Year :
2024
| Month :
June
| Volume :
18
| Issue :
6
| Page :
ZC01 - ZC08
Full Version
Evaluation of Anti-inflammatory, Antioxidant and Antimicrobial Activity of Pomegranate Peel Extract: An In-vitro Study
Published: June 1, 2024 | DOI: https://doi.org/10.7860/JCDR/2024/69878.19463
Pradeep C Dathan, Deepak Nallaswamy, Shanmugam Rajeshkumar, Suja Joseph, Shahin Ismail, Nazia Rashid
1. Research Scholar, Department of Prosthodontics, Saveetha Dental College, Chennai, Tamil Nadu, India.
2. Professor, Department of Prosthodontics, Saveetha Dental College, Chennai, Tamil Nadu, India.
3. Professor, Department of Pharmacology, Saveetha Dental College, Chennai, Tamil Nadu, India.
4. Research Scholar, Department of Prosthodontics, Saveetha Dental College, Chennai, Tamil Nadu, India.
5. Research Scholar, Department of Prosthodontics, Saveetha Dental College, Chennai, Tamil Nadu, India.
6. Research Scholar, Department of Prosthodontics, Saveetha Dental College, Chennai, Tamil Nadu, India.
Correspondence Address :
Dr. Pradeep C Dathan,
Research Scholar, Department of Prosthodontics, Saveetha Dental College, Chennai-600077, Tamil Nadu, India.
E-mail: pdathan70@gmail.com
Abstract 
Introduction: Pomegranate fruit contains biologically active compounds that provide anti-inflammatory properties. Byproducts of pomegranate and punicalagins inhibit the growth of pathogens while enhancing the growth of beneficial bacteria. The beneficial effects of phenolic compounds are exhibited in scavenging free radicals.
Aim: To evaluate the anti-inflammatory, antioxidant, and antimicrobial activity of Pomegranate Peel Extract (PPE).
Materials and Methods: The present in-vitro study was designed and carried out at the Nanobiomedicine Laboratort, Department of Pharmacology, Saveetha Dental College and Hospitals, Chennai, Tamil Nadu, India, from June 2021 to August 2021. The anti-inflammatory activity was evaluated using the Egg Albumin Denaturation assay (EA) and Bovine Serum Albumin Denaturation assay (BSA). The measurement of antioxidant activity was conducted using the 2,2-Diphenyl-1-Picrylhydrazyl (DPPH) assay, Hydrogen peroxide radical scavenging (H2O2) assay, and Ferric Reducing Antioxidant Power (FRAP) assay. Antimicrobial activity was evaluated using the agar well diffusion method. The microorganisms used to evaluate the antimicrobial effect of PPE were S. mutans, S.aureus, E.faecalis, and C.albicans. Results were analysed using independent t-tests, Analysis of Variance (ANOVA) and Tukey’s Honestly Significant Difference (HSD).
Results: Anti-inflammatory activity was observed with high concentrations of 40 and 50 μL in EA (70.06%±0.15, 78.08%±0.21) and BSA (75.50%±3.90, 80.82%±3.38) assays. Pronounced antioxidant activity of PPE was seen with higher concentrations of 40 and 50 μL in DPPH (88.17%±0.69, 92.50%±1.23), H2O2 (78.22%±0.94, 88.99%±1.03), and FRAP (78.43%±1.25, 88.49%±0.67) assays. The antimicrobial activity was highest at 100 μL for S.mutans (38±2.62 mm), S.aureus (36±3.16 mm), E.faecalis (21±1.48 mm), and C.albicans (23±2.36 mm).
Conclusion: The study concluded that PPE has anti-inflammatory, antioxidant and antimicrobial properties and these properties are concentration-dependent.
Keywords
Assays, Flavonoids, Polyphenols, Punica granatum L, Punicalgin
Introduction
There is an increase in demand for phytopharmaceutical products or active molecules contained in Ayurvedic medicines not only in India but also in the Western world. Natural products are considered as an alternate source for new active molecules. The healing power of plants has been used in traditional and Indian systems of medicine for quite a long time (1). In Ayurvedic medicines, extracts of various parts of herbs, namely the bark, roots, leaves, tender stems, fruits, and flowers, were used to cure various chronic ailments. Pomegranate (Punica granatum L) is one such fruit that possesses significant medicinal properties. Many components of the fruit have proven to have effects such as antioxidant, anti-inflammatory, anticarcinogenic, antiatherosclerotic, hypolipidemic, antidiabetic, antiviral, antibacterial, and antifungal activities, and they are attributed to the biological compounds (active molecules) present in the different parts of the fruit (2).
Pomegranate peel contains polyphenols (3),(4),(5) like punicalagin, which is a rich source of antioxidants. Other polyphenols include anthocyanins (delphinidin, cyanidin, and pelargonidin 3-glucosides and 3,5-glucosides) (6),(7),(8), as well as flavonols (9),(10). Lee CJ et al., have reported the anti-inflammatory properties of compounds present in pomegranate fruit. In-vitro studies have reported the anti-inflammatory properties of compounds present in pomegranate. These compounds showed a dose-dependent inhibition on nitric oxide production (11). Fabio M et al., reported that PPE was associated with the highest suppression of proinflammatory cytokine expression in the ex-vivo model (12). It has been reported that pomegranate by-products and punicalagins can inhibit the growth of pathogenic organisms while increasing the growth of beneficial bacteria (13). Phenolic compounds exhibit their beneficial effects through the scavenging action of free radicals. In the recent past, there has been a renewed interest in determining the relevant dietary sources of antioxidant phenolics (14). PPE has received much attention in the field of food preservation. PPE gains relevance in the health sector because of its potential in bone regeneration (15). The anti-inflammatory, antioxidant, and antimicrobial properties of PPE have not been evaluated in a singular research study. In this context, it was decided to prepare PPE and analyse its anti-inflammatory, antioxidant, and antimicrobial activity. The hypothesis is that PPE has significant anti-inflammatory, antioxidant, and antimicrobial activity. The objectives of the present study were to prepare PPE and to evaluate its anti-inflammatory, antioxidant, and antimicrobial activity.
Material and Methods
The present in-vitro study was designed and carried out at the Nanobiomedicine Laboratory, Department of Pharmacology, Saveetha Dental College and Hospitals, Chennai from June 2021 to August 2021. The Ethical Committee of the Institution approved the project (BRULAC/SDCH/SIMATS/IAEC/05-2022/125). The study evaluated the anti-inflammatory, antioxidant, and antimicrobial activity of the freshly prepared PPE.
Study Procedure
Fresh pomegranate fruits of Ganesh variety were soaked in diluted Koparo Clean vegetable and fruit wash (10 mL in 1 litre of water) for 15 minutes, then washed in running water. The pericarp was then separated and air-dried. The dried peel was coarsely powdered using a Multi-mill machine (SS 304). A 2 gm of peel powder was mixed with 100 mL of distilled water using a magnetic stirrer (Remi 5 MLH). The mixture was heated for 15-20 minutes using a heating mantle at 60-80 degrees Celsius. The boiled mixture was filtered using Whatman No. 1 filter paper. Then, the filtered extract was further condensed to 5 mL (Table/Fig 1) (16).
Anti-inflammatory Activity
Egg Albumin denaturation assay (EA): The EA was done as follows (17). A 5 mL solution was prepared using 2.8 mL of freshly manufactured pH-6.3 phosphate-buffered saline and 0.2 mL of chicken EA extract. The PPE of different concentrations, namely 10 μL, 20 μL, 30 μL, 40 μL, 50 μL (n=10), were prepared. Diclofenac sodium was used as the positive control. The mixes were then heated in a water bath for 15 minutes at 37°C. The samples were allowed to cool to ambient temperature, and the absorbance at 660 nm was measured.
Bovine Serum Albumin denaturation assay (BSA): The anti-inflammatory activity of PPE was tested using the convention proposed by Mizushima and Kabayashi with modifications (Pratik D et al., 2019) (18). A 0.05 mL of PPE of various concentrations (10 μL, 20 μL, 30 μL, 40 μL, 50 μL) was added to 0.45 mL of BSA (1% aqueous solution), and the pH of the mixture was adjusted to 6.3 using 1N hydrochloric acid. These samples were incubated at room temperature for 20 minutes and then heated at 55°C for 30 minutes in a water bath. The temperature of the samples was then reduced, and the absorbance was measured by spectrophotometry at 660 nm. Diclofenac Sodium was used as the standard, and Dimethyl Sulphoxide was utilised as a control.
Percentage of protein denaturation was determined by the following equation (18):
Inhibition=(Absorbance of control - Absorbance of sample/Absorbance of control)×100
Antioxidant Activity
Antioxidant activity of PPE was tested using three methods, of which two- DPPH and H2O2- were based on the free-radical scavenging capacity of PPE. The third one, FRAP was based on measuring the iron-reducing capacity.
DPPH assay: The assay utilised a commercially available free radical DPPH, which is soluble in methanol (Brand-Williams W et al., 1995) (19), and the antioxidant activity was measured by the decrease in absorbance at 515 nm. PPE of various concentrations (10 μL, 20 μL, 30 μL, 40 μL, 50 μL) was prepared and mixed with 1 mL of 0.1 mM DPPH in methanol and 450 μL of 50 mM Tris HCl buffer (pH 7.4) and incubated for 30 minutes. Later, the reduction in the quantity of DPPH free radicals was assessed based on the absorbance at 515 nm. Butylated hydroxytoluene was employed as a control. The percentage of inhibition was determined by the above mentioned equation.
H2O2 Assay
This was performed as described by Halliwell B with minor modifications (20). All the solutions were prepared freshly. A 1.0 mL of the reaction mixture contained the following: 100 μL of 28 mM of 2-deoxy-2-ribose (dissolved in phosphate buffer 7.4), 500 μL solution of various concentrations of PPE (10 μL, 20 μL, 30 μL, 40 μL, 50 μL), 200 μL of 200 μM FeCl3 and 1.04 mM Ethylenediamine Tetraacetic Acid (EDTA) (1:1 v/v), 100 μL H2O2 (1.0 mM) and 100 μL ascorbic acid (1.0 mM). After incubating the reactant mixture for a period of one hour at 37°C, the extent of deoxyribose degradation was measured by the Thiobarbituric Acid reaction. The absorbance was measured at around 532 nm against the blank solution. Vitamin E was used as the positive control.
FRAP assay: All the reagents were procured from Merck (Germany) company (21). A 3.6 mL of FRAP solution was added to 0.4 mL of distilled water and incubated at 37°C for five minutes. This solution was then mixed with various concentrations of PPE (10 μL, 20 μL, 30 μL, 40 μL, 50 μL) and incubated at 37°C for 10 minutes. The absorbance of the reaction mixture was measured at 593 nm. A calibration curve was constructed based on five concentrations of FeSO4·7H2O (0.1, 0.4, 0.8, 1, 1.12, 1.5 mM) and the absorbance values were measured for sample solutions.
Antibacterial Activity
The antibacterial activity of PPE was assessed using the agar well diffusion method against pathogenic bacteria, including Streptococcus mutans, Staphylococcus aureus, Enterococcus faecalis, and Candida albicans. Mueller Hinton agar was prepared and sterilised for 45 minutes under 120 lbs pressure. The medium was poured into sterilised plates and allowed to solidify. Wells were cut using a well cutter, and the test organisms were swabbed onto the plates. PPE with different concentrations of 25 μL, 50 μL, and 100 μL were loaded into the wells, and the plates were incubated for 24 hours at 37°C. After the incubation period, the zone of inhibition was measured and compared with the standard antibiotic Amoxicillin 100 mg/mL (Table/Fig 2).
Antifungal Activity
The antifungal activity of PPE was evaluated using the agar well diffusion method against C.albicans. Sabouraud’s dextrose agar was used to prepare the medium, which was sterilised for 45 minutes under 120 lbs of pressure. Wells were cut using a well cutter and then inoculated with the test organism C.albicans. PPE was added in different concentrations of 25 μL, 50 μL, and 100 μL. The plates were incubated for 48-72 hours at a temperature of 28°C. The zone of inhibition was measured and compared with the standard antifungal agent Fluconazole (Table/Fig 2).
Statistical Analysis
The results were tabulated and subjected to statistical analysis using Statistical Package for Social Sciences (SPSS) version 23.0 The independent t-test, ANOVA, and Tukey’s HSD were used for statistical analysis. A p-value less than 0.05 were considered significant.
Results
Anti-inflammatory Activity
In EA, the inhibition caused by PPE with a 10 μL concentration was (51.04%±0.145), and for the standard, it was 55.08%±0.252 (10 μ μL). The difference was statistically significant (p<0.001) (Table/Fig 3),(Table/Fig 4). For BSA, the percentage of inhibition was significantly lower for PPE when compared to the standard at 10 μL, 20 μL, and 30 μL (p<0.001) (Table/Fig 3),(Table/Fig 4).
There were significant differences between the groups of different concentrations of PPE in both EA and BSA (p<0.05) (Table/Fig 5). On pair-wise comparison, a significant difference was found between 10 μL and 40 μL (p=0.002) and 10 μL and 50 μL (p=0.001) in EA (Table/Fig 6). Similarly, in BSA, a significant difference was found between 10 μL and 50 μL (p=0.028) (Table/Fig 7).
Antioxidant Activity
The antioxidant activity observed for DPPH ranged between 65.44% to 92.50% in the experimental group and 66.25% to 93.18% with the standard. For H2O2, the values ranged from 51.94% to 88.99% for the experimental group and 51.06% to 89.65% for the standard. In the case of FRAP, the values ranged from 53.09% to 88.49% and 51.10% to 88.81%, respectively. (Table/Fig 8) Significant differences were found between PPE concentrations of 10 μL, 20 μL, and 30 μL with the standard for all three assays (p<0.05) (Table/Fig 9).
There were significant differences between the groups of different concentrations of PPE in both DPPH, H2O2, and FRAP (p<0.05) (Table/Fig 10). On pair-wise comparison, significant differences were found between 10 μL and 50 μL (p=0.01) and 20 μL and 50 μL (p=0.028) in DPPH (Table/Fig 11). However, in H2O2 and FRAP, significant differences were found between 10 μL and 50 μL (p<0.05) (Table/Fig 12),(Table/Fig 13).
Antibacterial Activity
The antibacterial activity was assessed against S.mutans, S.aureus, and E.faecalis using three different concentrations of PPE. The zone of inhibition was measured, and the highest value was observed for Streptococcus mutans (38±2.62 mm) at a concentration of 100 μL. Similarly, Staphylococcus aureus exhibited a zone of inhibition of 36±3.16 mm at a concentration of 100 μL. When assessing the antifungal activity against C. albicans, a zone of inhibition of 23±2.36 mm was observed at a concentration of 100 μL (Table/Fig 14).
Upon comparison of the antibacterial and antifungal activity of different concentrations of PPE with the standard used, a statistically significant difference was found at all concentrations against S. mutans, S.aureus, E.faecalis, and C.albicans (p<0.01), except for PPE at 100 μL for S.mutans (p=0.995) (Table/Fig 15). There were significant differences between the groups of different concentrations of PPE (p<0.05) (Table/Fig 16). On pair-wise comparison, significant differences were found between all three concentrations used for S.mutans and E.faecalis (p<0.01). However, for S.aureus, the difference between only 25 μL and 100 μL was statistically significant (p=0.003) (Table/Fig 17).
Discussion
A number of biologically active compounds present in pomegranate provide anti-inflammatory, antioxidant, and antibacterial properties (14). Parts of the fruit, especially the peel, are abundant in biologically active compounds; therefore, peel extract was selected for this study. The study has proven that PPE has definite anti-inflammatory, antioxidant, and antibacterial activity.
Anti-inflammatory Activity
Inflammation is caused by the denaturation of proteins, and PPE can inhibit that process, thereby reducing inflammation. The anti-inflammatory property was measured by EA and BSA using different concentrations of PPE. At higher concentrations of PPE, the anti-inflammatory activity was similar to that of the standard, with no statistically significant difference (p>0.05). The results indicate that both the experimental and standard groups have similar anti-inflammatory potential. At lower concentrations, the anti-inflammatory potential was slightly inferior. It can be stated that with the increase in concentration, the anti-inflammatory property also enhances. Based on the present observations, PPE can be considered a successful substitute for popularly used anti-inflammatory drugs.
The polyphenols contained in PPE are converted to urolithins in the gut by the activity of microbiota. Urolithins have shown significant anti-inflammatory activity (22). The individually fractionated biomolecules of pomegranate influence the expression of inflammatory cell signalling protein in cancer cells (23). Pomegranate juice, tannins, and punicalagin reduce the expression of Cyclooxygenase-2 (COX-2), responsible for the production of prostanoids that induce inflammation (24). Ellagic acid found in PPE can control intestinal inflammation by downregulating inflammation-mediating compounds and blocking cell signalling pathways (25). The polyphenol-rich pomegranate fruit extract or compounds derived from it can be used for the treatment of inflammatory diseases, possibly by suppressing basophils and mast cell activation (26).
Inflammation caused by free radicals can be eliminated by PPE. Due to the antimicrobial properties imparted by the phytochemicals of pomegranate, inflammation caused by microbes can also be eliminated. The phytochemicals present in pomegranate have multiple activities and can affect more than one inflammatory factor, resulting in enhanced healing (27),(28),(29),(30),(31). The outcomes of various researchers, as referenced earlier, align with the findings of the present study. The concentration of active components within PPE plays a crucial role in augmenting its anti-inflammatory properties.
Antioxidant Activity
The antioxidant property of all concentrations of PPE and the standard was similar across the three assays. When comparing the concentrations of 40 μL and 50 μL, there was no significant difference between the test material and the standard. This establishes the fact that at higher concentrations, the antioxidant activity of PPE was similar to that of the standard, indicating that the antioxidant activity is dose-dependent. The presence of punicalagin and hydrolysable tannins in pomegranate extract provides very high antioxidant activity compared to the antioxidant properties of green tea and red wine, with the potency of PPE being three times higher than the others (32). Pomegranate peel is a reservoir of biologically active compounds that provide excellent antioxidant properties (33). The presence of phenolic compounds is influenced by the extraction methods and cultivar, and the activity increased with the concentration of PPE (34).
Lamiae Benchagra compared PPE and extracts of arils and reported a higher concentration of phenolic compounds in peels than in arils. DPPH, FRAP, and H2O2 assays revealed that the antioxidant activity was dose-dependent, with higher concentrations giving higher antioxidant activity (35). Shalini M et al., made extracts of the Ganesh variety of pomegranate peel in water, methanol, and ethanol, as well as combinations with water. The antioxidant activity and total phenolic content were evaluated. The 70% ethanol: 30% water and 100% aqueous extract had higher phenolic content and showed higher antioxidant activity (36). Singh RP et al., prepared methanol, ethyl acetate, and water extracts of pomegranate seeds and peels. The methanol extract of pomegranate peel showed the highest antioxidant activity among all the extracts (37). The dried methanolic extract of pomegranate peel protected hepatic cells from the toxic effects of Carbon Tetrachloride, mainly due to the antioxidant function of the biologically active compounds found in the peel (38).
The findings of the large number of research workers mentioned above and the results obtained from the present study are comparable. PPE contains effective antioxidant elements which have established therapeutic potential. The concentration of the active components contained in PPE plays a significant role in enhancing the antioxidant property.
Antimicrobial Effect
When the antimicrobial efficacy was assessed, the maximum antibacterial effect of PPE was against staphylococcus aureus, followed by streptococcus mutans, and E.Faecalis. For all the organisms tested, the zone of inhibition increased with the increase in concentration of PPE. The methanolic extract of pomegranate showed an antibacterial effect. The antibacterial activity was attributed to the phenolic structure contained in the extract, specifically Gallic acid and other phenolics [39,40]. Ether, chloroform, methanol, and water extracts of Punica granatum had an antibacterial effect, with the methanolic extract being the most effective (41). Cruz-Valenzuela MR et al., reported that the peel extract showed antimicrobial activity against bacterial and fungal cultures, specifically against Staphylococcus and Aspergillus (42). The mechanism behind the antimicrobial activity has been reported by various investigators. The phytoneutrients are toxic to the bacterial cell wall and form complexes with enzyme cofactors and sulfhydryl groups of proteins. This alters the cell membrane permeability and disturbs the respiratory chain (43).
Antifungal Activity
The PPE showed definite antifungal activity, which is due to the presence of polyphenols. These polyphenols cause precipitation of cell membrane proteins, resulting in cell leakage. This cell leakage leads to alterations in the composition of cytoplasm and cell membrane, inhibiting fungal growth (44).
Both the crude extract and the isolated punicalagin compound from pomegranate demonstrated a significant inhibitory effect against both Trichophyton and Microsporum genera. The isolated punicalagin compound exhibited a similar minimum inhibitory concentration value as the crude extract (45). PPE, rich in gallic acid, strongly inhibited the growth of fungus and reduced its drug resistance. This extract is a promising natural antifungal agent for clinical use (46). The PPE exhibits high concentrations of polyphenols, specifically punicalagin and ellagic acid, attributing to its antifungal properties. The peel demonstrates effectiveness against a wide range of fungi, encompassing both pathogenic and opportunistic pathogens (47). The antimicrobial activity observed in the current study closely resembles that reported in previous research.
Limitation(s)
The specific biologically active component responsible for the anti-inflammatory, antioxidant, and antibacterial activity was not ascertained.
Conclusion
The PPE has a definite anti-inflammatory, antioxidant, and antibacterial effect and which depends on the concentration of the active ingredients contained in the PPE. PPE can be used as a therapeutic agent where an anti-inflammatory, antioxidant, and antibacterial effect is required. In the Indian context, natural products like pomegranate can be considered preferentially to improve affordability and accessibility among economically weaker sections of society without sacrificing therapeutic quality.
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DOI: 10.7860/JCDR/2024/69878.19463
Date of Submission: Feb 03, 2024
Date of Peer Review: Feb 20, 2024
Date of Acceptance: Apr 16, 2024
Date of Publishing: Jun 01, 2024
AUTHOR DECLARATION:
• Financial or Other Competing Interests: None
• Was Ethics Committee Approval obtained for this study? Yes
• Was informed consent obtained from the subjects involved in the study? NA
• For any images presented appropriate consent has been obtained from the subjects. NA
PLAGIARISM CHECKING METHODS:
• Plagiarism X-checker: Feb 03, 2024
• Manual Googling: Apr 10, 2024
• iThenticate Software: Apr 13, 2024 (20%)
ETYMOLOGY: Author Origin
EMENDATIONS: 9
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