Antioxidant Activity and Phenolic Compound Profile of Pistachio Skins (Pistacia vera L., Cultivars Kallehghuchi and Ohadi)

AUTHORS

Shima Azadedel 1 , Parichehr Hanachi ORCID 1 , * , Azra Saboora 2

1 Department of Biotechnology, Faculty of Biological Science, Alzahra University, Tehran, Iran

2 Department of Plant Biology, Faculty of Biological Sciences, Alzahra University, Tehran, Iran

How to Cite: Azadedel S, Hanachi P, Saboora A. Antioxidant Activity and Phenolic Compound Profile of Pistachio Skins (Pistacia vera L., Cultivars Kallehghuchi and Ohadi), Hormozgan Med J. Online ahead of Print ; In Press(In Press):e106093. doi: 10.5812/hmj.106093.

ARTICLE INFORMATION

Hormozgan Medical Journal: In Press (In Press); e106093
Published Online: December 1, 2020
Article Type: Research Article
Received: June 13, 2020
Revised: August 4, 2020
Accepted: August 17, 2020
Uncorrected Proof scheduled for 25 (2)
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Abstract

Background: Pistachio, with the scientific name Pistacia vera L., a native plant in Asia, is a member of the Anacardiaceae family. Pistachio nuts and skins are known as a rich source of phenolic compounds with antioxidant, anti-inflammatory, and antimicrobial properties.

Objectives: In the current study, the industrial production of phenolic compounds with antioxidant activity was investigated because of the high mass production of pistachio skin in Iran.

Methods: The extraction of two pistachio cultivars, namely Kalleghuchi and Ohadi were carried out by using two methods (maceration and ultrasonic extraction) and four solvents (acetone 70%, ethanol 50%, methanol 50%, and water). Antioxidant properties of pistachio skins were determined by three methods (Folin-Ciocalteau colorimetric method, DPPH assay, TLC/DPPH analysis).

Results: The results showed that the highest content of total phenolic compounds were measured by ultrasonic and maceration methods related to Ohadi and Kallehghuchi in acetone solvents 17.4 ± 0.04 and 17.26 ± 0.1 mg/g DW, respectively. The highest antioxidant activity was measured by ultrasonic and maceration methods related to Ohadi in acetone and water solvents IC50 = 0.057 ± 0.001 and 0.059 ± 0.002 µg/ml, respectively. By TLC/DPPH analysis, gallic acid, 4-hydroxy-3, 5-dimethoxy benzoic acid, tannic acid, and some unidentified compounds were determined. By HPLC analysis, gallic acid, coumaric acid, cinnamic acid, 4-hydroxy-cinnamic acid, and 4-hydroxy benzoic acid were determined.

Conclusions: In conclusion, this study clarifies some special biochemical characteristics of pistachio skins. Therefore, according to the results of the study, pistachio skins could be successfully used in the food and pharmaceutical industries.

1. Background

Plants contain many different bioactive compounds, such as phenolic acids (1, 2). Pistachio, with the scientific name Pistacia vera L., is a native plant in Asia and one of the members of the Anacardiaceae family (3). In Iran, up to 400,000 tons/year, pistachio skin is produced, and it may be used as a source of food for ruminants (4). However, due to the toxicity of tannin content and the possibility of interaction with biomolecules, the usage of these products by ruminants is restricted (5, 6).

Pistachio nuts and skins' phenolic compounds possess antioxidant, anti-inflammatory, and antimicrobial activities (4). Antioxidants in plasma are unable to neutralize free radicals in the body without assistance, therefore providing antioxidants from food sources is necessary (7). There is so much evidence that the toxicity and the effects of malnutrition of dietary synthetic antioxidants added to food such as butylated hydroxyanisole (BHA), butylated hydroxy-toluene (BHT), and tert-butylhydroquinone confirms. In addition, the risk of liver damage and cancer in laboratory animals from the use of synthetic antioxidants is possible, so that the need for less toxic and more effective natural antioxidants is an inevitable necessity (8, 9).

Natural antioxidants increase the antioxidant capacity of plasma, thus, reduces the risk of cardiovascular disease and stroke, as well as the development of cancer which causes DNA damage, will prevent (10, 11).

2. Objectives

The purpose of this study, the use of pistachio skins for the extraction of biochemical compounds such as phenolic compounds, flavonoids, and anthocyanins, as well as natural antioxidants of pistachio, which can be a good alternative to synthetic antioxidants.

3. Methods

3.1. Reagents

Quercetin, aluminium trichloride, acetic acid, Folin-Ciocalteau phenol reagent, sodium carbonate, hydrochloric acid, 2,2-diphenyl-1-picrylhydrazyl radical (DPPH), TLC silica-gel plates, toluene, ethyl acetate, formic acid, gallic acid, tannic acid, 4 -hydroxy 3, 5 dimethoxy benzoic acid, 4-hydroxy benzoic acid, 4-chloro benzoic acid, cinnamic acid, 4-hydroxy cinnamic acid, coumaric acid, vanillic acid, acetone, ethanol, and methanol were purchased from Merck company (Germany).

3.2. Sample Preparation

Pistachio skins (Pistacia vera L., Cultivars P. vera cv. Kallehghuchi and P. vera cv. Ohadi), were harvested in the summer of 2014 from a pistachio garden in the city of Kerman (Iran) and were detected at Alzahra University herbarium. Pistachio skins were dried in the shade and crushed and stored in the dark at 4°C.

3.2.1. Ultrasound-Assisted Extraction Procedure (UAE)

Ultrasonic enhancement mechanism includes shear force created by the implosion of cavitation bubbles upon the propagation of the acoustic waves in the kHz range. The collapse of bubbles can have physical, chemical, and mechanical effects, which result in the disruption of biological membranes to facilitate the release of extractable compounds.

In the UAE method, 5ml of solvents (acetone 70%, ethanol 50%, methanol 50%, and water) were added into a 100 mg sample, then, the mixture was homogenized for 5 min and ultrasonicated at 25ºC for 20 min. Afterward, it was centrifuged for 10 min at 3000 g, and then the supernatant was kept in refrigerator 4°C (4).

3.2.2. Extraction by Maceration

In the maceration method, 100 mg of sample with 5 ml of solvents (acetone 70%, ethanol 50%, methanol 50%, and water) was macerated for 2 hours at room temperature on a shaker. homogenates were centrifuged for 10 min at 3000 g then the supernatant was kept in refrigerator 4°C (12).

3.3. Evaluation of Antioxidant Properties

3.3.1. Folin-Ciocalteau Colorimetric Method

Total phenolic content was measured by the Folin-Ciocalteau colorimetric method using gallic acid as standard (the antioxidant capacity, expressed as content of total phenols) (13). 0.2 mL of pistachio skin extracts to be tested with 1.8 mL of deionized water and 0.2 ml of diluted Folin-Ciocalteaureagent (1:15 v/v), after 5 min, 2 mL of 7% sodium carbonate solution was added, then after 90 min, absorbance was measured at 750 nm (UNICO spectrophotometer UV/Vis 2100).

3.3.2. Evaluation of Antioxidant Activity by DPPH Radical

The 2,2-diphenyl-1-picrylhydrazyl radical is a stable free radical. In this way, the ability to extract hydrogen or electron to the DPPH radical, the change of the solution color is measured from purple to yellow. Different volumes of extracts (0.1 – 10 µL) with absolute methanol were brought to 2 mL volume. After adding 1 mL of DPPH solution 0.004 % mixture was kept in the dark at room temperature for 30 min. Absolute methanol as blank and a sample containing absolute methanol 2mL and 1ml DPPH was considered as control. The absorption of the samples was read in a 517 nm (UNICO spectrophotometer UV/Vis 2100), and the percentage of free radicals cleared (RSA%) was calculated (14, 15).

3.3.3. Thin Layer Chromatography to Confirm the Antioxidant Effect

The scavenging activity of the extracts also determined by thin layer chromatography (TLC), on TLC silica gel plates 60HF254 (16). Seven μL of pure standard compounds (1 mg/mL) and 12 μL of extracts of pistachio skins were put on the plates. Ethyl acetate, toluene, formic acid, acetic acid, and water (80 – 20 – 11 – 11 - 19 v/v) were used as mobile phase. Then the plates were dried, and 0.4% methanolic DPPH solution was sprayed on it. Plates after spraying were revealed as purple background with yellow bands due to radical scavenging activity. Standards included gallic acid, tannic acid, 4-hydroxy 3, 5 dimethoxy benzoic acid, cinnamic acid, 4-hydroxy cinnamic acid, coumaric acid, vanillic acid. Rf values were calculated for each spot.

3.4. Content of Total Flavonoids

Total flavonoid compounds were measured by the aluminum chloride colorimetric method using quercetin as standard (17). 0.2 mL of pistachio skin extracts were added to 0.2 mL of aluminum chloride, 0.1 mL acetic acid 33%, and they were well mixed. Finally, the reaction mixture with ethanol 90% was brought to 5 mL volume, samples were kept for 30 min at room temperature, then absorbance was measured at 414 nm (UNICO spectrophotometer UV/V is 2100).

3.5. Content of Total Anthocyanins

An amount of 0.1 g fresh plant tissue in a porcelain mortar with 10 mL of acidic methanol (pure methanol and pure hydrochloric acid volume ratio of 1: 99 v/v) was mixed completely. Homogenates were centrifuged for 10 min at 4000 g, and the supernatant absorbance was measured at 550 nm (UNICO spectrophotometer UV/Vis 2100). The concentration of anthocyanins was calculated using the formula A = εbc, while the extinction coefficient (ε) was considered 33000 M-1 cm-1, the results were expressed as μmol for g of fresh material (μmol/g FW) (18). A: absorption, b: width of the cuvette, c: concentration.

3.6. HPLC Analysis of Phenolic Compounds

Pistachio skins of Kalleghuchi and Ohadi were extracted by maceration and ultrasonic methods with aqueous acetone solvent (70%, v/v). After centrifugation, acetone was removed in a vacuum. The remaining sample was added ethyl acetate in three stages. The upper phase, which was then ethyl acetate, was lifted and dried. Then 10 mg of the residue was dissolved in 2 mL of acetonitrile and used for HPLC. Thirty μL of the sample volume was introduced onto the column and eluted under gradient conditions performed with redistilled water: acetonitrile: acetic acid in ratio 67:32:1, with the solvent flow rate of 1 mL/min, column temperature was set at 25°C and the chromatogram was recorded at 275 nm (19).

3.7. Statistical Analysis

Results were analyzed using the software SPSS version 20 and P < 0.05. The ANOVA for one factor designs, two-way analysis of variance for two or more factor designs and data were grouped with Duncan's multiple range test.

4. Results

It is widely accepted that different validated benchmark methods are needed to describe the properties of antioxidant agents. Since the mechanism and characteristics of reactions involved in antioxidant systems are very diverse, no single method is not able to reflect all the antioxidant capacity in a complex biological system (20). In the current study, three different assays, including the DPPH assay, Folin-Ciocalteau colorimetric method, and TLC/DPPH analysis, were used in measuring the antioxidant properties. The present study shows which of the pistachio cultivars, solvents, and extraction methods were suitable for the extraction of phenolic compounds.

4.1. Evaluation of the Content of Phenolic, Anthocyanin, and Flavonoides Compounds

The results showed that the highest and the lowest total phenolic content in the ultrasonic method was measured as 17.4 ± 0.04 and 16.26 ± 0.04 mg/g DW respectively, were related to Ohadi in acetone solvent and Kallehghuchi in methanol solvent, with a significant difference that the P < 0.05 indicated (Figure 1). Whereas, the highest and the lowest total phenolic content in the maceration method was measured as 17.26 ± 0.1 and 16.35 ± 0.15 mg/g DW, respectively was related to Kallehghuchi in acetone solvent and Ohadi in water solvent with a significant difference as the P < 0.05 indicated (Figure 1). These results in Kallehghoochi and Ohadi were lower than those reported by Nadernejad et al. (12).

Figure 1. Total phenolic content in different extracts (W: Water, M: Methanol, E: Ethanol, A: Acetone). Values with different letters in the same column represent the difference significant. (P < 0.05). K: Kallehghuchi, O: Ohai (A) ultrasonic extraction and (B) maceration method.

The results showed that the highest and the lowest total flavonoid content in the ultrasonic method was measured as 4.2 ± 0.6 and 0.7 ± 0.6 mg/g DW respectively related to Kallehghuchi in ethanol and water solvents with a significant difference in the P < 0.05 indicated (Figure 2); whereas, the highest and the lowest total phenol content in the maceration method was measured 4.63 ± 1.8 and 1.33 ± 0.22 mg/g DW respectively related to Ohadi in ethanol solvent and Kallehghuchi in water solvent with a significant difference in the P < 0.05 indicated (Figure 2). These results in Kallehghoochi and Ohadi are lower than those reported by Nadernejad et al. (12).

Figure 2. Total flavonoid content in different extracts (W: Water, M: Methanol, E: Ethanol, A: Acetone). Values with different letters in the same column represent the difference significant. (P < 0.05). K: Kallehghuchi, O: Ohadi (A) ultrasonic extraction and (B) maceration method.

Conventional extraction methods, such as maceration, due to the large volume of organic solvents used and long extraction time have low efficiency (21). In this study, UAE and maceration methods have no significant difference in the extraction of bioactive compounds of cultivars Kallehghuchi and Ohadi. Therefore, the UAE method is better for extracting antioxidant phenolic compounds. However, the type of cultivar and solvent showed a significant difference in the extraction of antioxidant compounds, where the Ohadi cultivar and 70% aqueous acetone were more suitable for extracting antioxidant phenolic compounds.

Many factors, such as extraction methods, solvents, extraction time, temperature, polarity of samples, may affect the yield of chemical extraction (22). Extraction of phenolic compounds of pistachio skins decreased with increasing solvent polarity. According to Markom et al., Snyder's polarity indexes for 70% aqueous acetone, 50% aqueous ethanol, 50% aqueous methanol and water were 6.5, 7.1, 7.8 and 9 (23). Thus, phenolic compounds of pistachio are often polar with some non-polar groups, therefore, the highest phenolic compounds were observed in 70% aqueous acetone. These results were similar to the results reported by Mokhtarpour et al. (4, 23).

Low polarity solvents such as benzene and chloroform are used for the flavonoid aglycones extraction whereas, high polarity solvents such as acetone and ethanol can be used for the extraction of flavonoid glycosides (24). Pistachio skins are often glycoside flavonoids that showed a maximum extraction in aqueous ethanol 50%. Turkmen et al., showed that ethanol has a higher efficiency than other solvents, such as acetone, in extracting flavonoids from tea, which were consistent with our results (25).

The anthocyanins were measured in the skin of Kallehghoochi and Ohadi, respectively, 9.09 ± 0.5 and 10.71 ± 0.15 μmol/g DW with significant difference in the P < 0.05 indicated (Figure 3). The concentration of anthocyanin in Kallehghoochi and Ohadi is lower than those reported by Nadernejad et al. (12).

Figure 3. Anthocyanin content in the hull two cultivar pistachio Kalleghuchi and Ohadi.

4.2. Evaluation of Antioxidant Activity by Diphenylpicryl Hydrazyl (DPPH)

The results showed that the highest and the lowest antioxidant activity in ultrasonic method was measured (IC50 = 0.057 ± 0.001 and 0.082 ± 0.002 µg/mL) respectively related to Ohadi in acetone and ethanol solvents with significant difference as the P < 0.05 indicated. Whereas the highest and the lowest antioxidant activity in the maceration method was measured (IC50 = 0.059 ± 0.002 and 0.099 ± 0.003 µg/mL) respectively related to Ohadi and Kallehghuchi in water solvent with significant difference as the P < 0.05 indicated. Also, ascorbic acid and gallic acid were used as standard that their antioxidant activity was measured respectively (IC50 = 1.32 ± 0.09 and 0.88 ± 0.014 µg/mL) (Figure 4). These results in Kallehghoochi and Ohadi were stronger than those reported by Tomaino et al. and Ordonez et al. (16, 26).

Figure 4. DPPH radical scavenging activity in different extracts (W: Water, M: Methanol, E: Ethanol, A: Acetone). Values with different letters in the same column represent the difference significant (P < 0.05).

4.3. Thin Layer Chromatography to Determine Phenolic Antioxidant Compounds

The scavenging activity of the extracts was performed also by TLC/DPPH method. Each component is identified by comparing their Rf value with recognized standards, radical scavenging activity showed that with the disappearance of purple background and converting it to the yellow spots and compounds of gallic acid, 4-hydroxy-3, 5-dimethoxy benzoic acid, tannic acid, and other unidentified substances were detected (Figure 5). Tomaino et al. (16), with TLC/DPPH analysis, identified 5 phenolic compounds in Pistacia vera L., variety Bronte skins (gallic acid, catechin, cyanidin-3-O-galactoside, eriodictyol-7-O-glucoside, and epicatechin).

Equation 1.Rf=distancetraveledbythecompounddistancetraveledbythesolventfront
Figure 5. TLC plate stained with 0.4% methanolic DPPH solution. Extracts derived from two cultivars, K: Kallehghuchi and F: Ohadi in solvents, W: Water, M: Methanol, E: Ethanol, A: acetone with ultrasonic extraction: U (A), maceration method: M (B). The spots marked with 1-7 (1: gallic acid, 2: 4-hydroxy 3, 5 dimethoxy benzoic acid, 3: cinnamic acid, 4: coumaric acid, 5: vanillic acid, 6: 4-hydroxy cinnamic acid, 7: tannic acid) corresponds to the compounds with DPPH scavenging activity.

4.4. High Pressure Chromatography to Determine Phenolic Compounds

Chromatogram peaks were detected through their retention time, wavelength and UV properties with pure standards, 5 phenolic compounds in pistachio skins (gallic acid, coumaric acid, cinnamic acid, 4-hydroxy-cinnamic acid and 4-hydroxy benzoic acid) were identified (Table 1). Gallic acid and 4-hydroxy cinnamic acid were detected in all extracts, but cinnamic acid was detected in extracts derived from Kalleghuchi and 4-hydroxy benzoic acid in the extracts derived from Ohadi (Figure 6). The quantity amount of identified phenolic compounds (expressed as mg/g DW) is reported in Table 1. In fact, in Kalleghuchi pistachio skins, gallic acid (0.11 mg/ g DW) is the most abundant compound, whereas in Ohadi pistachio skins, 4-hydroxy benzoic acid (0.0723 mg/ g DW) is the most abundant compound.

Table 1. Phenolic Compounds Identified in Pistachio Skins by HPLC
Compound (Peak No.)R.T. (min)The Area Under the PeakQuantity Amount of Compounds (mg/g DW)
vanillic acid (1)0.50.750-
4-chloro benzoic acid (2)0.72.985-
4-hydroxy benzoic acid (3)1.32.053
OM0.0704
OU0.0723
gallic acid (4)27.823
KM0.063
KU0.11
OM0.043
OU0.046
cinnamic acid (5)2.55.680
KM0.02
KU0.017
4-hydroxy cinnamic acid (6)3.51.785
KM0.042
KU0.022
OM0.024
OU0.016
3, 5 dimethoxy benzoic acid (7)5.53.787-
coumaric acid (8)6.854.504
KU0.022
OM0.023
OU0.023

Abbreviations: K, Kallehghuchi; O, Ohadi; M, maceration method; U, ultrasonic extraction.

Figure 6. HPLC chromatograms obtained from (A) Kallehghuchi skin in acetone solvent with maceration method (B) Kallehghuchi skin in acetone solvent with ultrasonic extraction (C) Ohadi skin in acetone solvent with maceration method (D) Ohadi skin in acetone solvent with ultrasonic extraction. 1= 4-hydroxy benzoic acid, 2 = gallic acid, 3 = 4-hydroxy-cinnamic acid, 4 = cinnamic acid, 5 = coumaric acid.

Tomaino et al. (16) with HPLC analysis identified 13 phenolic compounds in Pistacia vera L., variety Bronte skins (gallic acid, catechin, epicatechin, eriodictyol-7-Oglucoside, naringenin-7-O-neohesperidoside, quercetin-3-O-rutinoside, eriodictyol, quercetin, naringenin, luteolin, kaempferol, cyanidin-3-O-galactoside and cyanidin-3-O-glucoside).

5. Discussion

The current study clarifies biochemical characteristics of some Kallehghuchi and Ohadi pistachio skin compounds. The results of this study showed that pistachio skin can be used a cheap and available source of bioactive compounds. Given the importance of antioxidant compounds and their ability to inhibit the effects of free radicals, the antioxidant pistachio can be a suitable option in investigating the efficacy of these drugs. Antioxidants from fruits and vegetables play an important role in the prevention of cancer, inflammatory, and cardiovascular disease. Therefore, the introduction of pistachios in daily diet may be in the protection of human health. On the other hand, pistachio can be used as a significant product in industrial processes such as in the food, cosmetics, sanitary and pharmaceutical industry. It is recommended that other common pistachio cultivars, solvents, and extraction methods be examined for antioxidant properties. Also, the phenolic compounds of pistachio skin be examined for anti-cancer and anti-inflammatory potential in vivo and in vitro.

Acknowledgements

Footnotes

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