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Phyotherapeutic Properties of Urfa Pistachio Nuts (Pistacia vera L.)/Urfa Fistiginin (Pistacia vera L.) Fitoterapik Ozellikleri.

Introduction

According to archaeological records, the first human consumption of peanuts occured in 7000 BC (1). The oldest type of flowering peanut is the Urfa pistachio nut (Pistacia vera L.), which is a member of the cashew family (Anacardiaceae), originating from the Middle East. The Urfa pistachio nut, which is the only type of the Pistacia species that is farmed and used as a foodstuff, consists of an edible kernel, a hard outer shell and a softer shell. Currently, Urfa pistachio nuts are grown mostly in Iran, the United States, and Turkey. In Turkey, the majority are produced in the provinces of Gaziantep, Sanliurfa, and Siirt.

Some types of the Pistacia species (P. lentiscus, P. terebinthus, P. atlantica, and P. khinjuk), including the Urfa pistachio nut, are used by the general population for various purposes, such as the improvement of gastrointestinal, liver, urinary tract, and respiratory tract disorders and because of its aphrodisiac, antiseptic, and antihypertensive effects (2, 3). Due to the phenolic and flavonoid components of Pistacia species, they have antimuta-genic, antimicrobial, anti-inflammatory, anti-cancer, and antioxidant potential (3). As a source of rich phenolic components, the Urfa pistachio nut is accepted as a "unique functional food" and is in the top 50 foods with antioxidant potential (3-5).

Of all tree nuts, the Urfa pistachio nut is the richest in and has the most variations of water and fat-soluble antioxidants (6), is the only edible nut containing anthocyanin (7, 8), and contains important bioactive polyphenols such as transreservatrol and isoflavones, which have anti-cancer potential (9). All the studies that have been made on the Urfa pistachio nut can be classified in four categories:

1) Experimental Clinical Studies

Due to the mono-unsaturated fats, vitamins, and antioxidants contained in the Urfa pistachio nut, several studies have determined that it is beneficial in providing maintenance of anti-inflammatory activity, glycemic control, and endothelial function, that it prevents the oxidation of low-density lipoprotein (LDL) cholesterol in atherogenesis and may have a protective role against chronic diseases such as cancer and cardiovascular diseases (1, 10-12).

According to studies related to cardiovascular diseases, consumption of the Urfa pistachio nut creates positive effects on cardiovascular risk factors by showing a positive effect on the blood lipid profile (13-17). It has been determined in these studies, that the Urfa pistachio nut consumption has significantly reduced total cholesterol (13, 14, 16, 17), significantly reduced LDL (16-18), and increased low-density lipoprotein by a significant degree (14, 15).

As a result of studies where the Urfa pistachio nut has been added to the diet, an anti-inflammatory effect has been shown on endothelial function, oxidative status, and inflammation markers, which are strong indicators of cardiovascular diseases, and it has been determined that the Urfa pistachio nut may have a significant role in the prevention of pathogenetic events that lead to cardiovascular diseases (17, 19-21).

According to the results of an experimental study of the consumption of Pistacia vera L. on a diabetic rat model, a significant decrease was observed in the Malondialdehyde (MDA) levels of the rats given the nuts and a significant increase in total antioxidant activity (TAA). These results indicated that the nut provided antioxidant protection to membrane lipids and supported the antioxidant system and showed that inclusion of the nuts in the diet could have a dose-related beneficial effect on diabetic risk factors (22).

In addition to an intense content of fatty acids that protect cardiac health, the Urfa pistachio nut has also been determined to contain many phytochemical substances such as protein, diet fibers, potassium, magnesium, vitamin K, and [gamma]-tochopherol and has been determined to have the highest potassium, [gamma]-tochopherol, vitamin K, phytosterols, and xanthophyll carotenoid content of all the Pistacia species (1).

With a potassium content of 10.0 5 mg/gram (23-25), which is higher than other types of peanut, the sodium content of the Urfa pistachio nut may have the potential to play a role in balancing blood pressure by reducing the need for salt (26, 27).

In some recent studies, it has been suggested that the Urfa pistachio nut kernel and particularly the shell extract have a protective effect on the UV-B-origin skin damage, and these extracts can be successfully used as protective substances in topical cosmetic and medication formulations (28).

2) Studies Related to the Content of the Urfa Pistachio Nut (P. vera L.) and Antioxidant Properties

The Urfa pistachio nut, which has a high level of the three antioxidant substances of gallic acid, catechin, and epicatechin together (5), and is the richest in and has the most variations of water and fat-soluble antioxidants of all tree nuts (6), is the only edible nut containing anthocyanin (7, 8). As isoflavones and transreservatrol that have been determined in the Urfa pistachio nut are important bioactive polyphenols (29, 30), they undertake significant roles in the prevention of cancer by a chemical route (9). Due to the high amount of isoflavones (3.68 g daidzein and 3.40 mg genistein in 100 gr extract) (4, 30) and transreservatrol (1.67 [micro]g/g) (31, 32), the Urfa pistachio nut has been determined as the second richest foodstuff in respect of isoflavones after soya beans.

Another important component determined in the Urfa pistachio nut is flavonoid pro-anthocyanins, which are known as concentrated tannins (268.122 mg in 100 g nuts), and these prevent lipid peroxidization triggered by metals (4, 33-35).

As a result of chemical analysis of the kernel and shell of the Urfa pistachio nut, it has been determined that the shell contains approximately ten times more phenolic components than the kernel, and the majority of these phenolic components are formed of anthocyanins, and particularly those in the shell show a radical sweeper effect and antioxidant effect (28, 36). In a study by Tomaino et al. (5), an analysis was made of the total phenol and flavonoid content of the red shell and the kernel of the peanut plant. The results are shown in the table (Table 1, 2).

In an analysis made with High Performance Liquid Chromatography (HPLC), gallic acid, catechin, eriodictyol-7-O-glucoside, naringenin-7-O-neohesperidoside, quercetin- 3-O-rutinoside, and eriodictyol components were determined in both the outer shell and the kernel. Genistein-7-O-glucoside, genistein, daidzein, and apigenin components were found in the kernel only and epicatechin, quercetin, naringenin, lu-teolin, kaempferol, cyanidin-3-O-galactoside, and cyanidin-3-O-glucoside in the shell only. In that study, it was shown that the antioxidant activity of the shell was better than that of the kernel, and this was determined to originate from the rate of antioxidant phenolic components and the variety in the content (5).

In a similar study by Martorana et al. (28), while the majority of anthocyanin, cyanidin-3-O-galactoside, and cyanidin-3-O-glucoside components were found in the shell of the Urfa pistachio nut, the epicatechin, aglycones, quercetin, naringenin, luteolin, and kaempferol were determined only in the shell. Gallic acid and catechin were found in much greater amounts in the shell than in the kernel, but isoflavones (genistein, daidzein, genistein-3-O-glucose) were determined only in the kernel (Table 3).

In a study by Ballistreri et al. (37), daidzein, genistein, daidzin, quercetin, eriodictyol, luteolin, genistin, and naringenin flavonoids were determined in all the peanut samples. [gamma]-tochopherol, which is a major component of Vitamin E, was found in ripe red and unripe green peanuts, and it was determined that [alpha]- and [gamma]-tochopherol decreased together with ripening and drying. In the light of these results, it was suggested that unshelled peanuts are a rich nutritional source of phenolic components, especially of anthocyanin.

In a study by Gentile et al. (4) of Urfa pistachio nut kernels, while it was determined that isoflavones were not changed before peeling, the active components were significantly reduced after peeling, and the antioxidant activity was observed to reduce by 60%.

In an analysis of the essential oil content of Urfa pistachio nut plant leaves and fruit made with GC and GC/MS, it was determined that the fresh unripened nuts were richer (0.5%) than the leaves (0.1%).

3) Studies Related to Anti-cancer Properties

Due to the terpenes and phenolic components contained in the lipophyllic extracts and essential oils obtained from the leaves, fruit, gum, and resins of Pistacia species (P. lentiscus, P. terbintus, P. vera), effects have been determined such as antioxidant, antitumour, antimicrobial, anti-inflammatory, insecticidal, and antinociceptive effects (2, 38-43). In some studies, in an in vitro environment, the extract obtained from the gum of P. Lentiscus has been determined to direct human colorectal tumour cells to apoptosis and prevent proliferation (44). Furthermore, an antitumour effect has been shown with delayed growth of colorectal tumors developed in mice (45), resin has shown a cytotoxic effect against promyelocytic leukemia (46), and prostate cancer cells (47, 48).

In recent studies, the extract obtained from the fruit of P. atlantica showed growth inhibition similar to doxirubicin in human colon carcinoma cells (49), and oleoresin obtained from the resin of P. vera L. was determined to show a cyto-toxic effect against hepatocellular carcinoma, cervical cancer, and melanocyte cells (50). In another study, the metabolite pure substances in the ethanol extract, obtained from the soft outer shell of the fruit of P. vera L., showed a cytoxic effect by various rates of inhibition against the PVK-3 (anacardol 15:1), PVK-6 (anacardic acid 13:1), and PVK-8 (shikimic acid) A549 cancer cell lines (51).

Digallic acid (DGA), which is a purified from the Pistacia fruit was investigated with respect to antiproliferative and apoptotic activity on human lymphoblastoid TK6 cells, and the study results showed that DGA had a potential as a protective substance by showing an apoptosis inductor effect on the TK6 cells (52).

4) Studies Related to Antimicrobial Efficacy

While the lipophyllic extracts obtained from the red outer shell covering and the inner kernel of the Urfa pistachio show a low antibacterial effect, a significant degree of antifungal activity and antiviral effects have been shown against C. albicans and C. parapsilosis fungi (42).

In studies made with respect to the growth inhibition effect on 13 bacteria and three yeast species of the essential oils obtained from the Urfa pistachio resin, with the exception of Bacillus cereus, Pseudomonas aeruginosa, and Klebsiella pneumonia, an antimicrobial effect was seen in all otherbacteria and yeast species, and it was determined that it could be used even more effectively than nystatin, which is used effectively in the treatment of yeast infections (2, 53).

The antimicrobial activity of the foodstuff product of the polyphenol-rich extract obtained from raw shelled Urfa pistachio nuts and roasted nuts was investigated on Gram-negative and Gram-positive bacteria and some fungal species. It was determined that the extract showed a bactericidal effect against Listeria monocytogenes, Staphylococcus aureus, and methycillin-resistant S. aureus. Thus, it was suggested that the pistachio extract increased food safety by providing a control of the proliferation of some microorganisms in food products and that it could also be used in topical treatment of S. aureus. (54).

Conclusion

As the Urfa pistachio nut has antioxidant, anti-inflammatory, lipid regulatory, anti-cancer, antimicrobial, and antifungal properties, and it provides protection against cardiovascular diseases, there have been several reports stating that the intake in the daily diet would provide a significant protective effect for human health and protection from various pathological conditions (5).

As the Urfa pistachio nut is generally eaten raw as a snack, roasted, or processed (e.g., in baklava, chocolate, ice-cream, meat processing), the useful outer shell is discarded. The outer shell contains approximately ten times more phenolic components, especially anthocyanin, than the kernel, and these components show a radical sweeper effect and antioxidant properties (28, 36, 55-57). The outer shell extract, which has a protective effect against the UV-B-origin skin damage in particular, is a protective substance that can be used in topical cosmetic and medication formulations (28).

The outer shell of the Urfa pistachio nut, which has antibacterial, antifungal, antiprotozoal, and antiviral effects (42, 43, 53, 54), should not be seen as a waste product. In a study related to antiprotozoal efficacy, the extract obtained from the fruit of P. vera L. showed a cytoxic effect against Leishmania donovani, and the extract obtained from the leaves showed a cytotoxic effect against Plasmocium falciparum, and neither had any effect on normal cells (43, 56).

The shells discarded after industrial processing constitute 10% of the weight of the whole nuts (5). In Turkey, an average of 107,300 tons of Urfa pistachio nuts are produced per annum, which means 10,730 tons of waste from this production. Moreover, the waste after industrial processing causes environmental pollution. Unfortunately, these plant parts that contain anti-oxidants and perhaps many more important components as yet undetermined, are treated as agricultural waste as they cannot be evaluated. By drawing attention to this area with this review, it was aimed to create awareness for the transformation of these valuable plant parts treated as agricultural waste to products that could contribute to the national economy.

Peer-review: Externally peer-reviewed.

Author Contributions: Concept - I.K., A.K., R.D., S.S.; Design-H.K.O., I.K., A.K., R.D., S.S.; Supervision - I.K., A.K., R.D., S.S.; Resources - I.K., A.K., R.D., S.S.; Literature Search - I.K., A.K., R.D., S.S.; Writing Manuscript - I.K., A.K., R.D., S.S.; Critical Review - I.K., A.K.

Conflict of Interest: The authors have no conflicts of interest to declare.

Financial Disclosure: The authors declared that this study has received no financial support.

Hakem Degerlendirmesi: Dis bagimsiz.

Yazar Katkilari: Fikir - I.K., A.K., R.D., S.S.; Tasarim - H.K.O., I.K., A.K., R.D., S.S.; Denetleme - I.K., A.K., R.D., S.S.; Kaynaklar - I.K., A.K., R.D., S.S.; Literatur Taramasi - I.K., A.K., R.D., S.S.; Yaziyi Yazan - I.K., A.K., R.D., S.S.; Elestirel Inceleme - I.K., A.K.

Cikar Catismasi: Yazarlar cikar catismasi bildirmemislerdir.

Finansal Destek: Yazarlar bu calisma icin finansal destek almadiklarini beyan etmislerdir.

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Ismail KOYUNCU (1) [iD], Abdurrahim KOCYIGIT (2) [iD], Resat DIKME (3) [iD], Sahbettin SELEK (2) [iD]

(1) Department of Medical Biochemistry, Harran University School of Medicine, Sanliurfa, Turkey

(2) Department of Medical Biochemistry, Bezmialem Vakif University School of Medicine, Istanbul, Turkey

(3) Department of Medical Biology and Genetics, Harran University School of Medicine, Sanliurfa, Turkey

Address for Correspondence/Yazisma Adresi: Ismail KOYUNCU, Harran Universitesi Tip Fakultesi, Tibbi Biyokimya

Anabilim Dali, Sanliurfa, Turkiye E-mail: ismailkoyuncu1@gmail.com

Cite this article as: Koyuncu I, Kocyigit A, Dikme R, Selek S. Phyotherapeutic Properties of Urfa Pistachio Nuts (Pistacia vera L). Bezmialem Science 2018; 6(3): 200-5.

Received / Gelis Tarihi : 26.04.2017

Accepted / Kabul Tarihi : 01.08.2017

DOI: 10.14235/bs.2018.1842
Table 1. The antioxidant substance content of the Pistacia vera L.
fruit seed and shell (5)

                       Seed (kernel)      Shell

Total flavonoid        0.46[+ or -]0.03   70.27[+ or -]5.42
(mg CatE/g f.w.) (a)
Total flavonol         0.23[+ or -]0.02    0.99[+ or -]0.07
(mg QE/g f.w.) (b)
Total anthocyanin      Undetermined        4.86[+ or -]0.27
(mg Cy-G/g f.w.) (c)
Proanthocyanidin       1.03[+ or -]0.06   27.56[+ or -]0.18
(mg Cy/g f.w.) (d)
Vanillin index         Undetermined       16.43[+ or -]0.96
(mg CatE/g f.w) (a)
Polymerization index   Undetermined        0.60

(a) CatE: Catechin equivalent; (b) QE: Quercetin equivalent; (c) Cy-G:
Cyanidin-3-O-glucoside equivalenti; (d) Cy: Cyanidin chloride
equivalent; F.w: fresh weight

Table 2. Quantitative analysis of the phenolic components of the
Pistacia vera L. shell and seed (5)

                           Seed (kernel)       Shell
                           mg/g (f.w.)         mg/g (f.w.)

Gallic acid                12.66[+ or -]0.82   1453.31[+ or -]97.63
Catechin                    2.41[+ or -]0.18    377.45[+ or -]24.36
Epicathechin               Undetermined         104.8[+ or -]10.56
Eriodictyol-7-O-glucoside  31.91[+ or -]1.01    365.68[+ or -]13.56
Genistein-7-O-glucoside    47.02[+ or -]1.13    Undetermined
Naringenin-7-O-
neohesperidoside           37.11[+ or -]1.25    118.82[+ or -]9.64
Quercetin-3-O-rutinoside   98.08[+ or -]1.54      5.05[+ or -]0.02
Genistein                  69.15[+ or -]1.44     Undetermined
Eriodictyol                 9.37[+ or -]0.20     63.17[+ or -]1.04
Daidzein                   42.45[+ or -]1.46     N.D.
Quercetin                  Undetermined          17.75[+ or -]0.65
Naringenin                 Undetermined          11.44[+ or -]0.90
Luteolin                   Undetermined          18.97[+ or -]0.87
Kaempferol                 Undetermined           0.95[+ or -]0.001
Apigenin                    0.59[+ or -]0.001    Undetermined
Cyanidin-3-O-galactoside   Undetermined        5865.12[+ or -]362.45
Cyanidin-3-O-glucoside     Undetermined          32.56[+ or -]4.79

Table 3. Quantitative phenolic analysis of the Pistacia vera L. shell
and seed (28)

                          Seed (internal)      Shell
                          mg/g (f.w.)          mg/g (f.w.)

Phenolic acids            113.28[+ or -]4.99     5703.22[+ or -]382.06
Gallic acid               113.28[+ or -]4.99     5703.22[+ or -]382.06
Anthocyanins
- Glycosides N.D.                              16,606.64[+ or -]1036.88
Cyanidin-3-O-
galactoside                                    16,439.32[+ or -]1023.55
Cyanidin-3-O-glucoside                            167.32[+ or -]13.33
Flavan-3-ols
- Aglycones                24.33[+ or -]1.74     1932.42[+ or -]131.05
Catechin                   24.33[+ or -]1.74     1390.40[+ or -]102.59
Epicatechin               Undetermined            542.02[+ or -]28.46
Isoflavones
- Aglycones               876.72[+ or -]58.90  Undetermined
Genistein                 520.93[+ or -]30.60
Daidzein                  355.79[+ or -]28.30
- Glycosides              416.12[+ or -]24.33  Undetermined
Genistein-7-O-
glucoside                 416.12[+ or -]24.33
Flavanones
- Aglycones               112.26[+ or -]3.65      302.50[+ or -]18.15
Eriodictyol               112.26[+ or -]3.65      244.51[+ or -]14.89
Naringenin                Undetermined             57.99[+ or -]3.26
- Glycosides              636.51[+ or -]52.48    1449.34[+ or -]107.07
Eriodictyol-7-O-
glucoside                 274.85[+ or -]20.14    1120.66[+ or -]83.71
Naringenin-7-O-
neohesperidoside          361.66[+ or -]32.34     328.68[+ or -]23.36
Flavonols
- Aglycones               Undetermined             77.19[+ or -]3.96
Quercetin                  71.15[+ or -]3.68
Kaempferol                  6.04[+ or -]0.28
- Glycosides              874.11[+ or -]44.55      28.53[+ or -]4.96
Quercetin-3-O-rutinoside  874.11[+ or -]44.55      28.53[+ or -]4.96
Flavones
- Aglycones                 8.01[+ or -]0.08       85.14[+ or -]4.93
Luteolin                   85.14[+ or -]4.93
Apigenin                    8.01[+ or -]0.08
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Author:Koyuncu, Ismail; KocyIgIt, Abdurrahim; DIkme, Resat; Selek, Sahbettin
Publication:Bezmialem Science
Article Type:Report
Geographic Code:7TURK
Date:Jul 1, 2018
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