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Effect of drying on the bioactive compounds, antioxidant, antibacterial and antityrosinase activities of pomegranate peel
© The Author(s). 2016
Received: 23 December 2015
Accepted: 18 May 2016
Published: 26 May 2016
The use of pomegranate peel is highly associated with its rich phenolic concentration. Series of drying methods are recommended since bioactive compounds are highly sensitive to thermal degradation. The study was conducted to evaluate the effects of drying on the bioactive compounds, antioxidant as well as antibacterial and antityrosinase activities of pomegranate peel.
Dried pomegranate peels with the initial moisture content of 70.30 % wet basis were prepared by freeze and oven drying at 40, 50 and 60 °C. Difference in CIE-LAB, chroma (C*) and hue angle (h°) were determined using colorimeter. Individual polyphenol retention was determined using LC-MS and LC-MSE while total phenolics concentration (TPC), total flavonoid concentration (TFC), total tannins concentration (TTC) and vitamin C concentration were measured using colorimetric methods. The antioxidant activity was measured by radical scavenging activity (RSA) and ferric reducing antioxidant power (FRAP). Furthermore, the antibacterial activity of methanolic peel extracts were tested on Gram negative (Escherichia coli and Klebsiella pneumonia) and Gram positive bacteria (Staphylococcus aureus and Bacillus subtilis) using the in vitro microdilution assays. Tyrosinase enzyme inhibition was investigated against monophenolase (tyrosine) and diphenolase (DOPA), with arbutin as positive controls.
Oven drying at 60 °C resulted in high punicalin concentration (888.04 ± 141.03 mg CE/kg dried matter) along with poor red coloration (high hue angle). Freeze dried peel contained higher catechin concentration (674.51 mg/kg drying matter) + catechin and –epicatechin (70.56 mg/kg drying matter) compared to oven dried peel. Furthermore, freeze dried peel had the highest total phenolic, tannin and flavonoid concentrations compared to oven dried peel over the temperature range studied. High concentration of vitamin C (31.19 μg AAE/g dried matter) was observed in the oven dried (40 °C) pomegranate peel. Drying at 50 °C showed the highest inhibitory activity with the MIC values of 0.10 mg/ml against Gram positive (Staphylococcus aureus and Bacillus subtili. Likewise, the extracts dried at 50 °C showed potent inhibitory activity concentration (22.95 mg/ml) against monophenolase. Principal component analysis showed that the peel colour characteristics and bioactive compounds isolated the investigated drying method.
The freeze and oven dried peel extracts exhibited a significant antibacterial and antioxidant activities. The freeze drying method had higher total phenolic, tannin and flavonoid concentration therefore can be explored as a feasible method for processing pomegranate peel to ensure retention of the maximum amount of their naturally occurring bioactive compounds.
Not relevant for this study.
Pomegranate (Punica granatum L.) fruit is an important commercial crop cultivated in different parts of the world. The adaptability and health benefits are some of the characteristics responsible for its wide scale cultivation. About 50 % of the total fruit weight corresponds to the peel, which is an important source of bioactive compounds . Meanwhile the edible part of pomegranate fruit consists of 40 % arils and 10 % seeds . Pomegranate peel is a waste from juice processing. Several studies have confirmed that pomegranate peel is a rich source of bioactive compounds including ellagitannins, catechin, rutin and epicatechin among others [1, 3–5]. These bioactive compounds possess different biological activities such as scavenging reactive oxygen species (ROS), inhibiting oxidation and microbial growth and reducing the risk of chronic disease such as cancers and cardiovascular disorders [1, 4, 6].
However, the concentrations of bioactive compounds widely fluctuate among cultivars, environmental conditions, fruit maturity status, storage and postharvest treatments which may affect fruit quality and health beneficial compounds [7–11]. In the past, pomegranates was commonly used in conventional medicine for eliminating parasites and vermifuge, and to treat and cure apthae, ulcers, diarrhoea, acidosis, dysentery, haemorrhage, microbial infections and respiratory pathologies . According to Gil et al. , pomegranate peel has the higher antioxidant activity than the pith and juice.
Drying is an ancient process used to preserve and prolong shelflife of various food products . The main aim of drying food products is to remove water in the solid to a level at which microbial spoilage and deterioration resulting from chemical reactions is significantly reduced [14–17]. This enables the product to be stored for longer periods since the activity of microorganisms and enzymes is inhibited through drying [18, 19]. Generally, drying involves the application of thermal energy which cause water to evaporate into the vapour phase. However, drying results in structural, chemical and phytochemical changes that can affect quality properties such as texture, colour and nutritional values [20–22]. Several drying techniques used for various products include air, oven and freeze drying. Generally, air-drying and oven drying are favoured due to processing cost and efficiency . However, air drying has drawbacks of both long drying time required and poor quality [24, 25]. By far, freeze drying is regarded as the better method for moisture removal, with final products of the highest quality compared with air-drying [13, 26].
Pomegranate ‘Wonderful’ is the most widely grown and consumed pomegranate cultivar globally  and during the past 10 years, South Africa has seen tremendous increase in commercial production of the registered cultivar, accounting for over 1000 ha of total planted area and 56 % of total production . Pomegranate peel has been known for many years for its health benefit, including antibacterial activity. More recently, research indicated that pomegranate peel extracts also inhibit tyrosinase activity  an enzyme that induces the production of melanin which leads to hyperpigmentation of the skin.
The high level of bioactive compounds in the peel as well as the reported health benefits to date make these desirable by-products as functional ingredients in food, nutraceuticals and pharmaceutics [4, 5, 29]. Previous researches have been limited to the characterization of phenolic compounds of the pomegranate peel extracts and the evaluation of its biological activities. However, the information on the effect of drying on the pharmacological properties is limited. Therefore, the aim of this study was to investigate the concentrations of polyphenols compounds, antioxidant activity and the in vitro pharmacological properties of pomegranate peel using freeze and oven drying (at various temperature range).
Pomegranate ‘Wonderful’ fruit (a commercial registered cultivar in South Africa) were sourced during commercial harvest from Sonlia packhouse (33°34′851″S, 19°00′360″E) in Western Cape, South Africa. The ‘Wonderful’ is the only late cultivar grown in South Africa, harvested between April and May of every year. The fruit was further verified by Mr. Neil Maree of the Pomegranate Association of South African (POMASA) and a voucher specimen retained with as PUC: W1153. Fruit were transported to the Postharvest Technology Laboratory at Stellenbosch University. Fruit of the same size shape, colour and without any physical defects were randomly selected. Fresh pomegranate peel was cut in the dimension of 20 ± 0.5 mm (length), 20 ± 0.5 mm (width) and 5 ± 0.5 mm (thickness) were used. Before drying, the peels were stored at −80 °C until use. Moisture content was measured using a modified AOAC method 925.45  with slight modifications by drying the peel using the oven at 105 ± 0.5 °C for 24 h. The oven was kept functional for an hour to equilibrate the oven temperature before drying. The accuracy of the oven temperature was monitored using thermometer (Thermco®, Germany). All the drying tests were run two times in triplicates at each temperature and averages were reported.
Three different temperature levels (40, 50 and 60 °C) were used and the oven dryer (Model nr. 072160, Prolab Instruments, Sep Sci., South Africa) was operated at an air velocity of 1.0 m/s, parallel to the drying surface of the sample. Weight change was recorded by a digital balance (ML3002.E, Mettler Toledo, Switzerland) at an hourly interval during drying. Peels were dried until equilibrium (no weight change) was reached.
Residual moisture using freeze and oven drying methods
Drying time (h)
Residual moisture (kg water/kg dry matter)
0.087 ± 0.002b
0.093 ± 0.002a
0.094 ± 0.002a
0.096 ± 0.004a
where ∆L*, ∆a* and ∆b* are the differences between the colour of the fresh and dried sample.
Dried peel was ground to a fine powder using a miller (Model A11, IKA, Germany) and screened through a plastic mesh sieve, with a mesh size of 1.4 mm particle size (Vanguard, India). Dried pomegranate peel (2 g) from each drying methods were extracted separately with 10 ml of 80 % (w/v) methanol using sonication for approximately 1 h . The extracts were separately filtered with Whatman no.1 filter paper and residues were re-extracted following the same procedure. The extracts were pooled before drying under stream of air.
Determination of individual phenolic acids and flavonoids concentration
LC-MS and LC-MSE analyses were conducted on a Waters Synapt G2 quadrupole time-of-flight mass spectrometer system (Milford, MA, USA). The instrument was connected to a Waters Acquity ultra-performance liquid chromatograph (UPLC) and Acquity photo diode array (PDA) detector. Ionisation was achieved with an electrospray source using a cone voltage of 15 V and capillary voltage of 2.5 kV using negative mode for analysis of phenolic compounds. Nitrogen was used as the desolvation gas, at a flow rate of 650 L/h and desolvation temperature of 275 °C. The separations were carried on a waters UPLC BEH C18 column (2.1 × 50 mm, 1.7 μm particle size), with injection volume of 3 μl at flow rate of 0.4 ml/min. The gradient for the analysis of phenolic compounds started with 100 % using 0.1 % (v/v) formic acid (solvent A) and kept at 100 % for 0.5 min, followed by a linear gradient to 22 % acetonitrile (solvent B) over 2.5 min, 44 % solvent B over 4 min and finally to 100 % solvent B over 5 min. The column was subjected to 100 % solvent B for an extra 2 min. The column was then re-equilibrated over 1 min to yield a total run time of 15 min. Reference standards (Sigma-Aldrich, South Africa) of phenolic acids and flavonoids were used for the quantification of individual compounds in pomegranate peel extracts.
Determination of total phenolic concentration
Total phenolic concentration (TPC) was measured using the Folin-Ciocalteu (Folin-C) method as described by  with slight modification . Diluted peel extracts (50 μl) was mixed with 450 μl of 50 % methanol followed by the addition of 500 μl Folin-C and then sodium carbonate (2 %) solution after 2 min. The mixture was vortexed and absorbance read at 725 nm using a UV-visible spectrophotometer (Thermo Scientific Technologies, Madison, Wisconsin). Gallic acid standard curve (0.08− 0.32 mg/ml) was used and TPC was expressed as milligram gallic acid equivalent per kilogram peel extracts (mg GAE/kg DM).
Determination of total tannin concentration
Results were expressed as milligram gallic acid equivalent per kilogram peel extracts (mg GAE/kg DM).
Determination of total flavonoid concentration
Total flavonoid concentration was measured spectrophotometrically as described by Yang et al. . PJ (1.0 g) was extracted with 50 % methanol (49 ml) and vortexed for 30 s. The mixture was sonicated in an ultrasonic bath for 10 min and centrifuged at 4000 g for 12 min at 4 °C. Distilled water (1.2 ml) was added to 250 μl of extracted peel extracts and then followed by 75 μl of 5 % sodium nitrite. After 5 min, freshly prepared 10 % aluminium chloride (150 μl) was added to the mixture, followed by the addition of 500 μl sodium hydroxide after a another 5 min, and 775 μl distilled water bringing the final volume to 3 ml. The mixture was vortexed and absorbance was immediately read using spectrophotometer at 510 nm. Catechin (0.01–0.5 mg/ml) was used for the standard curve. The results were expressed as catechin equivalent per kilograms peel extracts (mg CE/kg DM).
Radical scavenging activity (RSA)
The ability of peel extract to scavenge 2, 2-diphenyl-1-picryl hydrazyl (DPPH) radical was measured following the procedure described by Karioti et al.  with slight modifications . Peel extract (15 μl) was mixed with 735 μl methanol and 0.1 mM solution of DPPH (750 μl) dissolved in methanol. The mixture was incubated for 30 min in the dark at room temperature before measuring the absorbance at 517 nm using a UV-visible spectrophotometer (Thermo Scientific Technologies, Madison, Wisconsin). The RSA was determined by ascorbic acid standard curve (0–1500 μM). The results were presented as millimolar ascorbic acid (AA) equivalent per gram of peel extracts (mM AAE/g DM).
Ferric reducing antioxidant power
Ferric reducing antioxidant power assay was performed according to the method of Benzie and Strain . FRAP solutions contained 25 ml acetate buffer (300 mM acetate buffer, pH 3.6), 2.5 ml (10 mM of TPTZ solution), 2.5 ml (20 mM of FeCl3 solution). Ten millilitre of aqueous methanol (50 %) was added to peel extract (1 ml), sonicated for 10 min in cold water and centrifuged for 5 min at 4 °C. PJ (150 μl) was mixed with 2850 μl FRAP and the absorbance was read at 593 nm after 30 min incubation using a UV-visible spectrophotometer. Trolox (0–1.5 mM) was used for calibration curve, and results were expressed as trolox (μM) equivalents per millilitre pomegranate juice (μM TE/g DM).
Determination of ascorbic acid concentration
Ascorbic acid was determined according to Klein and Perry  with slight modifications . Briefly, peel extract (1.0 g) was mixed with 50 ml of 1 % metaphosphoric acid followed by sonication on ice for 4 min and centrifugation at 4000 g for 12 min. Supernatant (1.0 ml) was pipetted into a tube and mixed with 9 ml of 2, 6 dichlorophenolindophenol dye (0.0025 %). The mixture was incubated in the dark for 10 min before absorbance was measured at 515 nm. Calibration curve of authentic L-ascorbic acid (0.01–0.1 μg/ml) was used to calculate ascorbic acid concentration. Results were expressed as ascorbic acid equivalents per millilitre crude juice (μg AAE/g DM).
Antibacterial activity of pomegranate peel was determined following microdilution assay for the minimum inhibitory concentration values . Four bacterial strains used comprised 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). All the bacteria were grown in sterile MH broth. The stock solutions of the peel extracts were dissolved in methanol to make 50.0 mg/ml. Under aseptic conditions, 100 μl of sterile water were added in a 96-well micro plate followed by 100 μl peel extracts as well as bacterial culture and serially diluted (two-fold). Similarly, two fold serial dilution of streptomycin (0.1 mg/ml) was used as positive control against each bacterium. Bacteria-free broth, methanol solvent (100 %) and sterile water were included as negative controls. The final concentration of peel extract ranged from 0.097 to 12.5 mg/ml, whereas streptomycin was between (0.097–12.5 mg/ml). Plates were incubated for 18 h at 37 °C. After incubation, bacterial growth in the plate was indicated by adding 40 μl of p-iodonitrotetrazolium chloride (Sigma-Aldrich, Germany) after incubation. Bacterial growth was indicated by pink colour, while clear wells indicated inhibition. The results were recorded in terms of the minimal inhibitory concentration which is regarded as the lowest concentration of the extract without bacterial growth. The assay was measured in triplicates.
Mushroom tyrosinase inhibition assay
Statistical analyses were carried out using statistical software (STATISTICA, Vers. 12.0, StatSoft Inc., USA). Data was subjected to analysis of variance (ANOVA) and means were separated by least significant difference (LSD; P = 0.05) according to Duncan’s multiple range test. GraphPad Prism software version 4.03 (GraphPad Software, Inc., San Diego, USA) was used for graphical presentations. Principal component analysis (PCA) was carried out using XLSTAT software version 2012.04.1 (Addinsoft, France). Triplicate measurements were carried out and the values are reported as mean ± standard error.
Results and discussion
Drying time and residual moisture content
The drying time required to achieve a final moisture concentration of the peel were, 22, 17, 16 and 12 h for 40, 50 °C, freeze drier and 60 °C, respectively (Table 1). Drying time resulted in the residual moisture concentration which varied from 0.087 to 0.096 kg water/kg dry matter. Overall, freeze dried peel had the lowest residual moisture whereas oven dried peels did not vary in all temperature range.
Pomegranate peel colour attributes after drying
51.01 ± 1.67b
28.85 ± 1.70a
35.14 ± 1.60a
34.61 ± 2.05b
61.46 ± 1.59a
23.33 ± 1.28b
29.99 ± 0.86b
38.85 ± 2.18ab
17.77 ± 1.07b
41.51 ± 1.09c
24.33 ± 1.01b
33.13 ± 0.77a
42.32 ± 1.70a
18.72 ± 1.14ab
39.29 ± 1.37c
25.24 ± 0.88b
33.25 ± 0.78a
39.82 ± 1.76ab
23.10 ± 2.42a
42.04 ± 0.92c
25.24 ± 1.16b
35.08 ± 0.66a
43.78 ± 1.90a
16.82 ± 2.00b
Individual phenolic acid and flavonoid compound
Individual phenolic and flavonoid concentration in fresh and dried pomegranate peel
Punicalin (mg CE/kg DM)
+Catechin (mg/kg DM)
708.38 ± 48.86b
4666.03 ± 311.70a
674.51 ± 21.30a
70.56 ± 0.22a
16.45 ± 1.65a
768.11 ± 1.67b
2135.00 ± 0.00c
377.26 ± 22.05c
28.93 ± 1.55c
5.07 ± 0.02b
672.98 ± 26.93b
0.45 ± 0.02
340.64 ± 21.06c
31.95 ± 3.37bc
4.59 ± 0.54b
888.04 ± 57.57a
3401.36 ± 0.00b
0.57 ± 0.52
443.41 ± 0.30b
34.74 ± 0.11b
1.77 ± 0.54c
Total phenolic (TPC), total tannins (TTC) and flavonoid concentration (TFC)
Radical scavenging activity (RSA) and ferric reducing antioxidant power (FRAP) and vitamin C concentration
The reducing power of pomegranate peel was determined using ferric reducing antioxidant power method which measures reduction of Fe+3 to Fe+2. In this study, antioxidant activity (FRAP) of pomegranate peel did not vary significantly (P > 0.05) between the drying methods. The reducing power was in the order of 40 °C > 50 °C, 60 °C > freeze-dried (Fig. 2b). It can be observed that freeze and oven drying at various temperatures affected vitamin C (P < 0.05), thus a considerable higher vitamin C in samples dried at 40 °C was observed (Fig. 2c). However, no significant difference was observed between freeze and oven-dried (at 50 and 60 °C) peel. According to Marques and Freire , the small losses in vitamin C in freeze dried product are attributed to low temperature and to the use of vacuum in the process. Researchers observed loss of vitamin C during air-drying of pomegranate peel . Our findings are in agreement with those of Vega-Gàlvez et al.  who reported loss of vitamin C during oven drying at temperatures between 50 and 90 °C in red pepper. Miranda et al.  reported the loss of 70 % of vitamin C after drying in aloe vera gel and the authors concluded that this may be the result of irreversible oxidation during drying with hot air. Therefore, lower vitamin C concentration observed in this study may be as a result of irreversible oxidation during drying. Vitamin C is a thermo-sensitive compound, therefore lower concentration was likely due to elevated processing temperature [67, 68] and period of exposure required to dry the sample at 50 and 60 °C.
Antibacterial activity (MIC, mg/ml) of dried pomegranate peel extracts using two different drying methods
Tyrosinase inhibitory activity
Effective inhibition concentration (EC50) of fresh and dried fruit peel extracts against tyrosinase
107.73 ± 10.08a
86.93 ± 15.23ab
45.07 ± 6.05b
119.79 ± 20.23a
22.95 ± 1.53c
74.05 ± 10.27ab
64.27 ± 10.35b
62.09 ± 2.98b
44.00 ± 5.56b
14.99 ± 2.52c
Principal component analysis
Factor loadings, eigenvalue, cumulative variance (%) and score for the first two principal (F1–F2) components based on pomegranate peel from two different drying methods
Hue angle (h°)
The results of the study showed that drying processes have an impact on the bioactive compounds of pomegranate peel. Freeze drying peels had a positive effect on the total phenolic, tannins and flavonoid than oven drying at all temperature range. Moreover, freeze drying had a positive impact on the +catechin, -epicatechin, hesperidin and rutin concentrations of fruit peel. Pomegranate fruiot obtained from all the drying methods investigated were less effective against tyrosinase activity; however, they exhibited the best MIC against all the test bacteria. In addition, drying peels at 50 °C had a positive influence on the inhibitory activity of peel extracts against monophenolase. The results of the present study reveal that freeze-drying can be explored as a viable method for processing pomegranate peel to retain the maximum amount of their naturally occurring bioactive compounds.
%, percentage; °C, Degree celsius; CIE, Commission Internationale de l’Eclairage; L, CIE lightness coordinate; a*, CIE red(+)/green(−) colour attribute; b*, CIE yellow(+)/blue(−) colour attribute; C*, chroma; h°, hue angle; LC-MS, liquid chromatography–mass spectrometry; LC-MSE, liquid chromatography–mass spectrometry elctroscopy; TPC, total phenolic concentration; TFC, total flavonoid concentration; TTC, total tannins concentration; RSA, radical scavenging activity; FRAP, ferric reducing antioxidant power; DOPA, dihydroxyphenylalanine; mg CE/kg, milligram catechin equivalent per kilogram; mg/kg, milligram per kilogram; μg AAE/g, microgram ascorbic acid equivalent per gram; mg/ml, milligram per millilitre; POMOSA, Pomegranate Association of South African; mm, millimetre; AOAC, Association of Official Analytical Chemists; nr, number; m/s, meter per second; h, hour; ∆E*, total colour difference; ∆, change in measured attribute; g, gram; w/v, weight per volume; UPLC, ultra-performance liquid chromatograph; PDA, photo diode array; V, volt; kV, kilovolt; L/h, liter per hour; μm, micrometer; μl, microliter; ml/min, millimeter per minute; v/v, volume per volume; Folin-C, Folin-Ciocalteu; nm, nanometer; UV, ultraviolet; DM, dry weight; GAE, gallic acid equivalent; PVPP, polyvinylpolypyrrolidone; s, second; DPPH, 2, 2-diphenyl-1-picryl hydrazyl; mM, millimolar; μM, micromolar; pH, potential of hydrogen; TPTZ, 2,4,6-tripyridyl-s- triazine; FeCl3, iron(III) chloride; PJ, pomegranate juice; TE, trolox equivalent; MH, Mueller Hinton; L-DOPA, L-3,4-dihydroxyphenylalanine; DMSO, dimethyl sulfoxide; IC50, effective concentration at 50 %; EC50, effective concentration at 50 %; PCA, principal component analysis; MIC, minimum inhibitory concentration.
The authors thank Ms Samkele Zonyane for her assistance with antibacterial assays. Dr M Stander (Central Analytical Facility, Stellenbosch University) is thanked for her assistance with HPLC-MS analysis.
This work is based on research supported by the South African Research Chairs Initiative of the Department of Science and Technology and National Research Foundation.
Availability of data and materials
The datasets supporting the conclusions of this article are presented in this main paper. The fruit was verified by Mr. Neil Maree of the Pomegranate Association of South African (POMASA) and a voucher specimen retained with as PUC: W1153.
RRM was involved in sample collection, carried out the antibacterial, antityrosinase and antioxidant assays as well as statistical analysis and also prepared the manuscript. OAF conducted the antityrosinase assay and participated in the manuscript preparation. NPM was involved in the antibacterial assay and was also mainly involved in scientific correction of the draft manuscript. ULO designed and supervised the study, and revised the manuscript for critically important content. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Consent for publication
Not applicable in this section.
Ethics and approval and consent to participate
Not applicable in this section.
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