a super-efficient zwitterionic-type surfactant and a protective coating agent [10]. These unique properties make lecithin a potent carrier for hydrophilic and lipophilic micronutrients. To encapsulate heat-sensitive bioactive compounds, whey proteins concentrate (WPC) form a polymeric networking hydrogel, which enhances the nutraceutical compound’s stability. In addition, due to their high nutritional value, WPC and lecithin are widely used in formulated food [11,12].
Currently, food industries are focusing on ready-to-eat food, and hot-melt extrusion (HME) has gained much consideration in the research of modern functional food processing developments [13]. It has excellent beneficial effects such as increased solubility, miscibility, and bioavailability of poorly soluble compounds and materials. The HME mixes raw materials (coarse powder) with antioxidants, lubricants, plasticizers, polymers, excipients, etc., under high shear and elevated temperatures; hence, some sensitive bioactive compounds face thermal and mechanical degradation during the processing operation [14,15]. To resolve this problem, plasticizers or stabilizers can be used, which mainly enhance the workability and processability of biopolymers by modifying their physical properties. In such cases, Ascorbyl Palmitate “potent plasticizer” and Vitamin E “universal stabilizer” are frequently used as safe food additives for food processing and preservation [16,17]. Moreover, many previous studies reported that adding such ingredients during food processing can enhance the final products’ stability, quality, shelf life, and nutritional properties [18,19].
The application of medicinal plants and natural herbs with a view to maintaining health status has obtained an imperative demand in functional food industries. Moringa oleifera Lam. is known as a miracle tree owing to its rich source of innumerable nutrients with high biological values [20]. Each part of this plant is used in natural medicine, dietary supplements, food, feed, and even in cosmetic products. Research has found that, due to the presence of abundant phytochemicals, as well as macro- and micronutrients, M. oleifera remarkably recovered the embryonic health quality [21]. Daily supplementation of M. oleifera to rabbits, cows, goats, mice, and some species of fish revealed rapid growth and reproductive performance. In humans, the reported major health effects of M. oleifera are antidiabetic, anticancer, anti-inflammatory, neuroprotectant, antiulcer, etc., [22]. A study implemented various treatments, such as boiling, simmering and blanching, on Moringa leaves with the aim of enhancing antioxidant activity. It was concluded that antioxidant capacity was significantly increased by boiling, among all other techniques [23].
In this study, we aimed to enhance the secondary metabolites and antioxidant capacity of M. oleifera (leaves, seed, and husk) by preparing various formulations with physical (HME-induced temperature and high share) and chemical (polymer-carriers: whey proteins and lecithin; plasticizer: Ascorbyl Palmitate; stabilizer: Vitamin E) modification. We hypothesized that polymer–plasticizer–stabilizer-based composites can encapsulate soluble and insoluble bioactive compounds, and thus such a formulation can serve as a nutrient-rich food source.

2. Materials and Methods

M. oleifera (leaves, seed, and husk) was procured from Chuncheon local market, Chuncheon, Korea. Lecithin, Ascorbyl Palmitate, Vitamin E, and whey protein were purchased from Sigma (Sigma Chemical Co., St. Louis, MO, USA). Phenolic reagent (Folin Ciocalteu, 2 N), sodium bicarbonate (Na2CO3), aluminum nitrate (AlNO3)3, potassium acetate (CH3CO2K), and DPPH (2,2-diphenyl-1 picryl hydrazyl) were also procured.

2.1. Preparation of Formulations

The collected M. oleifera (leaves, seed, and husk) was first blended using an electric blender. Afterwards, sieves of different series were used to fractionate the blended powders, which were then passed into the 700 µm mash size sieves. The remaining powders (big particles) on the sieves were crushed again to maintain a uniform size of particles. The obtained fine powder of M. oleifera (leaves, seed, and husk) was stored at 4 °C until further investigations.
In this study, M. oleifera-based (leaves, seed, and husk) food composites were formulated according to the experimental conditions. In composition, Ascorbyl Palmitate acted as a plasticizer, Vitamin E acted as stabilizer, and two types of food grade biopolymers, such as whey protein and lecithin, were used along with M. oleifera (leaves, seeds, and husk) powder for solid formulations. M. oleifera (leaves, seed, and husk) were mixed with water with different ratios of biopolymers and preservatives, as shown in Table 1.
The formulated composites were extruded using an STS-25HS twin screw extruder, commonly called hot-melt extrusion (HME) (Hankook E.M. Ltd., Pyoung-Taek, Korea). The HME was furnished with various parameters, these being 1 mm of round shape die, a feeding rate of 50 g/min, and a 200 rpm screw speed with high shear (80–100 bar pressure). During the extrusion process, water was added (50–60 mL/min) to the extruder barrel in order to avoid the thermal degradation of material. The barrel temperature of HME was maintained at 70-80-80-70 °C in order to protect the biopolymer used in this study. For instance, whey protein is denatured when heated above 70 °C. On the other hand, the phase transition temperature of lecithin is above 60 °C. In view of this information, an ideal processing temperature was optimized for this study. After successful extrusion, all samples (extrudate, F1, and F2) were oven dried at 55 °C for 24 h. The dried samples were again powdered following the above-mentioned process and stored in a refrigerator at 4 °C for further analysis. For experimental accuracy, three replications were performed for each formulation to obtain reliable data.

2.2. Extract Preparation

The fine powder (200 g of each) of the extrudate, F1, and F2 was dissolved in 70% of ethanol (1 L v/v in water). The mixture was placed at room temperature for 4 days on a rotary shaker (continuous stirring and shaking) and then filtered by Whatman filter paper. The filtered solution was evaporated using a rotary evaporator which resulted in a semisolid yield. The collected yield of each sample was preserved in a refrigerator for further investigation.

2.3. Estimation of Total Phenolic Content

The total content of phenol was evaluated by the Folin Ciocalteu assay [24]. In brief, each 1 mL sample of extract (1 mg/mL) was added to a test tube containing 200 µL of phenol reagent (1 N). The volume of the mixture was increased by adding 1.8 mL of deionized water. After gentle shaking, the mixture was set aside for 5 min at room temperature for the reaction. Afterwards, 400 µL of sodium carbonate (10% in water, v/v) was added and the final volume (4 mL) was adjusted by adding 600 µL of deionized water. The absorbance was measured at 725 nm after incubation for 1 h at room temperature. A calibration curve of gallic acid was used to calculate TP, expressed as mg/g of gallic acid equivalent (GAE).

2.4. Estimation of Flavonoid Content

The total flavonoid content was measured based on our previous study [24]. In short, each sample (500 µL) of extract (1 mg/mL) was mixed with 100 µL of aluminum nitrate (10%) and 100 µL of potassium acetate (1 M) solution. Later, distilled water (3.3 mL) was added to make a total volume of 4 mL. This was then vortexed and incubated for 40 min. The TF content was measured using a spectrophotometer (UV-1800 240 V, Shimadzu Corporation, Kyoto, Japan) at 415 nm. The TF content was expressed as mg/g quercetin equivalents.

2.5. DPPH and H2O2 Free Radical Scavenging Capacity

The antioxidant capacity was assessed using DPPH free radical and H2O2 [25]. In order to assess DPPH scavenging capacity, different concentrations (100, 200, 300, 500, and 1000 µg/mL) of extract (1 mL) were added to 3 mL of DPPH solution. The control was prepared with 1 mL of distilled water in 3 mL of DPPH solution. The mixture was put in a dark place for 30 min at room temperature after being shaken vigorously. For H2O2 scavenging, 0.4 mL of various concentration of extract (100, 200, 300, 500, and 1000 µg/mL) was added to 0.6 mL of H2O2 solution (4 mM prepared with 0.1 M phosphate buffer pH 7.4). The mixture was shaken and incubated (for 10 min). The percent inhibition was calculated against a blank sample using the following equation:
Inhibition (%) = [(blank sample − extract sample)/blank sample] × 100

2.6. Statistical Analysis

Data are expressed as mean ± standard deviation (SD) of triplicate measurements. The obtained results were compared among the M. oleifera (leaves, seed, and husk) using a paired t-test, in order to observe the significant differences at the level of 5%. The paired t-test between the mean values of all samples and control was analyzed by MINITAB (version 17.0, Minitab Inc., State College, PA, USA).

3. Result and Discussion

3.1. Total Phenolic and Flavonoid Contents

In this study, the contents of phenolic, flavonoid, and antioxidant capacity of M. oleifera (leaves, seed, and husk) were elevated by processing hot-melt extrusion (HME). Here, two types of formulations (F1 and F2) were prepared using a biopolymer, a plasticizer, and a stabilizer with high share and controlled temperature (selected based on the melting point of biopolymers).
Table 2 and Table 3 show that the phenolic and flavonoid contents (TPC and TFC) in the extrudate compared to the control noticeably increased. This is because of the high mechanical energy and temperature of the barrel section induced by HME, which enhanced the extraction process of phenolic and flavonoid compounds [26]. The main feature of HME is the transformation of the high crystalline to amorphous state by de-structuring the fiber matrix, which results in the high surface area and saturation solubility [27]. Research has reported that HME has the highest extraction of secondary metabolites (phenolic and flavonoid contents) in ginseng and black rice [28,29].
However, the most promising TPC and TFC were found in F2 of M. oleifera (leaves, seed, and husk). Mainly, TPC (11.27 + 0.09 mg/g) and TFC (10.61 + 0.05 mg/g) were noted as containing a significant amount in the leaves of F2 in comparison to seeds and husk. Research has found that the highest amount of total phenolics was 13.23 g/100 g extract, and that of total flavonoids was 6.20 g/100 g extract from the maceration with 70% ethanol of dried leaves [30]. In our previous study, TPC and TFC were enhanced in the kenaf seed extract following the same process of HME and found to be 2.4-fold higher than control [31]. After the leaves, F2 in seed was found to contain 3.19-fold higher TPC and 3.74-fold higher TFC compared to the control. A similar attribution was also noticed in the case of husk, which also showed enhanced TPC and TFC.
Commonly, plants possess two types of phenolic compounds, for instance, soluble phenolic and insoluble phenolic compounds. The vacuoles of plant cells contain soluble phenolic compounds and the cell wall matrix reserves insoluble phenolic compounds [32]. To obtain the highest extraction, the high share of HME stimulates the cell wall matrix disruption followed by decomposing the carbon–carbon bonds of phenolic and conjugated moieties. Such a mechanism assists the extraction of secondary metabolites and diffuses rapidly in the solution [33].

3.2. Antioxidant Activity

The antioxidant capacity of M. oleifera (leaves, seed, and husk) increased more significantly when measured using the DPPH and OH free radical scavenging capacity (Figure 1 and Figure 2). The activity remarkably varied among the control, extrudate, F1, and F2 of leaves, seed, and husk. Overall, the highest antioxidant activity was observed in the F2 leaves (Figure 1A and Figure 2A).
Interestingly, the scavenging capacity (DPPH and H2O2) of F1 was found to be lower in leaves compared to extrudate, which might be due to the parallel content of total phenolic compounds and flavonoids. In contrast, F1 showed noticeable changes in DPPH and H2O2 free radical scavenging in seed and husk (Figure 1B,C and Figure 2B,C). Such variation can be explained by the excellent secondary metabolite contents in F1. However, the optimum DPPH scavenging capacity was manifested by the F2 of leaves (84.2 ± 0.17%), followed by seeds (74.8 ± 0.11%), and husk (67.7 ± 0.23%) at 1000 µL. The analysis of IC50 recommended that the F2 of leaves require 10 times and 5.95 times lower concentrations to scavenge 50% DPPH free radicals in comparison to F2 seeds and husk, respectively (Figure 1D). A similar pattern was noted for H2O2 scavenging activity. Here, a strong IC50 was observed for F2 leaves (309.6), followed by seed (524.28), and then husk (881.1) (Figure 2D).
Biopolymers are effectively implemented to encapsulate bioactive compounds in order to protect chemical and thermal degradation [34]. The encapsulation efficiency of the biopolymer depends on the chemical nature of the target molecules to be encapsulated [35]. The incorporation of phenolic compounds into the polymeric matrix is an effective approach to protect the degradation of the molecules due to environmental factors [31]. Generally, biopolymers reduce the melting point of the secondary compounds by forming hydrogen bonds between polymers and mixtures [36]. It is observed from the current study that the phenolic, flavonoid, and antioxidant capacity was higher in F2 that it was in the lecithin-mediated formulation. Previous research aligned with this positive response [14,26,31]. It was stated that lecithin-formed liposomes efficiently protect both soluble and insoluble active compounds by lipid and phospholipid bilayers (Figure 3), and encapsulation efficiency is enhanced in a slightly acidic environment [37,38]. The higher stability of phenolic compounds and flavonoids in an acidic environment is because of the availability of H+ donor sites by acid which protects the produced free radical [39]. It was previously recognized that ascorbyl palmitate or ascorbic acid is the most efficient plasticizer among the broadly used acids in food, such as citric acid, malic acid, tartaric acid, and HCL [40]. Importantly, the barrel temperature of HME denatures the whey protein, which excites the tannin–protein interaction, and subsequently increases the antioxidant properties [41]. Other research revealed that protein–compound complex formations improved the bioavailability of active constituents, and thereby improved antioxidant activity [42].
However, the highest obtained TPC, TF, and antioxidant activities in F2 formulation are due to the electrostatic interactions and established hydrogen bonding between bioactive molecules and lecithin phospholipids [43]. The stability of phenolic and flavonoid contents in HME is due to the presence of vitamin E, which also elevates antioxidant capacity [44].

4. Conclusions

It was noted that higher total phenolic and flavonoid contents, as well as optimum antioxidant capacity, depend on the chemical nature of the formulated biopolymer. The overall outcomes show that F2 (ascorbyl palmited-lecithin-vitamin E) reserved higher secondary metabolites and antioxidant capacity in solid extrudate. Our proposed technical approach would be to help process and preserve secondary metabolite-enriched foods, which would be beneficial for health.

Author Contributions

Conceptualization, M.-O.P. and M.A.; methodology, M.-O.P. and I.-Y.C.; software, C.-I.P.; validation, S.-J.J. and M.-R.P.; formal analysis, M.-O.P., C.-I.P. and M.-R.P.; investigation, C.-I.P., M.-R.P. and I.-Y.C.; resources, C.-H.P.; data curation, C.-I.P. and S.-J.J.; writing—original draft preparation, S.-J.J. and M.A.; writing—review and editing, M.-O.P., I.-Y.C. and C.-H.P.; supervision, M.A.; project administration, M.A.; funding acquisition, C.-H.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by the Ministry of Small and Medium-sized Enterprises (SMEs) and Startups (MSS), Korea, under the “Regional Specialized Industry Development Plus Program (R&D, Project number: S3092631)” supervised by the Korea Technology and Information Promotion Agency for SMEs (TIPA).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The study did not report any data.

Conflicts of Interest

The authors have declared no conflict of interest. They have no known competing financial interests or personal relationships that could have appeared to influence the research reported in this publication.

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Processes 10 00819 g001 550
Figure 1. DPPH free radical scavenging capacity. (A) Moringa leaves composites (MLC), (B) moringa seed composites (MSC), (C) moringa husk composites (MHC), and (D) inhibitory concentration (IC50) of F2. Mean ± SD from triplicate separated experiments are shown. Values expressed by different letters in each column are significantly different in the t-test (p < 0.05).
Figure 1. DPPH free radical scavenging capacity. (A) Moringa leaves composites (MLC), (B) moringa seed composites (MSC), (C) moringa husk composites (MHC), and (D) inhibitory concentration (IC50) of F2. Mean ± SD from triplicate separated experiments are shown. Values expressed by different letters in each column are significantly different in the t-test (p < 0.05).
Processes 10 00819 g001
Processes 10 00819 g002 550
Figure 2. Hydrogen peroxide free radical scavenging capacity. (A) Moringa leaves composites (MLC), (B) moringa seed composites (MSC), (C) moringa husk composites (MHC), and (D) inhibitory concentration (IC50) of F2. Mean ± SD from triplicate separated experiments are shown. Values expressed by different letters in each column are significantly different in the t-test (p < 0.05).
Figure 2. Hydrogen peroxide free radical scavenging capacity. (A) Moringa leaves composites (MLC), (B) moringa seed composites (MSC), (C) moringa husk composites (MHC), and (D) inhibitory concentration (IC50) of F2. Mean ± SD from triplicate separated experiments are shown. Values expressed by different letters in each column are significantly different in the t-test (p < 0.05).
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Figure 3. Lecithin-mediated liposome formation and entrapped molecules.
Figure 3. Lecithin-mediated liposome formation and entrapped molecules.
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Table
Table 1. The formulation composition of the extrudate M. oleifera (leaves, seed, and husk) and HME processing parameters.
Table 1. The formulation composition of the extrudate M. oleifera (leaves, seed, and husk) and HME processing parameters.
MaterialsMixing Ratio (w/w) and Preparation of Formulation
ControlExtrudateF1F2
M. oleifera (leaves, seed, and husk)1001008383
Whey protein isolated (WPI)NANA10NA
LecithinNANA55
Ascorbyl Palmitate (AP)NANANA10
Vitamin ENANA22
Processing statusNon extrusionExtrusionExtrusionExtrusion
HME barrel temperature (°C)NA70-80-80-7070-80-80-7070-80-80-70
Here, NA = Not applicable.
Table
Table 2. Total phenolic contents of the control, extrudate, F1 and F2 formulation of M. oleifera (leaves, seed, and husk).
Table 2. Total phenolic contents of the control, extrudate, F1 and F2 formulation of M. oleifera (leaves, seed, and husk).
Total Phenolic Content (mg/g)
Concentration (1 mg/mL)LeavesSeedHusk
Control8.73 + 0.04 bd3.17 + 0.28 cd1.74 + 0.02 d
Extrudate8.96 + 0.03 b5.29 + 0.16 c3.86 + 0.04 bc
F18.98 + 0.05 c6.04 + 0.18 b4.05 + 0.08 b
F211.27 + 0.09 a10.13 + 0.14 a6.06 + 0.13 a
Mean ± SD from triplicate separated experiments are shown. Values marked by different letters in each column are significantly different in the t-test (p < 0.05).
Table
Table 3. Total flavonoid contents of the control, extrudate, F1 and F2 formulation of M. oleifera (leaves, seed, and husk).
Table 3. Total flavonoid contents of the control, extrudate, F1 and F2 formulation of M. oleifera (leaves, seed, and husk).
Total Flavonoid Content (mg/g)
Concentration (1 mg/mL)LeavesSeedHusk
Control9.60 + 0.03 bd2.62 + 0.08 c1.65 + 0.15 cd
Extrudate9.82 + 0.04 b3.73 + 0.05 bc1.87 + 0.08 c
F19.94 + 0.06 bc3.95 + 0.02 b2.11 + 0.05 b
F210.61 + 0.05 a9.82 + 0.05 a3.72 + 0.07 a
Mean ± SD from triplicate separated experiments are shown. Values marked by different letters in each column are significantly different in the t-test (p < 0.05).
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Park, M.-O.; Park, C.-I.; Jin, S.-J.; Park, M.-R.; Choi, I.-Y.; Park, C.-H.; Adnan, M. Comparison in Content of Total Polyphenol, Flavonoid, and Antioxidant Capacity from Different Organs and Extruded Condition of Moringa oleifera Lam. Processes 2022, 10, 819. https://doi.org/10.3390/pr10050819

AMA Style

Park M-O, Park C-I, Jin S-J, Park M-R, Choi I-Y, Park C-H, Adnan M. Comparison in Content of Total Polyphenol, Flavonoid, and Antioxidant Capacity from Different Organs and Extruded Condition of Moringa oleifera Lam. Processes. 2022; 10(5):819. https://doi.org/10.3390/pr10050819

Chicago/Turabian Style

Park, Min-Ook, Choon-Il Park, Se-Jong Jin, Mi-Ri Park, Ik-Young Choi, Cheol-Ho Park, and Md. Adnan. 2022. "Comparison in Content of Total Polyphenol, Flavonoid, and Antioxidant Capacity from Different Organs and Extruded Condition of Moringa oleifera Lam" Processes 10, no. 5: 819. https://doi.org/10.3390/pr10050819

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