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International Journal of Pharmacology

Year: 2021 | Volume: 17 | Issue: 4 | Page No.: 208-216
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ABSTRACT

Background and Objective: Medicinal plants and their bioactive extracts have comprehensively been considered by researchers to turn out some prospective drugs with no toxicity. Pomegranate peel is considered as a food waste part obtained during the manufacture of the juice. The study aimed to comparative analysis of nutritional values, microbial population, bioactive components as polyphenol, flavonoid, tannin, anthocyanin and antioxidant activities of pomegranate peel extracts. Materials and Methods: The nutritional values such as moisture, ash, carbohydrates, protein, fibre, fat and reducing sugar contents; microbial population as some bacterial and fungal strains; bioactive components as total polyphenol, flavonoid, tannin and anthocyanin contents and antioxidant activities of pomegranate peel extracts for four pomegranate varieties (Wonderful-Francis-Cloud-Balegal) was analyzed by different methods. Tukey test was used for the statistical analysis. Results: Wonderful variety reported the highest moisture 6.95%, ash 4.22 g/100 g, protein 8.97 g/100 g, fibre 19.41 g/100 g and reducing sugar 3.71 g/100 g. Results on the microbial population observed that Francis variety recorded the highest DIZ 16.2 and 15.72 mm on Escherichia coli and Aspergillus niger. The highest phenolics and anthocyanin were detected in methanol (ME 90%) extract of Francis and Wonderful varieties 26.17 g GAEs/100 g and 0.133 g/100 g, respectively. Conclusion: The ability of pomegranate peel varieties extracts to scavenge antioxidant activities was a little similar and it can be stated that pomegranate peel extracts have high bioactive components and antioxidant activities to be used for various fields such as therapeutic, pharmaceutical and medicinal manufactures.
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How to cite this article

Rokayya Sami, Ebtihal Khojah, Ahmed M.A. Mansour, Amina A.M. Al-Mushhin, Abeer Elhakem, Dina M. El-Sherif, Mohammed Saeed Alkaltham and Ahmad Mohammad Salamatullah, 2021. Nutritional Values, Microbial Population and Bioactive Components of Pomegranate (Punica granatum L.) Peel Extracts. International Journal of Pharmacology, 17: 208-216.

DOI: 10.3923/ijp.2021.208.216

URL: https://scialert.net/abstract/?doi=ijp.2021.208.216

INTRODUCTION

Bioactive compounds and phytochemicals have been connected with health due to the high intake of vegetables and fruits especially pomegranate1-3. Pomegranate (Punica granatum L.) is one of the oldest trees worldwide. Actuality, polyphenols can effectively exhibit a variety of physiological functions, such as anti-allergenic, anticancer, anti-inflammatory, antiviral, antioxidant, anti-thrombotic and antimicrobial4. Polyphenols in pomegranate are more efficient against disease than those are in green tea5. Besides, raising records of pomegranate foodstuffs, cosmetics, supplements and beneficial formulae are available in stores at convenient prices6. All pomegranate parts including peels have been good used for medical and therapeutic purposes such as stomachic, urinary infection, fever, dysentery, diabetes, bronchitis, diarrhoea, vaginitis, malaria, intestinal parasites ischemia, cardiac disease, aids and cancer7,8. Pomegranate extracts can control cholesterol levels, avoid heart attacks and increase the haemoglobin count by decreasing lipids levels in the blood9,10. Pomegranate juice is used for eye drops manufacture against cataracts11. Currently, technical attention for the chemical properties of pomegranate is not just for the arils, juice, flower, leaf but also on the peel, which represents about (40-50%) of the total bulk by weight12. Peels are usually discarded and therefore constitute the major by-product resulted after the extraction of the pomegranate juice13. In vitro and in vivo some biological activities against pathogenic fungus and bacteria were achieved on the pomegranate peels extract illustrated highly antimicrobial activities14. Solvent extractions have important effects on the extract's bioactive properties and phytochemicals due to their different polar properties15-17. Numerous studies exposed that bioactive compounds can differ from the extractor of solvent polarities7,11,18. Pomegranate peels have received more attention as natural preservatives in meat and can be exploited as bi-preservatives in food industry applications and nutraceuticals13,19.

Consequently, this research was carried out for a comparative analysis of nutritional values, microbial population, bioactive components as polyphenol, flavonoid, tannin, anthocyanin and antioxidant activities of pomegranate peel extracts.

MATERIALS AND METHODS

Study area: The current work was carried out at the Department of Food Science and Nutrition, Taif University, Saudi Arabia from November, 2020-March, 2021.

Chemicals: All the solvents (methanol, ethanol) were reagent grade obtained from (Tianjin Fu, China). Sabouraud Dextrose Agar was purchased from Agriculture's culture collection, Egypt. Folin and rutin reagents were from (Oxford lab., United Kingdom). Gallic and tannic acids and other reagents were from Sigma (USA).

Plant materials: Pomegranate varieties (Wonderful-Francis- Cloud-Balegal) at the maturity stage were randomly obtained from a local market of Taif, Saudi Arabia. Pomegranates were manually peeled carefully by a sharp knife. Peels were washed, sun-dried before extraction at room temperature, milled and stored (4°C) until use.

Preparation of pomegranate extracts: Briefly, finely powdered (10 g) of each variety were separately dissolved in 100 mL of various solvents as methanol (ME 90 and 70%), ethanol (EE 90 and 70%) and water (WE) for microbial population, bioactive compounds and phytochemicals screening. Solvents were blended for 15 min, filtered and centrifuged for 30 min.

Morphological properties determination: In the current study, 30 slices of each variety were evaluated for weight, thickness and colour. Peel weight was evaluated by a digitalized sensitive balance with a capacity of 0-1200 g and an accuracy of ±0.01 g, while the dry matter was evaluated after drying until reaching a constant weight20. Thickness was evaluated by a digital micrometre (Mitutoyo, Tokyo, Japan) at 8 random locations that contain an intermediate point and the average values were estimated21. The colour was evaluated by a ZE-6000 colorimeter (Nippon Co., Tokyo, Japan) calibrated with a white standard tile22. Hunter L*, a* and b* values, as the former allows a better comparison between varieties23.

Nutritional values determination: Moisture, ash, carbohydrates, protein, fibre, fat and reducing sugar contents were carried out as per methods described by Gbenga-Fabusiwa et al.24. The Titratable Acidity (TAA) was evaluated by titration with 0.1 mol L–1 sodium hydroxide up to titration-endpoint of pH equals (8.1)25. Results were expressed as a percentage of citric acids (factor 0.75)26:

Image for - Nutritional Values, Microbial Population and Bioactive Components of Pomegranate (Punica granatum L.) Peel Extracts

Microbial population analysis: Bacterial and fungal strains such as (Bacillus subtilis, Escherichia coli, Klebsiella pneumonia, Pseudomonas aeruginosa and Staphylococcus aureus) and (Candida albicans, Candida pellicullosa and Aspergillus niger) were purchased from Agriculture's culture collection, Egypt and were subjected to ethanolic pomegranate extracts (EE 90%). Bacteria and fungi were evaluated in Sabouraud dextrose agar plates, while ethanol was applied as a negative control according to the described method18, respectively. The ethanolic against bacteria was 10 mg well–1, while it was 200 mg well–1 against fungi. The Diameter of the Inhibition Zone (DIZ) formed around the inoculated well was expressed in mm.

Bioactive components determination
Determination of total polyphenol contents (TPC): The Folin–Ciocalteu method was used to evaluate polyphenol contents with some slight modifications10. Total 100 μg mL–1 of pomegranate extracts were dissolved into (96 well plates), mixed well with corresponded Folin reagent and 1.0 mL 7% of Na2CO3 solution was added. The final solutions were incubated for (90 min) in the dark at ambient temperature. The Plate was read at 765 nm (MRX II, China)27. Analyses were detected in triplicate and polyphenol contents concentrations were calculated as gallic acid equivalents (GAEs) g/100 g as a standard.

Determination of total flavonoid contents (TFC): The number of flavonoid contents in pomegranate peel extracts were detected by the AlCl310,28. To 0.2 mL of pomegranate extracts, 0.2 mL of 30% ethanolic AlCl3·6H2O was immediately added and incubated for (5 min). The absorbance was evaluated at a wavelength of 430 nm2. The number of flavonoid contents was calculated as rutin equivalents (REs) g/100 g as a standard.

Determination of total tannin contents (TTC): Tannin contents were detected according to TS Faten et al.29. Within screw-capped tubes, (1 mL) of pomegranate extracts and (5 mL) of potassium iodide (2.5%) were mixed, then the tubes were closed and placed in a water bath ~30°C for (10 min). The absorbance was evaluated at 590 nm. The results were calculated as tannic acid equivalents (TAEs) g/100 g as a standard.

Determination of total anthocyanin contents (TAC): The TAC was evaluated by mixing aliquot (5 g) of pomegranate extracts with (0.5% 18 mL) hydrochloric acid in methanol and placed for 1 hr before extraction at a wavelength of 520 nm30. Anthocyanin results were calculated as g/100 g as dry weight31.

Antioxidant activities: 2,2-Azino-bis-(3-ethylbenzothiazoline) -6-sulphonate activity (ABTS) and 2,2-diphenyl-1-picrylhydrazyl activity (DPPH) were evaluated by ME 90% according to the mentioned methods16,32. ABTS and DPPH activities were measured at 734 and 517 nm, respectively.

Statistical analysis: Experiments were detected and the results were calculated as the (mean±Standard Deviations) in triplicate per each value. Differences were carried out and considered significantly p<0.05 by the Tukey test.

RESULTS AND DISCUSSION

Morphological properties: A summary of the morphological properties such as weight (g) and thickness (mm) of the pomegranate peel extracts is presented in Fig. 1(a-b). The four varieties such as Wonderful is characterized by large fruit size and softer seeds consistency; Francis is non-pigmented arils with a red-blue colour skin; Cloud is a soft yellow mottled with pink, while seeds are approximately clear; Balegal is extremely sweet, large fruit size with round pale pink and darker flesh. Regarding the peel weight in the fresh pomegranate weight, the range was from 44.71 g for the Balegal variety up to 47.53% for the Cloud variety, which reported the maximum thickness of 0.52 mm (Fig. 1a). These morphological properties are valuable in evaluating the size of the machine component for separation and transportation by hydrodynamic means, deciding the spacing of slicing discs and the numbers of slices33,34. According to colour determinations, the L* value (brightness) of pomegranates was found between 64.33 and 69.2, the a* value (redness) was found between 0.65 and 0.93, while the b* value (yellowness) was between 16.99 and 24.03, Fig. 1b. Orak et al.35 noticed similar consequences for colour determination.

Nutritional values: The summary of the results for all the nutritional values is shown in Table 1. The moisture contents varied from 5.41% for Francis to 6.95% for Wonderful. It can be noticed that the moisture contents were similar to the pomegranate peel variety under the study of El-Hamamsy and El-Khamissi3. Moisture content evaluation is a very essential parameter that has a significant issue on all processing procedures and other physical characterizes36,37 and can be fluctuated by the seasonal temperature and the relative humidity38,39.

Image for - Nutritional Values, Microbial Population and Bioactive Components of Pomegranate (Punica granatum L.) Peel Extracts
Fig. 1: Morphological properties of the tested pomegranate peel extracts
(a) Weight and thickness and (b) Colour


Table 1: Nutritional values of the tested pomegranate peel extracts
Wonderful
Francis
Cloud
Balegal
Moisture (%)
6.95±0.23a
5.41±0.17c
6.88±0.14a
5.87±0.26b
Ash (g/100 g DW)
4.22±0.16a
3.43±0.21c
3.99±0.15b
4.02±0.17b
Carbohydrate (g/100 g DW)
59.83±1.44d
69.22±1.14a
64.75±2.17c
66.88±2.29b
Protein (g/100 g DW)
8.97±0.25a
4.82±0.21d
4.92±0.32c
6.53±0.16b
Fibre (g/100 g DW)
19.41±0.43a
16.33±0.18c
18.32±0.27b
15.93±0.31d
Fat (g/100 g DW)
0.62±0.14d
0.85±0.11b
1.16±0.15a
0.77±0.17c
Reducing sugar (g/100 g DW)
3.71±0.15a
1.98±0.15d
2.42±0.12c
3.13±0.16b
Titratable acidity (citric acid, %)
1.47±0.21c
3.14±0.24a
3.66±0.11d
2.45±0.28b
*Each value presents as mean±standard deviation. Different letters indicate a significant difference (p<0.05) analyzed by Duncan's multiple range tests

Ash contents among pomegranate peel variety were being 3.43 g/100 g in Francis and 4.22 g/100 g in Wonderful. These ash results were similar to the other pomegranate peel varieties11. While total carbohydrates in the pomegranate peel varieties were in-between 59.83 g/100 g in Wonderful and 69.22 g/100 g in Francis. Protein contents varied from 4.82 g/100 g in Francis followed by 6.53 g/100 g in Balegal to reach the highest value 8.97 g/100 g in Wonderful as shown in Table 1. The protein daily allowance is ranged from 50-63 g according to Wu40, which can be detected from the vegetable origin than animal origin especially in developing countries to supply the human needs41,42. The fibre contents were in-between 15.93 g/100 g in the Balegal variety and 19.41 g/100 g in Wonderful variety. Fibre content values can be due to several factors such as type and age43. Cloud variety reported the highest fat content 1.16 g/100 g, while Wonderful variety reported the lowest 0.62 g/100 g. The differences might be mainly perhaps due to genetic backgrounds and the growth conditions which enhanced the fat contents35. The reducing sugar contents were evaluated within 1.98 and 3.71 g/100 g. Cloud had the highest titratable acidity 3.66% followed by Francis at 3.14%, while Wonderful had the lowest 1.47%. Vardin and Abbasoglu44 reported a negative correlation shown between acidity and reducing sugar. The obtained results reported that the pomegranate peels are an excellent source of carbohydrates, fibre and protein while the fat and reducing sugars were very low. The results were similar to those findings by Ranjitha et al.45.

Microbial population: Several studies reported that ethanolic pomegranate peel extract has effective activities against pathogenic bacteria and fungi with no side effects and high cost46,47. Results for the pathogenic bacteria reported that the highest Diameter of Inhibition Zone (DIZ) 13.64 and 15.85 mm were exhibiters for Wonderful variety on Pseudomonas aeruginosa and Staphylococcus aureus, while Francis variety recorded the highest DIZ 16.2 mm on Escherichia coli (Fig. 2a). Cloud and Balegal varieties showed the highest DIZ 13.88 and 11.96 mm on Bacillus subtilis and Klebsiella pneumonia, respectively. The current results were agreed with Nozohour et al.48 who reported antibacterial activities against Staphylococcus aureus and Pseudomonas aeruginosa. The detected antibacterial activity of pomegranate peel extracts can be due to the presence of metabolic toxins that defence against Gram-negative and positive bacteria49.

Image for - Nutritional Values, Microbial Population and Bioactive Components of Pomegranate (Punica granatum L.) Peel Extracts
Fig. 2(a-b): Microbial population of the tested pomegranate peel extracts
(a) Antibacterial activity and (b) Antifungal activity

The data of Fig. 2b presents DIZ of the pathogenic fungi which reported that the highest DIZ 16.87 mm on Candida albicans was recorded for Wonderful variety, while Cloud reported the highest DIZ on Candida pellicullosa. Francis variety had the highest DIZ 15.72 mm on Aspergillus niger and the other hand, Balegal had the lowest. According to the previous results, pomegranate peel extracts had effective anti-fungal activities which agreed with Bassiri et al.50 who reported antifungal activities against Candida pellicullosa and Candida albicans.

Bioactive components
TPC results for peel pomegranate extracts: Pomegranate varieties were detected by various solvents according to the polarity. The extraction results depended on the concentration and solvent type, which differed among pomegranate peel extracts. The result of Fig. 3a shows TPC results of peel pomegranate extracts range (7.07-26.17 g GAEs/100 g) according to the solvent systems. Francis variety obtained the highest value by using ME 90% solvent followed by Cloud which recorded 25.68 g GAEs/100 g by using WE. Thus, the opportunity to improve the natural extraction of bioactive compounds and phytochemicals using water only and keep away from organic solvents for enhancing health. The current TPC results were in agreement with Walid et al.51. Reduced amounts of TPC were achieved in Wonderful variety by using WE or even EE 70% as 7.07 and 7.46 g GAEs/100 g, respectively. The TPC variability might be partially related to differences in solvents, concentrations, geographical environment and pomegranate varieties2,7,13,52,53. Polyphenols are phytochemicals in plants especially in fruits' pericarp and responsible for sensory evaluation and colour; besides the vital role in vitro and in vivo oxidation.

TFC results for peel pomegranate extracts: TFC was detected in pomegranate peel varieties (Fig. 3b). Francis variety contained the highest value by using ME 90% solvent felled by Cloud which recorded 5 g REs/100 g by using WE. Concentrations of TFC results were comparable to those determined by Ibrahium et al.54. Flavonoids are as well as antioxidants that have effective biological activities against free radicals2,13,32,55.

TTC results for peel pomegranate extracts: The major significant factor for prospective manufacturing application of a plant is TTC results (Fig. 3c). It is observed that TTC result was relatively high in Balegal variety by using ME 70% felled by EE 90% and ME 90% solvents (59.53, 48.60 and 37.20 g TAEs/100 g), respectively. TTC in WE had the lowest tannin content values in Wonderful and Cloud varieties. The date was in agreement with the previous reports56,57, while Madrigal-Carballo et al.58 reported that TTC were the main phenolics in pomegranate peel extracts in the methanolic solvent.

TAC results for peel pomegranate extracts: Anthocyanins are the main sources of natural pigments for the pretty red, purple and violet-blue colours of pomegranate peels moreover can exhibit significant antioxidant activity effects13,26,30,31,59. The result of Fig. 3d shows TAC results in between 0.017-0.133 g/100 g for Wonderful, 0.012-0.083 g/100 g for Francis, 0.013-0.052 g/100 g for Cloud, 0.013-0.022 g/100 g for Balegal extracts. Wonderful variety contained the highest value 0.133 g/100 g by using ME 90% solvent, while Francis recorded the lowest 0.012 g/100 g by using EE 90% solvent, respectively. The richest TAC results were recorded for Wonderful variety60.

Image for - Nutritional Values, Microbial Population and Bioactive Components of Pomegranate (Punica granatum L.) Peel Extracts
Fig. 3(a-d): Bioactive components of the tested pomegranate peel extracts
(a) TPC, (b) TFC, (c) TTC and (d) TAC

Image for - Nutritional Values, Microbial Population and Bioactive Components of Pomegranate (Punica granatum L.) Peel Extracts
Fig. 4: Antioxidant activities of the tested pomegranate peel extracts

Antioxidant activities: An only one method cannot perfectly evaluate the antioxidant potential of food systems, as a result, several methods such as ABTS and DPPH scavenging activity assays were used for that purpose. It is known that ABTS assay is used to evaluate the antioxidant activity of lipid peroxyl and phase radicals and inhibit and decolourize ABTS radicals1,2 with ethanol extract, the ABTS activity of peel varieties varied from 70.53% in Wonderful to 95.05% in Balegal variety (Fig. 4). Those differences can be due to the content and the quality of the phenol components. The antioxidant activity of phenol components can be influenced by the redox properties that act as a reducing agent, hydrogen donor, singlet oxygen quencher with a metallic chelating potential51. DPPH has a maximum absorption at (λmax 517 nm) which is a stable free radical as it donates protons to this radical and therefore there is a reduction in the absorbance and neutralization of the free radical character after changing the colour from purple to yellow2,13,30,61,62. DPPH results were comparatively high-quality compared to the percentage of ascorbic acid as an antioxidant standard. On the other hand, the DPPH assay reported that the Balegal variety had the highest value (93.5%) followed by Cloud (89.4%), Wonderful (79.65%) and Francis (77.97%) (Fig. 4). These results are in agreement with the finding confirmed by Khalil et al.63 who reported that the pomegranate peel extracts had patently higher antioxidant activity than the other parts of pomegranate fruit with no cytotoxicity for HL-60 cells. The ability of pomegranate peel varieties extracts to scavenge ABTS and DPPH radicals was a little similar which could be due to the differences in their solubility, reaction rates and diffusivity in the reaction extracts under actual analytical conditions13,15,26,64. It can be stated that pomegranate peel extracts have high bioactive components and antioxidant activities.

CONCLUSION

Pomegranate peels have been widely used in folk medicine due to their phytochemicals components, antioxidant and pharmacological activities. In the present study, four varieties of pomegranate peels were examined by various extraction solvents and concentrations for their nutritional values, microbial population, bioactive compounds and phytochemicals screening as polyphenol, flavonoid, tannin, anthocyanin contents and antioxidant activities. The data exposed that, the detected antibacterial activity of pomegranate peel extracts was efficient against the pathogenic bacteria and fungi. Besides, methanol solvents achieved the majority abundance of bioactive compounds as compared to the other solvents. Water extract recorded the highest value for flavonoid contents in Cloud variety.

SIGNIFICANCE STATEMENT

This work has had probable applications in the food industry and pharmacology for bioactive compounds of pomegranate peel extracts to exploit them as novel ingredients for designing nutraceuticals in the pharmaceutical industry instead.

ACKNOWLEDGMENTS

The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding this work through research group no (RG-1441-426). Taif University Researchers Supporting Project Number (TURSP-2020/140), Taif University, Taif, Saudi Arabia. Also, the authors thank Prince Sattam Bin Abdulaziz University, Al-Kharj for their scientific contributions.

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