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Antibacterial, antioxidant and tyrosinase-inhibition activities of pomegranate fruit peel methanolic extract
© Fawole et al.; licensee BioMed Central Ltd. 2012
Received: 5 June 2012
Accepted: 3 October 2012
Published: 30 October 2012
This study evaluated, using in vitro assays, the antibacterial, antioxidant, and tyrosinase-inhibition activities of methanolic extracts from peels of seven commercially grown pomegranate cultivars.
Antibacterial activity was tested on Gram-positive (Bacillus subtilis and Staphylococcus aureus) and Gram-negative bacteria (Escherichia coli and Klebsiella pneumonia) using a microdilution method. Several potential antioxidant activities, including radical-scavenging ability (RSA), ferrous ion chelating (FIC) and ferric ion reducing antioxidant power (FRAP), were evaluated. Tyrosinase enzyme inhibition was investigated against monophenolase (tyrosine) and diphenolase (DOPA), with arbutin and kojic acid as positive controls. Furthermore, phenolic contents including total flavonoid content (TFC), gallotannin content (GTC) and total anthocyanin content (TAC) were determined using colourimetric methods. HPLC-ESI/MSn analysis of phenolic composition of methanolic extracts was also performed.
Methanolic peel extracts showed strong broad-spectrum activity against Gram-positive and Gram-negative bacteria, with the minimum inhibitory concentrations (MIC) ranging from 0.2 to 0.78 mg/ml. At the highest concentration tested (1000 μg/ml), radical scavenging activities were significantly higher in Arakta (83.54%), Ganesh (83.56%), and Ruby (83.34%) cultivars (P< 0.05). Dose dependent FIC and FRAP activities were exhibited by all the peel extracts. All extracts also exhibited high inhibition (>50%) against monophenolase and diphenolase activities at the highest screening concentration. The most active peel extract was the Bhagwa cultivar against monophenolase and the Arakta cultivar against diphenolase with IC50 values of 3.66 μg/ml and 15.88 μg/ml, respectively. High amounts of phenolic compounds were found in peel extracts with the highest and lowest total phenolic contents of 295.5 (Ganesh) and 179.3 mg/g dry extract (Molla de Elche), respectively. Catechin, epicatechin, ellagic acid and gallic acid were found in all cultivars, of which ellagic acid was the most abundant comprising of more than 50% of total phenolic compounds detected in each cultivar.
The present study showed that the tested pomegranate peels exhibited strong antibacterial, antioxidant and tyrosinase-inhibition activities. These results suggest that pomegranate fruit peel could be exploited as a potential source of natural antimicrobial and antioxidant agents as well as tyrosinase inhibitors.
Numerous epidemiological studies suggest that diets rich in phytochemicals and antioxidants have protective roles in health and disease. These natural antioxidants might play an important role in combating oxidative stress associated with degenerative diseases such as cancer, cardiovascular diseases, diabetes, Alzheimer’s disease and aging[2, 3]. The antioxidative phytochemicals, especially phenolic compounds, found in vegetables and fruits have received increasing attention for their potential role in the prevention of human diseases[4–8].
Pomegranate (Punica granatum L.; Punicaceae) has gained popularity in recent years due to its multi-functionality and nutritional benefit in the human diet. The fruit is rich in tannins and other biochemicals, particularly phenolics, which have been reported to reduce disease risk[9, 10]. Pomegranate fruit peel constitutes about 50% of the total fruit weight, and it is often discarded as waste. However, the fruit peel contains higher amounts of polyphenol compounds than the juice, and it possesses stronger biological activities[12–14]. Studies have shown that pomegranate peel extract had markedly higher antioxidant capacity than juice extract in scavenging against superoxide anion, hydroxyl and peroxyl radicals and it inhibited CuSO4-induced LDL oxidation. Besides high antioxidant capacity, pomegranate peel extracts have been reported to possess a wide range of biological actions including anti-cancer activity[15–17], antimicrobial activity[18, 19], anti-diarrheal activity, apoptotic and anti-genotoxic properties[21, 22], anti-tyrosinase activity, anti-inflammatory and anti-diabetic activities[24, 25]. Polyphenol compounds such as ellagic tannins, flavonols, anthocyanins, catechin, procyanidins, ellagic acid and gallic acid have been implicated in various pharmacological activities in the fruit peel[24–26]. However, the levels of these compounds in the pomegranate peel may vary among pomegranate cultivars which may result in differing levels of bioactivity.
In South Africa, more than ten pomegranate cultivars are being commercially cultivated. Till date, there is no available information on bioactivities of fruit peels of pomegranate cultivars grown under South African agro-climatic conditions. If fruit peels of pomegranate cultivars show potential to improve human health, their utilisation should be encouraged during fruit processing. In the quest to promote the development of functional foods with health-benefiting properties, we investigated the antibacterial, antioxidant, and tyrosinase-inhibition activities of extracts from peels, using in vitro assays, of seven commercially pomegranate cultivars grown in the Western Cape, South Africa. Furthermore, the total phenolic content including flavonoid, gallotannin and anthocyanin content, and individual phenolics were quantified.
The studies were performed on peels of seven pomegranate fruit cultivars (Arakta, Bhagwa, Ganesh, Herskawitz, Molla de Elche, Ruby, and Wonderful) which are commercially grown in South Africa. Fruit were procured from a commercial pomegranate pack house in Porterville (Western Cape Province). Fruit were harvested between February and May 2010, packed in paperboard cartons and transported in air-conditioned car to the Postharvest Research Laboratory. Immediately on arrival in the laboratory, ten fruits per cultivar were washed and manually peeled. The peels were freeze-dried, ground into powder form, and stored in airtight containers at 7°C in the dark.
Preparation of peel extract
For each cultivar, each finely-powdered peel sample (2 g) was extracted separately with 10 ml of 80% (v/v) methanol (MeOH) and distilled water (aqueous) by sonication for 1 h. The extract was filtered under vacuum through Whatman No.1 filter paper, and the residue was re-extracted further following the same procedure. Extracts were air-dried under a stream of air and first tested in the antibacterial assay to determine which extracts would be worth subjecting to further pharmacological investigations. Only the methanol extract was tested further in other assays, as it recorded highest antibacterial activity.
Microdilution antibacterial assay
The antibacterial activity of peel extract was tested using the microdilution antibacterial assay for the minimum inhibitory concentration (MIC) values as detailed by Fawole et al., except that in the present study the initial concentration (50 mg/ml) of the sample was prepared by dissolving dried extracts in 80% (v/v) methanol. Two Gram-negative bacteria (Escherichia coli ATCC 11775 and Klebsiella pneumonia ATCC 13883) and two Gram-positive bacteria (Bacillus subtilis ATCC 6051 and Staphylococcus aureus ATCC 12600) were used. The extract was serially diluted two-folds with sterile distilled water in a 96-well micro-plate in triplicate for each of the four bacteria used. Streptomycin (0.1 mg/ml) was used as positive control, while water and bacteria-free broth were included as negative controls under the same conditions. Methanol (80%) was also included to check for false antibacterial activity. The final concentration of pomegranate extract ranged from 0.097 – 12.5 mg/ml, reducing the methanol content in the test extract to between 0.19 and 20%, whereas streptomycin was between 0.78 and 100 μg/ml.
where A test is the absorbance of the reaction mixture containing the standard antioxidant or extract, and A blank is the absorbance of the blank test.
Ferrous ion chelating (FIC) assay
where A test is the absorbance of the reaction mixture containing extract or ascorbic acid and A blank is the absorbance of the blank test.
Ferric ion reducing antioxidant power (FRAP) assay
The reducing power of extracts was measured according to the colourimetric method reported by Benzie and Straino with a few modifications. In triplicates, methanolic extract (150 μl) of different concentrations at 10, 100 or 1000 μg/ml was added to 2850 μl of FRAP solution that constituted of 300 mM acetate buffer, 50 ml; 10 mM 2,4,6-tripyridyl-s-triazine (TPTZ), 5 ml; and 20 mM ferric chloride, 5 ml. Following the same procedure, a blank test containing 80% methanol instead of extract was included, while trolox at 10 μg/ml served as the positive control under the same condition. The reaction mixtures were incubated in the dark for 30 min. The reduction of the Fe3+-TPTZ complex to a coloured Fe2+-TPTZ complex by the extract was monitored by measuring the absorbance at 593 nm using a Helios Omega UV–vis spectrophotometer (Thermo Scientific technologies, Madison, USA). The changes in absorbance values of test reaction mixtures from the initial blank reading were considered as FRAP activity.
Tyrosinase inhibition property
where A control is the absorbance of DMSO and A sample is the absorbance of the test reaction mixture containing extract or arbutin. The IC50 values of extracts and arbutin were calculated.
Phenolic content determination
Total phenolic content (TPC)
The total phenolic (TP) content was determined in triplicate by the Folin-Ciocalteu (Folin-C.) colourimetric method as modified by Makkar and calculated as gallic acid equivalents (GAE) per gram DM.
Total flavonoid content (TFC)
Total flavonoid content (TFC) was determined using the method described by Yang et al. and the results were expressed as catechin equivalent (CAE) per gram DM.
Rhodanine assay for gallotannin content (GTC)
Determination of the gallotannin content in peel methanolic extracts was carried out as described by Makkar. Samples (50 μl) were mixed with 150 μl of 0.4 N sulphuric acid followed by 600 μl rhodanine. After 10 min, 200 μl of 0.5 N KOH were added and subsequently distilled water (4 ml) after 2.5 min. The absorbance was read at 520 nm (room temperature) against a blank test that contained aqueous methanol instead of the sample after 15 min incubation. The GTC was calculated from the standard curve (gallic acid) and expressed as gallic acid equivalents (GAE) per gram DM.
Total anthocyanin content (TAC)
A = Absorbance, ε = Cyd-3-glucoside molar absorbance (26,900), MW = anthocyanin molecular weight (449.2), DF = dilution factor, L = cell path-length (1 cm). Final results are expressed as Cyd-3-glucoside equivalent (C3gE) per gram dry matter (μg C3gE/g DM).
HPLC-ESI/MSn analysis of phenolic composition
The LC-MS analysis of phenolics and anthocyanin components in the pomegranate peel extract was performed according to Fischer et al. with slight modification, using a Synapt G2 mass spectrometer UPLCTM system (Waters Corp., Milford, USA) connected to a photo diode array detector and a BEH C18 column (1.7μm particle size, 2.1x100 mm, Waters Corp.). The mobile phases were 5% formic acid in water (v/v) as eluent A and 95% acetonitrile, 5% formic acid (v/v) as eluent B. The flow rate was fixed at 0.2ml/min and the column temperature was set at 40°C. The electrospray ionization (ESI) probe was operated in the positive mode with the capillary voltage of 3 kV; and cone voltage of 15 V. The injection volume was 10 μl and the detection was the diode array detector was set at between 200–600 nm. Individual phenolic compounds were quantified by comparison with a multipoint calibration curve obtained from the corresponding standard (catechin, epicatechin, protocatechuic acid, gallic acid, ellagic acid) from Sigma Aldrich (Germany), while anthocyanins were quantified by an external standard cyanidin 3, 5-diglucoside (Sigma Aldrich, Germany).
All data are presented as mean values (±S.E). Analysis of variance (ANOVA) was performed using SPSS 10.0 for Windows (SPSS Inc. Chicago, USA). Where there was statistical significance (P < 0.05), the means were further separated using Duncan’s Multiple Range Test. Graphical analysis carried out using GraphPad Prism software version 4.03 (GraphPad Software, Inc. San Diego, USA). The IC50 values for the tyrosinase assay were calculated from the logarithmic non-linear regression curve derived from the plotted data using GraphPad Prism software version 4.03 (GraphPad Software, Inc., San Diego, USA).
Results and discussion
Antibacterial activity of fruit peel methanol extracts of pomegranate cultivars cultivated in South Africa
Minimum inhibitory concentration (MIC; mg/ml)
Molla de Elche
Pomegranate peel polyphenols, especially tannins are the major components in the pomegranate peel extract that have been implicated in antimicrobial potential (for example, antiviral, antifungal and antibacterial activities). Vasconcelos studied the antibacterial activity of methanolic peel extracts of pomegranate cultivars against both Gram negative and positive bacteria strains and reported MIC values ranging from 0.25 to 4.0 mg/ml against the test bacteria. The author reported a two-fold MIC value against a Gram positive bacterium (S. aureus) than against a Gram negative bacterium (E. coli). It has been suggested that the antimicrobial activity of tannins may be due to the ability of tannin compounds to precipitate proteins, therefore causing leakage of cell membrane of the microorganism, and aiding cell lysis which ultimately leads to cell death.
Antioxidant activity of fruit peel methanol extracts of seven pomegranate cultivars cultivated in South Africa
FRAP (abs. at 593 nm)
Molla de Elche
The chelating ability of methanolic extracts of pomegranate peel on ferrous ion is presented in Table2. Similar to the RSA results, the ferrous ion chelating (FIC) activity of methanolic peel extract exhibited a linear exponential relationship with extract concentration. Although low FIC activity was exhibited at the lowest concentration (10 μg/ml) assayed, extracts of Molla de Elche, Ruby and Wonderful showed relatively good FIC activity, ranging from 47.24 to 49.65%. At 100 μg/ml the FIC activity of all extracts (except Arakta cultivar) increased above 50%, with Herskawitz, Molla de Elche and Wonderful, showing highest values of 69.97%, 70.57% and 71.02%, respectively. Moreover, FIC activity exhibited by methanolic extracts of most of the investigated at 100 μg/ml were higher than that of the positive control (ascorbic acid at 1000 μg/ml). Dose dependent FIC activity exhibited by all the investigated extracts indicate that the pomegranate fruit peel contains constituents that inhibit oxidation through a mechanism other than radical scavenging activity.
The FRAP assay measures the ability of an antioxidant to reduce ferric (III) to ferrous (II) in a redox-linked colourimetric reaction that involves single electron transfer. The reducing power of a compound serves as a significant indicator of its potential antioxidant activity. All the investigated extracts showed dose-dependent reducing power (Table2). Interestingly, there was no significant difference (p < 0.05) in the reducing capacities among all the cultivars at the highest concentration (1000 μg/ml).
Antioxidant capacity based on both the free radical scavenging and the oxidation–reduction mechanisms may be determined by several methods, although the mechanism of action set in motion by antioxidant compounds is still not clearly understood. Previous studies have shown strong antioxidant activity in pomegranate fruit peel extracts[12, 13]. In comparison with other fruit peels, Okonogi et al. studied the radical scavenging activity on DPPH and ABTS of pomegranate peel extract with other fruit types including rambutan, mangosteen, banana, coconut, dragon fruit, passion fruit as well as long-gong fruit. In the study the highest scavenging activity was reported in pomegranate peel extract. The observed antioxidant property in the peel extract in this study could be attributed to polyphenol compounds such as ellagic tannins, ellagic acid and gallic acid[24, 50]. The results show that pomegranate peel may have great relevance in the prevention and therapies of diseases in which oxidants or free radicals are implicated, hence could serve as an economic source of natural antioxidants.
Tyrosinase inhibition activity
Effective inhibition concentration (EC 50 ) of fruit peel methanol extracts against tyrosinase
IC50 Monophenolase (μg/ml)
IC50 Diphenolase (μg/ml)
Molla de Elche
According to Yoshimura et al., ellagic acid in pomegranate rind showed an inhibitory effect on tyrosinase in vitro and a whitening effect in vivo on UV-induced pigmentation of brownish guinea pig skin. On the contrary, however, Chang argued that some phenolic compounds could be mistakenly classified as tyrosinase inhibitors due to their role as alternative enzyme substrates whose quinoid reaction products absorb in a spectral range different from that of dopachrome. As a result, when the phenolics show a good affinity for the enzyme, dopachrome formation is prevented.
Phenolic compounds analysis
Total phenolics, flavonoid, gallotannin and anthocyanin
Phenolic contents in fruit peel methanol extracts of seven pomegranate cultivars cultivated in South Africa
mg GAE/ g DM
mg CAE /g DM
μg GAE/ g DM
μg C3gE /g DM
Molla de Elche
HPLC-MSn analysis of phenolic composition
Noda et al. reported that cyanidin, pelargonidin, and delphinidin were the principal anthocyanins in pomegranate peel. In the present study, Rutin was found in all cultivars except in Wonderful cultivar, and catechin was the highest in Molla de Elche cultivar with a concentration of 28.85 μg/ml. Overall, the total concentration of the identified phenolic compounds was in the order of Ganesh > Herskawitz > Molla de Elche > Bhagwa > Arakta > Wonderful > Ruby. The presence of these polyphenols in the pomegranate peel may be responsible for the bioactivities observed in the methanol extracts. Phenolic types contained in plants influence antimicrobial activity of the plants. For instance, flavone, quercetin and naringenin were reported showing strong inhibitory activity on the growth of Aspergillus niger, Bacillus subtilis, Candida albicans, Escherichia coli, Micrococcus luteus, Pseudomonas aeruginosa, Saccharomyces cerevisiae, Staphylococcus aureus and Staphylococcus epidermidis, while gallic acid inhibited only P. Aeruginosa whereas no inhibitory activity was exhibited by rutin and catechin on the tested microorganisms. Major chemicals identified through LCMS may not be the only compounds responsible for bioactivity in the pomegranate peel extracts. Other compounds not identified may play a more significant role in the biological activities exhibited by the peel extracts.
This study has shown that the peel of the investigated pomegranate fruit cultivars possess strong antibacterial, antioxidant and anti-tyrosinase activities. Therefore the peel of the pomegranate fruit cultivars, instead of being wasted, could be exploited as a potential source of natural antimicrobial and antioxidant agents, as well as a potential tyrosinase inhibitor. The findings provide scientific basis to promote value-adding of pomegranate fruit peels for pharmaceutical and cosmetic purposes. Further studies on the isolation of active ingredients, determination of cytotoxicity and genotoxicity effects as well as the mode of action of tyrosinase-inhibitory, antibacterial and antioxidant properties in pomegranate peel extracts are warranted.
This work is based upon research supported by the South African Research Chairs Initiative of the Department of Science and Technology and National Research Foundation (Pretoria). The authors are grateful to Citrogold Ltd South Africa and Perishable Products Export Control Board (PPECB) for their financial support. Dr M Stander (Central Analytical Facility, Stellenbosch University) is thanked for her assistance with HPLC-MS analysis. The authors acknowledge the input of the Division of Research Development (Subcommittee B) at Stellenbosch University.
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