Hindawi Publishing Corporation The Scientific World Journal Volume 2013, Article ID 219815, 33 pages http://dx.doi.org/10.1155/2013/219815

Review Article Five Pistacia species (P. vera, P. atlantica, P. terebinthus, P. khinjuk,andP. lentiscus): A Review of Their Traditional Uses, Phytochemistry, and Pharmacology

Mahbubeh Bozorgi,1 Zahra Memariani,1 Masumeh Mobli,1 Mohammad Hossein Salehi Surmaghi,1,2 Mohammad Reza Shams-Ardekani,1,2 and Roja Rahimi1

1 Department of Traditional Pharmacy, Faculty of Traditional Medicine, Tehran University of Medical Sciences, Tehran 1417653761, Iran 2 Department of Pharmacognosy, Faculty of Pharmacy, Tehran University of Medical Sciences, Tehran 1417614411, Iran

Correspondence should be addressed to Roja Rahimi; [email protected]

Received 1 August 2013; Accepted 21 August 2013

Academic Editors: U. Feller and T. Hatano

Copyright © 2013 Mahbubeh Bozorgi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Pistacia, a genus of flowering plants from the family Anacardiaceae, contains about twenty species, among them five are more popular including P. vera, P. atlantica, P. terebinthus, P. khinjuk, and P. l e nti s c u s . Different parts of these species have been used in traditional medicine for various purposes like tonic, aphrodisiac, antiseptic, antihypertensive and management of dental, gastrointestinal, liver, urinary tract, and respiratory tract disorders. Scientific findings also revealed the wide pharmacological activities from various parts of these species, such as antioxidant, antimicrobial, antiviral, anticholinesterase, anti-inflammatory, antinociceptive, antidiabetic, antitumor, antihyperlipidemic, antiatherosclerotic, and hepatoprotective activities and also their beneficial effects in gastrointestinal disorders. Various typeshytochemical ofp constituents like terpenoids, phenolic compounds, fatty acids, and sterols have also been isolated and identified from different parts of Pistacia species. The present review summarizes comprehensive information concerning ethnomedicinal uses, phytochemistry, and pharmacological activities of the five mentioned Pistacia species.

1. Introduction Different parts of Pistacia species have been investigated for various pharmacological activities. Most of the papers are The genus Pistacia belongs to the Anacardiaceae, a cosmopo- devoted to the resin of P. l e nti s c u s that is known as mastic. litan family that comprise about 70 genera and over 600 spe- In addition to their therapeutic effects, Pistacia species are cies. The species of the genus Pistacia are evergreen or decidu- used in food industry, for example, consumption of pistachio ous resin-bearing shrubs and trees which are characterized as (P. v e ra ) nut as food additive [4], P. te rebinthu s fruit as snack xerophytic trees and growing to 8–10 m tall. Pistacia lentiscus food or in making coffee-like drink [5, 6], and the antho- L., P. atl anti ca Desf., P. terebinthus L., P. v e ra L., and P. cyanin composition of P. l e nti s c u s fruit as food colorants [7]. khinjuk Stocks. are distributed from the Mediterranean basin to central Asia [1, 2]. Three Pistacia species naturally occur Chemical studies on Pistacia genus have led to discover- in Iran: P. v e ra L., P. khinju k Stocks., and P. atl anti ca Desf.; ing diverse secondary metabolites in addition to high level of P. atl anti ca has three subspecies or varieties which have been vitamins and minerals. described as cabulica, kurdica, and mutica [3].P.verais the Ourreviewpresentsacomprehensivereportonphyto- onlyspeciesofthegenuscultivatedcommercially,andtherest chemical aspects, pharmacological activities, and toxicity of ofthespeciesaremostlyusedasrootstocksforP. v e ra [1, 2]. the genus Pistacia by focusing on the data reported since 2 The Scientific World Journal the year 2000 via papers on databases including PubMed, P. te rebinthu s [16–18], P. l e nti s c u s [19–24], and P. atl anti ca Scopus, Google Scholar, and Web of Science. [25–27]. In addition to 𝛼-pinene, other major components isolated from different parts of Pistacia species are as follows: limonene (2), 𝛼-terpinolene, and ocimene (3,4) from fruits 2. Traditional Uses and leaves of P. v e ra [28]; (E)-𝛽-Ocimene (5) and limonene in fruits [18, 28, 29]; (E)-𝛽-Ocimene and terpinen-4-ol (6) Traditional uses, plant part used, and pharmacological activi- 7 ties of Pistacia lentiscus, P.atlantica, P. te rebinthu s , P. v e ra , and in leaves and p-cymen, ( )inyoungshootsofP. te rebinthu s [28–30]; bornyl acetate (8), terpinen-4-ol, sabinene (9), and P. khinju k from different regions are listed in Table 1. 10 Different parts of Pistacia species including resin, leave, myrcene ( ) in fruits, terpinen-4-ol, myrcene, p-mentha-1 (7),8 diene (11), and ocimene from leaves [27, 28, 31], sabinene fruit, and aerial part have been traditionally used for a wide Δ3 12 range of purposes. Among them, P. l e nti s c u s is the most and p-mentha-1 (7),8 diene in leaf buds, and -carene ( ) commonly used in different regions and resin of that has been in unripe galls of P. atl anti ca [31, 32]. Monoterpens are also utilized for as long as 5000 years. Resin of P. l e nti s c u s has detected in mastic water which was separated from the mastic oilduringsteamdistillation.Verbenone(13), 𝛼-terpineol been used for variety of gastric ailments in the Mediterranean 14 15 16 and Middle East countries for the last 3000 years [8]. It was ( ), linalool ( ), and trans-pinocarveol ( )arethemain constituents of mastic water [33]. 𝛽-pinene (17) in oleoresin, used in ancient Egypt as incense; it has also been used as a 𝛽 preservative and breath sweetener [4] Most of the traditional -myrceneandsabineneinfruits[28, 30, 34], terpinen-4-ol uses reports for resin of P. atl anti ca are from Iran and have in aerial parts [22], and limonene, myrcene, sabinene, and been used for the treatment of digestive, hepatic, and kidney teroinen-4-ol in leaves of P. l e nti s c u s were determined as the diseases [9]. Fruit of P. v e ra (pistachio) is used all over the main composition [28, 30, 35, 36]. world. Records of the consumption of pistachio as a food date Some of the other monoterpenes identified as effective antibacterial components of these essential oils are camphene to 7000 BC [4]. Pistachio is cultivated in the Middle East, 18 19 United States, and Mediterranean countries. Iran is one of ( ), limonene, and carvacrol ( )fromP. v e ra resin [12]. the biggest producers and exporters of pistachio nuts [10]. In Sesquiterpenes isolated in lower amount compared with monoterpenes. Germacrene-D (20)and𝛽-caryophyllene traditional Iranian medicine (TIM), different parts of P. v e ra , 21 P. atlantica, P. khinjuk P. terebinthus ,andP. l e nti s c u s have been ( ) were identified in P. l e nti s c u s and P. te rebinthu s leaves with higher concentration in comparison with other sesquit- used for a long time as useful remedies for different diseases, 22 for example, the fruit kernel of P. v e ra as a cardiac, stomach, erpenes [28]. Spathulenol ( ), an azulenic sesquiterpene hepatic, and brain tonic; the fruits of P. atl anti ca , P. khinju k , alcohol, is the predominant component of leaves of P. and P. te rebinthu s for their aphrodisiac activity and treatment atlantica and P. khinju k [37, 38]. Congiu et. al. [34]recov- of liver, kidney, heart, and respiratory system disorders, and ered Caryophyllene with the highest amount from P. l e n - the gum resin of P. l e nti s c u s , P. atl anti ca , P. khinju k , and tiscus leaves by means of supercritical CO2 extraction. Germacrene-D in P. te rebinthu s flowers, 𝛽-caryophyllene in P. te rebinthu s for their wound healing activity, and treatment 23 of brain and gastrointestinal disorders [9, 11]. P. l e nti s c u s galls, and Longifolene ( )inaerialpartsof P. l e nti s c u s are dominant [24, 29, 39].

3. Phytochemical Studies 3.1.2. Diterpenoids. Trace amounts of Diterpenoids were iso- lated from the essential oil of these species. Abietadiene (24) Various compounds from different phytochemical groups 25 were identified in Pistacia species. These are summarized and abietatriene ( ) were detected in essential oil of P. v e ra below and also in Table 2 basedonthestructureoffinding resin [12]. components. 3.1.3. Triterpenoids. Resin of these species has been char- acterized by penta and tetracyclic triterpenes. Triterpenes 3.1. Terpenoids such as masticadienonic acid (26), masticadienolic acid (27), 3.1.1. Monoterpenoids, Sesquiterpenoids, and Volatile Oil. morolic acid (28), oleanolic acid (29), ursonic acid (30)and Essential oil is one of the main components reported from their derivatives have been detected in acidic fractions of different parts of Pistacia species including leaves, resin, P. l e nti s c u s , P. te rebinthu s , and P. atl anti ca resins [40–42]. ripe and unripe fruits, galls, leaf-buds, twigs, and flowers. Several triterpenoid compounds were isolated from neutral Analysisofessentialoilsismostlyperformedbymeansof fraction of P. l e nti s c u s and P. te rebinthu s resins like tirucallol gas- chromatography (GC) based techniques. There are many (31), dammaradienone (32), 𝛽-Amyrin (33), lupeol (34), qualitative and quantitative variations between the content of oleanolic aldehyde, and 28-norolean-12-en-3-one. Quanti- essential oils. These variations are related to several param- tative and qualitative varieties in chemical composition of eters like plant species and part, sex of cultivars, harvesting resins according to the method of collection were reported time, geographical origin, and climatic conditions [12, 13]. [40, 41]. Hydrocarbon and oxygenated monoterpens are the major Anti-inflammatory properties have been reported from chemical constituents in essential oil and among hydrocar- masticadienolic acid, masticadienonic acid, and morolic acid bon monoterpens, 𝛼-pinene (1) has been reported as the isolated from P. te rebinthu s [43]. Among triterpenes isolated main compound of some samples like P. v e ra [12, 14, 15], from the resin of three sub-species of P. atl anti ca (kurdica, The Scientific World Journal 3

Table 1: Ethnomedicinal uses of selected Pistacia species.

Species Regions Plant part(s) used Traditional uses and ethnobotanical reports Reference(s) Algeria Leaf Appetizer and astringent [75] Stomach ache, dyspepsia, stomach ulcer, Resin intestinal disorders, hepatic inflammation, tooth disease, diabetes, [33, 128, 129] Greece hypercholesterolemia, and diuretic Stimulant, diuretic, hypertension, kidney stones, jaundice, cough, Aerial part [88] sore throat, eczema, and stomach ache Iraq Resin Abdominal pain [130] Gum tissue strengthener, breath deodorizer, brain and liver tonic, Iran Resin [11, 100, 102] and gastrointestinal ailments Toothache, mycosis, herpes, abdominal and intestinal pain, Italy Leaf rheumatism, antiseptic, cicatrizant, emollient, expectorant, and [131, 132] astringent Leaf Jaundice Jordan [121, 133] Pistacia lentiscus Resin Heart burn and stomach ache Morocco Leaf Digestive disease, evil eye [134] Leaf, bark Gastric analgesic [135] Root Antiseptic and antiodontalgic [135] Portugal Seeds Antirheumatic [135] Stem Buccal antiseptic [135] Aerial part Hypertension [136] Spain Fruit Influenza [71] Leaf Dermatophytosis in cows [72] Tender bud Warts [73] Edible usage, condiment, scabies, Tunisia Fruit [60] Rheumatism, and antidiarrheal Eczema, diarrhea, throat infections, paralysis, kidney stones, Turkey leaf Jaundice, asthma, stomach ache, astringent, anti-inflammatory, [96] antipyretic, and stimulant Stomach ache, cough, stress, tonic, and Algeria Fruit [20, 63] antidiarrheal Greek Fruit Mouth flavouring, tanning, and as fodder [31] Aerial part Veterinary [31] Fruit Antidiarrheal [11] Peptic ulcer, mouth freshener, antiseptic, gum tissue strengthener, as chewing gum, appetizer, phlegm dissolver, astringent, laxative, Iran Resin demulcent, diuretic, emmenagogue, carminative, visceral [9] inflammation, scabies, stomach, liver and kidneys tonic, Pistacia atlantica gastrointestinal disorders, and motion sickness Resin, bark Joint pains, toothache, wound healing [137] Fruit Stomach ache [133] Jordan leaf Antidiabetic [109] Leaf Eye infection [134] Morocco Gum tissue strengthener, breath deodorizer, cough, chill, and Resin [27] stomach disease Fruit Mouth disease [138] Turkey leaf As vegetables and food [127] Resin Wound healing [138] 4 The Scientific World Journal

Table 1: Continued. Species Regions Plant part(s) used Traditional uses and ethnobotanical reports Reference(s) Greece Resin Antidote, aphrodisiac, expectorant, and treatment of leprosy [139] Resin Smoke of it as air purifier and antiseptic [140] Iran Leaf, bark Astringent and antidiarrhea [11] Resin Diuretic, laxative, stimulant, and aphrodisiac [18] Jordan Leaf Diuretic, antihypertensive, and treatment of jaundice [18] Aerial part Hypotensive and cephalalgic [141] Pistacia terebinthus Spain Branch Antiseptic [141] Flower, leaf Odontalgia and Dislocated joint [142] Fruit Antiprostatitis [141] Cold, flu, diuretic, stomach ache, rheumatism, stimulant, [29, 53, 138, Fruit antitussive, appetizer, as coffee, urinary inflammations, and 143] soap production [29, 53, 144, Turkey Leaf Stomach ache, mycosis, and antidiabetic 145] Urinary and respiratory antiseptic, asthma, antipyretic, and Resin [53] anti-inflammatory Nut shell Tonic, sedative, and antidiarrhea [11] Iran Pistacia vera Fruit Food [10] Jordan Oil Facial skin cleanser [133] Turkey Resin Asthma, stomach ache, and hemorrhoids [146] Aerial part Veterinary use [147] Pistacia khinjuk Iran Resin Stomach discomfort, nausea, vomiting, and motion sickness [148]

cabulica and mutica), 3-O-acetyl-3-epiisomasticadienolic of P. v e ra has been reported during the fruit ripening acid (35) has been identified as the most effective antimicro- [51]. In addition to some known flavonoids isolated from 󸀠 󸀠 bial agent [42]. P. te rebinthu s and P. atl anti ca fruits, 6 -hydroxyhypolaetin 3 - methyl ether (55) has been identified in fruits of P. te rebinthu s [46, 53]. Flavonoids were also isolated from aer- 3.2. Phenolic Compounds. Gallic acid (36), catechin (37), 38 ial parts of P. atl anti ca and P. l e nti s c u s , and quercetin-3- epicatechin ( ), and gallic acid methyl ester were identified glucoside (56) was reported as the most abundant one in P. v e ra seed and skin, leaves of P. l e nti s c u s and leaves and [54]. 3-Methoxycarpachromene (57), a flavone with anti- galls of P. atl anti ca [44–46]. Bhouri et al. [47] demonstrated 39 plasmodial activity, was isolated from aerial parts of P. that digallic acid ( ) from fruits of P. l e nti s c u s has anti- atlantica [55]. mutagenic properties. Monounsaturated, diunsaturated, and Myricetin-3-glucoside (58), myricetin-3-galactoside saturated cardanols have been detected in P. v e ra kernel. 3-(8- 59 60 40 ( ), and myricetin-3-rutinoside ( )arethemajorflavonoid Pentadecenyl)-phenol ( ) was the dominating cardanol in glycosides from P. khinju k [54]. Myricetin derivatives also P. v e ra [48]. Trans and cis isomers of phytoalexin, resveratrol 󸀠 were determined as 20% of the total polyphenol amount of (3,5,4 -trihydroxystilbene) (41-42), and trans-resveratrol-3- 𝛽 P. l e nti s c u s leaves [45]. O- -glucoside (trans-piceid) were quantified in P. v e ra kernel Anthocyanins have been reported from some Pista- [49–51]. P. l e nti s c u s leaf is a rich source of polyphenol cia species. Cyanidin-3-O-glucoside (61), cyanidin-3-galac- compounds (7/5% of leaf dry weight) especially galloyl 62 43 toside ( ), and quercetin-3-O-rutinoside are the main derivatives like mono, di, and tri-O-galloyl quinic acid ( ) anthocyanins of P. v e ra fruit [44, 56, 57]. Cyanidin-3-O- and monogalloyl glucose (44)[45]. 63 45 glucoside and delphinidin-3-O-glucoside ( )havebeen 1,2,3,4,6-Pentagalloyl glucose ( ) and gallic acid from detected in P. l e nti s c u s berries and leaves [7, 45]. fruits of P. l e nti s c u s were introduced as antioxidant and anti- mutagenic compounds [52]. Flavonoid compounds have been detected in different 3.3. Fatty Acids and Sterols. Pistacia species have oleaginous parts of these species. Naringenin (46), eriodyctyol (47), fruits considered by several researchers. The oil content in daizein (48), genistein (49), quercetin (50), kaempferol (51), P. v e ra kernel and seed is about 50–60% [58, 59]andinripe apigenin (52), and luteolin (53)wereisolatedfromP. v e ra fruits of P. l e nti s c u s , P. te rebinthu s ,andP. atl anti ca is 32.8–45% fruit, and quercetin-3-O-rutinoside (54)isthemain [60–63]. The main fatty acid in seed and kernel of P. v e ra is constituent of seed [44]. Decrease in flavonoid content oleic acid [58, 64, 65]. Oleic acid has been also determined The Scientific World Journal 5

Table 2: Chemical compounds isolated from selected Pistacia species.

Name of compound Structure Species Plant part References Monoterpenoids, sesquiterpenoids, and volatile oil Leaf and [14] P. v e ra unripe fruit Resin [12, 15] Fruit [16] P. te rebinthu s Aerial part [17] P. te rebinthu s 𝛼 1 -pinene Leaf and gall [18] var. palaestina P. l e nti s c u s Resin [19] var. chia Leaf [20] P. l e nti s c u s Fruit [21] Aerial part [22–24] Leaf, fruit, [25] P. atl anti ca and gall Resin [26, 27] Leaf [28] P. v e ra Fruit [28] 2 Limonene Resin [12] Unripe and P. te rebinthu s [29] ripe fruits Fruit [28] P. l e nti s c u s Leaf [28, 36]

P. v e ra Leaf [28] 3 Terpinolene P. atl anti ca Leaf [28]

4 𝛼-Ocimene

P. v e ra Leaf [28] Unripe and [18] 5 𝛽-Ocimene P. te rebinthu s ripe fruits Leaf [28] 6 The Scientific World Journal

Table 2: Continued.

Name of compound Structure Species Plant part References P. te rebinthu s Leaf [30] Unripe [31] 6Terpinen-4-ol P. atl anti ca fruits Leaf [27, 31] OH Aerial parts [22] P. l e nti s c u s Leaf [30, 35]

Young 7 p-Cymene P. te rebinthu s [29] shoots

8 Bornyl acetate P. atl anti ca Fruits [27]

Fruits [28] Unripe P. atl anti ca [31] fruits 9 Sabinene Leaf buds [31] P. l e nti s c u s Fruits [28] Leaf

Unripe [31] P. atl anti ca fruits 10 Myrcene Leaf [31]

Fruits P. l e nti s c u s [34, 36] Leaf

Leaf [31] 11 p-Mentha-1 (7),8 diene P. atl anti ca Leaf buds [31]

3 12 Δ -carene P. atl anti ca Unripe galls [32] The Scientific World Journal 7

Table 2: Continued.

Name of compound Structure Species Plant part References O Mastic [33] 13 Verbenone P. l e nti s c u s water Mastic oil [19]

[33] 14 𝛼-terpineol P. l e nti s c u s Mastic water Mastic oil [19] OH

HO

15 Linalool P. l e nti s c u s Mastic water [33]

CH2

16 Trans-pinocarveol P. l e nti s c u s Mastic water [33]

OH

17 𝛽-pinene P. l e nti s c u s Resin [30]

18 Camphene P. v e ra Resin [12]

OH

19 Carvacrol P. v e ra Resin [12]

P. l e nti s c u s Leaf [28] 20 Germacrene-D P. te rebinthu s Flowers [29]

P. te rebinthu s Leaf [28]

21 𝛽-caryophyllene Leaf [34] P. l e nti s c u s Galls [24] 8 The Scientific World Journal

Table 2: Continued.

Name of compound Structure Species Plant part References

P. atl anti ca Leaf [37] 22 Spathulenol P. khinju k Leaf [38] HO

23 Longifolene P. l e nti s c u s Aerial parts [39]

Diterpenoids

24 Abietadiene P. v e ra Resin [12]

25 Abietatriene P. v e ra Resin [12]

Triterpenoids COOH

P. l e nti s c u s Resin [40] 26 Masticadienonic acid P. te rebinthu s Resin [41] P. atl anti ca Resin [42]

O

COOH

P. l e nti s c u s Resin [40] 27 Masticadienolic acid P. te rebinthu s Resin [41] P. atl anti ca Resin [42] HO The Scientific World Journal 9

Table 2: Continued.

Name of compound Structure Species Plant part References

P. l e nti s c u s Resin [40] COOH 28 Morolic acid P. te rebinthu s Resin [41] P. atl anti ca Resin [42]

HO

P. l e nti s c u s Resin [40] COOH 29 Oleanolic acid P. te rebinthu s Resin [41] P. atl anti ca Resin [42]

O

30 Ursonic acid COOH P. atl anti ca Resin [42]

O

P. l e nti s c u s Resin [40] 31 Tirucallol P. te rebinthu s Resin [41] HO

P. l e nti s c u s Resin [40] 32 Dammaradienone P. te rebinthu s Resin [41] O

P. l e nti s c u s Resin [40] 33 𝛽-Amyrin P. te rebinthu s Resin [41]

HO

P. l e nti s c u s Resin [40] 34 Lupeol P. te rebinthu s Resin [41]

HO 10 The Scientific World Journal

Table 2: Continued.

Name of compound Structure Species Plant part References COOH

3-O-acetyl-3- 35 epiisomasticadienolic P. atl anti ca Resin [42] acid AcO

Phenolic compounds COOH Seed and P. v e ra skin [44] Leaf [45] 36 Gallic acid P. l e nti s c u s Fruit [52] HO OH Gall and P. atl anti ca [46] OH Leaf OH

HO O OH Seed and 37 Catechin P. v e ra skin [44] P. l e nti s c u s Leaf [45] OH

OH OH

HO O OH Seed and 38 Epicatechin P. v e ra [44] skin OH OH COOH

O HO 39 Digallic acid O OH P. l e nti s c u s Fruits [47] OH HO

OH

3-(8-Pentadecenyl)- OH 40 P. v e ra Kernel [48] phenol The Scientific World Journal 11

Table 2: Continued.

Name of compound Structure Species Plant part References HO

41 Trans-resveratrol P. v e ra Kernel [49–51] OH HO

HO 42 Cis-resveratrol P. v e ra Kernel [49]

OH OH O HO OH O O

HO OH O O 3,4,5-Tri-O-galloyl O 43 O P. l e nti s c u s Leaf [45] quinic acid HO OH

OH OH

HO OH OH OH OH

O OH OH 44 Monogalloyl glucose O O O P. l e nti s c u s Leaf [45]

HO OH OH HO

HO O OH HO O OH HO O O O O OH 1,2,3,4,6-Pentagalloyl HO O O 45 O P. l e nti s c u s Fruit [52] glucose O O HO

HO OH HO OH OH OH 12 The Scientific World Journal

Table 2: Continued.

Name of compound Structure Species Plant part References OH

HO O Seed and 46 Naringenin P. v e ra [44] skin

OH O OH OH

HO O Seed and 47 Eriodictyol P. v e ra [44] skin

OH O HO O

Seed and 48 Daidzein P. v e ra [44] skin O OH HO O

Seed and 49 Genistein P. v e ra [44] skin OH O OH OH OH

HO O Seed and 50 Quercetin P. v e ra [44] skin OH OH O OH

HO O Seed and 51 Kaempferol P. v e ra [44] skin OH OH O OH

HO O Seed and 52 Apigenin P. v e ra [44] skin

OH O The Scientific World Journal 13

Table 2: Continued.

Name of compound Structure Species Plant part References OH OH

HO O Seed and 53 Luteolin P. v e ra [44] skin

OH O OH OH

HO O

Quercetin-3-O- Seed and 54 P. v e ra [44] rutinoside O O skin O OH O O HO OH HO OH OH OH

OCH3 OH OH

󸀠 6 -Hydroxyhypolaetin HO O 55 󸀠 P. te rebinthu s Fruits [53] 3 -methyl ether OH

OH O OH OH

HO O

P. atl anti ca 56 Quercetin-3-glucoside O Aerial parts [54] P. l e nti s c u s OH O OH O

OH OH OH OH

O O 3- 57 P. atl anti ca Aerial parts [55] Methoxycarpachromene O OH O 14 The Scientific World Journal

Table 2: Continued.

Name of compound Structure Species Plant part References OH OH

HO O OH

58 Myricetin-3-glucoside O P. khinju k Aerial parts [54] OH O OH O

OH OH OH OH OH

HO O OH

59 Myricetin-3-galactoside O P. khinju k Aerial parts [54] OH O OH O

OH OH OH OH OH

HO O OH

O OH O OH 60 Myricetin-3-rutinoside O P. khinju k Aerial parts [54]

OH

O O OH

HO OH OH OH

OH

HO O+ Skin [44] P. v e ra [56] Nuts [57] 61 Cyanidin-3-O-glucoside O OH Berries [7] OH P. l e nti s c u s O leaves [45]

OH

OH OH The Scientific World Journal 15

Table 2: Continued.

Name of compound Structure Species Plant part References OH

OH

HO O+

Skin [44, 56] 62 Cyanidin-3-galactoside O P. v e ra Nuts [57] OH OH O

OH

OH OH OH

OH

HO O+ OH

Delphinidin-3-O- Berries [7] 63 O P. l e nti s c u s glucoside Leaves [45] OH OH O

OH

OH OH asthemostabundantfattyacidinoilofP. atl anti ca and var. chia, and P. te rebithu s [72]. Tocopherols and tocotrienols P. te rebinthu s fruits [62, 66, 67]. Increase of oleic acid and are the most abundant constituents of unsaponifiable matter decrease of linoleic acid have been recorded during ripening of P. atl anti ca hull oil [73]. Different isomers of tocopherol, of P. l e nti s c u s fruits [60]. Other fatty acids identified in these tocotrienol, and plastochromanol-8 have been identified in species are linolenic, palmitic, palmitoleic, stearic, myristic, seed oil of P. te rebinthu s [70]. Evaluating the nutritional eicosanoic, behenic, lignoceric, arachidonic, pentadecanoic, composition of P. te rebinthu s fruits illustrates the richness of hexadecanoic, octadecanoic, and margaric acid [58, 66, 68]. this fruit in protein, oil, minerals, and fiber [62, 68]. The most abundant sterol reported in fruits of P. v e ra , P. atl anti ca , P. l e nti s c u s ,andP. te rebinthu s is 𝛽-sitosterol 5 fallowed by campesterol, Δ -avenasterol, stigmasterol, bras- 4. Pharmacological Aspects sicasterol, and cholesterol [59, 60, 69, 70]. Different pharmacological activities of five mentioned Pista- The oil from fruits of P. atl anti ca , P. l e nti s c u s , and P. te re - cia species have been described in detail in Table 3. binthus, in addition to its desirable odor and taste, has been recommended as a new source for production of vegetable oils concerning the high amount of mono-unsaturated and 4.1. Antioxidant Activity. Different parts and constituents omega-3 fatty acids like oleic acid and linolenic acid and high from P. l e nti s c u s have been shown in vitro radical scavenging quantity of phytosterols like 𝛽-sitosterol [60, 68]. properties [23, 47, 52, 74–76]. Pistacia lentiscus var. chia and P. te rebinthu s var. chia resins were effective in protecting human LDL from oxidation in vitro [77]. P. atl anti ca leaf and 3.4. Miscellaneous. Chlorophylls a and b and lutein are the fruit have shown antioxidant activity similar to or signifi- major colored components of P. v e ra nuts [56]. Pheophytin, cantly higher than those of standard antioxidant compounds 𝛽-carotene, neoxanthin, luteoxanthin, and violaxanthin were in different in vitro antioxidant assays78 [ –80]. However, the also determined in different samples of P. v e ra nuts [71]. 𝛼- essential oil from P. atl anti ca leaf showed weak antioxidant tocopherol was determined in leaves of P. l e nti s c u s , P. l e nti s c u s activity in DPPH test compared to synthetic antioxidants 16 The Scientific World Journal ] ] ] ] ] ] ] 75 52 74 76 47 23 149 [ Ref. [ [ [ [ [ [ g/mL) and 𝜇 comparable to -tocopherol) 2 𝛼 O 2 g/mL; 28% reduction of 𝜇 g/mL) 𝜇 g/mL) 𝜇 g/mL) 𝜇 -tocopherol and BHA) 𝛼 g/mL) and PGA (IC50: 1 𝜇 formation of uric acid and superoxide anions (O2-) by lipid peroxidation (IC50: 178 High scavenging capacity against H standards ( Antioxidant activity ranged between 0.52 and 4.61 mmol/L Dose dependent inhibition by GA (IC50:PGA(IC50:200 220 Higher activity of aqueous fractions fromchloroform hexane than and standards (BHA and Inhibition of linoleic acidfrom peroxidation chloroform by and aqueous hexane extracts comparablestandard to (BHA) those of the High scavenging activity (90%) equivalent tostandard that BHA of (89%) the by all extracts except chloroform Dose dependent radical scavenging activity of2 GA (IC50: ↑ increasing concentrations of both GA and PGA IC50 ranged between 5.09 and 11.0 mg/L Activity ranged between 84.6 and 131.4extract; mmol IC50: Fe2+/L 5.09–11.0 plant (mg/L) Observations 21% XO inhibitory activitysuperoxide at anion 150 activity ↓ Free radical scavenging activity towards thewas ABTS 99% + at radical 0.2 mg/mL Effectively scavenged hydroxyl radical generatedFenton reaction by the g/mL g/mL g/mL 𝜇 𝜇 𝜇 g/mL 𝜇 species. g/mL 𝜇 Pistacia g/mL for PGA g/mL g/mL g/mL g/mL 𝜇 𝜇 𝜇 𝜇 𝜇 0.2, 0.4, 1.0, 2.0, and 4.0 mM 200, 400, and 800 for GA and 100, 200, and 400 100 100, 80, 50, 30, 20,and 10, 5 mg/L 100 Dose or concentration 1, 3, 10, 30, and 100 0.05, 0.1, and 0.15% w/w Significant antioxidant activity 50,100,and150 0.05, 0.1, 0.15, and 0.2 mg/mL 0–3 mg/mL No nitric oxide scavenging activity ND Methanolic extracts Seven different extracts (1) Ethanol, (2) Ethyl acetate, (3) Aqueous/ethyl acetate, (4) Hexane, (5) Aqueous/hexane, (6) Chloroform, (7) Aqueous/chloroform Extract/essential oil/isolated component Polyphenols: galic acid (GA) and 1,2,3,4,6 pentagalloyl-glucose (PGA) Resin solution in dichloromethane Digallic acid Mastic in water Table 3: Pharmacological activities of selected in K562 cell line 2 O 2 DPPH method DPPH method Essential oil Reducing power Linoleic acid peroxidationDPPH methodScavenging activity against hydrogen peroxide 100 10–100 In vitro DPPH method Xanthine oxidase inhibitionInhibition of lipid peroxidation induced by H 100, 200, and 300 FRAP assay 5000 mg/L Oil oxidation assay by the oven test ABTS TBARsElectron-spin resonance Spectroscopy for the determination of hydroxyl radical by Fenton reaction 200, 400, and 800 Xanthine oxidase (XO) inhibition and superoxide scavenging activity Nitrate/nitrite colorimetric assay Aerial parts Leaf Fruits Resin Fruit Gum . var Plant Plant part Assay P. l e nti s c u s P. l e ntichia s c u s P. l e nti s c u s Pharmacological activity Antioxidant The Scientific World Journal 17 ] ] ] ] ] ] ] ] ] ] 81 32 78 82 77 79 88 88 44 80 [ Ref. [ [ [ [ [ [ [ [ [ mmol C; at ∘ 2.19 ± 0.14 showed the most LDL -tocopherol and -tocopherol 𝛼 𝛼 mg for seeds and skins, and g/mL. nearly similar to 𝜇 P. l e nti s c u s 0.25 ± 0.02 .015 ± 0.001 and -tocopherol 𝛼 3.25 ± 0.19 -tocopherol and BHT and nearly similar to BHA Weak radical scavenging activity Effective retardingin deteriorationoil at 60 Reducing power comparable to ascorbic acid Reducing power close to values observed by ascorbic acid Superoxide anions scavenger at a concentration0.0625 as mg/mL low as Significant reducing power; the highest reducingamongst power the USM fractions belongedtocotrienols to and the linear tocopherols and and triterpenic alcohols respectively (1) Reducing power of significantly higher𝛼 than Antioxidant power: 0 The antioxidant activity of thelipophilic lower extract than hydrophilic one much was Trolox/g of seeds and skins, respectively IC50 of concentration of 0.06%, similar to BHA0.02%. and BHT added at respectively Theantioxidant activity of hullthat oil of was TBHQ exactly at the low same concentrations as LDL protective activity; methanol/water extract of protection EC50 value significantly lower than Inhibition of LDL oxidation Radical scavenging activity (2) The chelating activity of less mg/mL1.0 than nearly was EDTAfourfold at 0.037 mg/mLcapacity for and iron has binding slightly effective (3) 85% inhibition rate at 15 ascorbic acid and BHA (4) Higher antioxidant activity than similartoBHA,BHT,andtrolox (5) Concentration-dependent scavenging compared to BHA, BHT, and Observations g/mL 𝜇 g/mL g/mL 𝜇 g/mL 𝜇 𝜇 gofnut L 𝜇 𝜇 -hexane 50 0.02%, 0.04%, and 0.06% in soybean oil 0.25;0.5;0.75; 1; 2; 3 mg/mL ND0.25;0.5;0.75; 1; 2; 3 mg/mL ND 100mgin10mLof n Superoxide anions scavenging activity (1) 20–100 (2) 0.25, 0.50, 0.75, and 1.0 mg/mL (3) 5–25 (4) 100 (5) 100 ND ND ND Different percentages (up to 15%) 2.5, 5, 10, 25, and 50 mg/2 mL ND Extracts from 30, 60,100 or 0.050–12.00 mg/mL Dose or concentration Table 3: Continued. Hexane extract - Essential oil Water and methanolextracts Ethanolic extracts The unsaponifiable matter (USM) of fruit’s hull oil Ethanolic extract Decoction Methanol/water or Dichloromethane 𝑛 Hexane and methanol/water extracts Methanol/water extract Hydrophilic extractHydrophilic extract 0.25, 0.5, or 1.0 mg/mL Radical scavenging activity in a dose-dependent manner Extract/essential oil/isolated component DPPH test Pyrogallol autoxidation method Reduction power activity Pyrogallol autoxidation method FRAP test Reduction power activity (1) Reducing power (2) Chelating abilities on metallic ions (3) Radical scavenging Activity (DPPH) (4) The totalantioxidant activity (thiocyanate method in linoleic acid emulsion) (5) Hydrogen peroxide scavenging activity Trolox equivalent antioxidant capacity (TEAC) assay (ABTS radical) ABTS radical cation decolorization assay Scavenging activity against the superoxide anion FRAP test ND Higher antioxidant capacity relative to ascorbic acid Rancimat test Copper-induced LDL oxidation DPPH radical-scavenging assay Oven test ND Significant stabilizing effect DPPH assay Lipid peroxidation (TBARS assay) LDL Copper-mediated oxidation Leaf Fruit hull Oven test Leaf Hull Leaf Leaf Kernel Fruit hull Gum Seed and skin (hull) . . . . var var var. subsp subsp ., L P. atl anti ca P. v e ra P. atl anti ca . P. atlantica mutica P. l e nti s c u s P. atl anti ca P. v e ra Bronte P. atlantica mutica P. l e ntichia, s c P. u s terebinthus. chia Plant Plant part Assay Pharmacological activity 18 The Scientific World Journal ] ] ] ] ] ] ] 83 85 87 86 84 53 150 [ Ref. [ [ [ [ [ [ g/plate 𝜇 g/mL 𝜇 antioxidant power of brain g/plate, respectively ↑ 𝜇 radical 2 O 2 g/plate, respectively; in TA98: 99 and 𝜇 g/plate 𝜇 g/plate: 67.7 and 87.8% for TA100 and 𝜇 -tocopherol 𝛼 g/plate, respectively; TA98: 62.5, 77, and 93.5% g/plate: 23% inhibition in TA100 and 52.2% in TA98; 𝜇 𝜇 -tocopherol; acetone extract reducing power was equal to brain MDA level by 63% and 50 300 and 600 58–76.8% for TA98 TA100: 47, 75.3, and 88.6% inhibition600 by 50, 300, and inhibition by 50, 300, and 600 Scavenging effect lower than that of quercetin High scavenging effect especially at 2000 Concentration-dependent radical scavenging activity Remarkable metal-chelation properties as compared to EDTA In TA100: 76, 82.8, and 96.5%,250, mutagenic 500, inhibition and rate 1000 for 100% mutagenic inhibition rate with 250 and 500 Inactive in scavenging H by 235% Isolated pure 60-hydroxyhypolaetin-30-methyl Ether showed higher antioxidant activity thanand both BHT extracts Both extracts had scavenging activity nearhigher to activity ascorbic of acid; methanol extract thanHigher acetone reducing extract power of methanol extract𝛼 than that of ↓ Scavenging capacity of crude and purifiedhigher extracts than was standards compounds (TBHQ and BHT) Considerably higher antioxidant activity compared with BHA and ascorbic acid Observations Mutagenic inhibition of 76.7% by 250,96.5% 82.8% by by 1000 500, and g/plate 𝜇 g g/mL High radical scavenging activity 𝜇 𝜇 g/plate g/mL Methanol extract had higher activity than acetone extract 𝜇 𝜇 g/mL Concentration-dependent antioxidant capacity 𝜇 g/mL g/mL g/plate g/plate 𝜇 𝜇 𝜇 𝜇 g g/mL 𝜇 𝜇 50, 300, 600 250, 500, 1000 and 2000 1, 1.5, 2,5, 3,5 and 4 0.3, 250, 500, 1000 25, 50 and 100 50 25, 50 and 100 Dose or concentration 250, 500 and 1000 Table 3: Continued. Flavonoid-enriched extract extracts Aqueous extract 0.3, 50, 300, 600 Ethyl acetate and methanol extracts Aqueous Essential oil Acetone and methanol extracts Ethanol-water extract ND Extract/essential oil/isolated component Essential oil TA100 or S. TA 100 radical scavenging 2 O S. typhimurium 2 -carotene-linoleic acid -carotene bleaching method 0.48–9.5 H DMPD radical scavenging activity DPPH radical scavenging activity DPPH assay FRAP assayPRAP assay High reducing power High reducing power Metal-chelation effect TA98 activity Total antioxidant activity in 𝛽 system DPPH test Superoxide anion scavenging activity FRAP 0.2–1 Metal chelating activity 1000–4000 Trolox equivalent antioxidant capacity assay (ABTS/K2S8O2 method) ABTS assay𝛽 ND (AFB1)-induced mutagenicity in Aflatoxin B1 (AFB1)-induced mutagenicity in typhimurium Fruits and 4 terebinth coffee brands Hull Fruits Leaf Gum TBARS and FRAP in rat Extract 0.1–0.5 g/kg Leaf P. te rebinthu s P. v e ra Plant Plant part Assay P. l e nti s c u s Pharmacological activity Antimutagenic The Scientific World Journal 19 ] ] ] ] ] ] 19 33 87 88 88 86 [ Ref. [ [ [ [ [ is S. S. , S. . S. g, 𝜇 . and g/plate, S. and g/mL) 𝜇 S. aureus 𝜇 Ent. -myrcene, B. subtilis 𝛽 S. aureus E. coli S. aureus g/mL), g/mL ,and -anethole 𝜇 B. subtilis 𝜇 C. albicans g/mL Bacillus subtilis -linalool, and 𝜇 and Fusarium sp Escherichia coli (±) (MIC: 30 trans Escherichia coli. P. ae r ug inos a ,and and E. coli E. coli and , (MIC: 4 -linaloolcomparedtothe is resistant to up to 1000 by MWR g); significant antifungal up to 1000 𝜇 (±) Enterococcus faecalis Candida albicans, g/mL). No effect on 𝜇 -caryophyllene, methyl Salmonella typhi E. coli S. enteritidis E. coli g/mL); 𝛽 g/mL) -terpineol against ,and 𝜇 𝜇 𝛼 -terpinene, and 𝛾 Trichoderma sp ,and g/mL), and no activity against ,and g/mL); less important activity against 𝜇 S. typhimurium pinene, slightly inhibited Ent. faecalis 𝜇 - -pinene. -terpineol against 𝛽 𝛼 𝛼 Staphylococcus aureus S. enteritidis, S. typhimurium -terpineol and Candida albicans -Cymene, (30 , p 𝛼 (MIC: 100 ,and , (MIC: 150 g/plate: from 54 to 68% inhibition in TA1535 Klebsiella pneumoniae 𝜇 (MIC: 40 showed an intermediate response, and g/plate, respectively E. coli 𝜇 by (+)- , St. aureus -linalool and )-verbenone, and (+)- − Verbenone, R-terpineol, and linalool showed higher antibacterial activity than other components TA100: 92, 96, and 98% inhibitionrespectively; by 50, TA 1535: 300, 62, and 600 80,concentrations and 94% for the same andfrom84to93%inTA100 showed moderate antibacterial activity, and inthe some bacteria cases, were resistant to them. isoeugenol, limonene, were resistant to TA100: 79, 83, and 94% inhibitionrespectively;TA1535:,62,76,and93%inhibitionby10,15, by 10, 15, and 30 and 30 50 and 300 foecalis,P.aeruginosa Escherichia coli were resistant to sensitive to it. The most potent antimicrobial constituentswere (±) S. aureus Observations Noticeable activity against Inhibiting activity on and Most active against significant inhibitory activity towards No effect on Significant inhibitionagainst Staphylococcus aureus enteritidis aureus TOF extract exhibited antibacterial activitytyphimurium only against typhimurium Activity against No significant inhibitory activity towards Pseudomonas aeruginosa Significant antifungal activity of MWR, activity against (MICs between 30 and 620 ( The broadest average inhibition zones were for positive control (gentamicin 10 aureus g/plate 𝜇 )-linalool g/Plate g/plate − L, and 1 mL 𝜇 𝜇 𝜇 L 𝜇 -terpineol 𝛼 -linalool )-trans-pinocarveol )-verbenone − − MWR (58 mg/mL), ( 50,300,600 ND (13 mg/mL), ( 0.125%, 0.063%, and 0.032% (v/v) (37.6 mg/mL), (±) (36.6 mg/mL), ( 4%,2%,1%,0.5%,0.25%, Dose or concentration 0.03, 0.15, 0.62, 2.5, 10.0, 40.0 mg/mL ND (29.5 mg/mL), and (+)- (29.2 mg/mL) Table 3: Continued. Mastic gum water (MWR) and its major constituents Aqueous extractFlavonoid-enriched extract extracts 1.5, 50, 300, 600 Essential oil and its fractions and components Essential oil 1.5, 10, 15, 30 Extract/essential oil/isolated component Total oligomerflavonoid-enriched extract TA1535 S. typhimurium Disc diffusion and TA100 Microdilution Sodium azide- induced mutagenicity in Disc diffusionEssential oil Disc diffusionDisc diffusion Ethanolic extract Aqueous extract 50, 100, 500 ND Disc diffusion Disc diffusion Ethanolic extract and 5 10 Microdilution agar Essential oil ND Gum Gum Disc diffusion Leaf . var P. l e ntichia s c u s Plant Plant part Assay P. l e nti s c u s Pharmacological activity Anitmicrobial and antiviral 20 The Scientific World Journal ] ] ] ] ] ] ] ] 88 91 33 55 76 92 151 152 [ [ Ref. [ [ [ [ [ [ and and ,and H. Landa 𝜇 ,and Penicillium Prevotella Aspergillus g/mL against were not sensitive and 𝜇 and all ;lessactivityin K1 strain where the Fomitopsis pinicola and Pseudomonas Escherichia coli, g/disk), tobramycin g/disk) Bacillus cereus, -pinene ranged Corynebacterium sp 𝜇 E. coli, Staphylococcus 𝜇 𝛼 H. pylori colonization in the antrum L species ,and Escherichia coli Trichoderma sp, Fusarium sp 𝜇 , P. fal c ip ar um and H. pylori Bacillus followed by the TMEWP and neutral showed a sensitizing effect at the 5 and ranged from 2 to 100 Porphyromonas gingivalis Candida albicans, Staphylococcus aureus . by volatile constituents of galls; volatile Magainst 𝜇 and Staphylococcus epidermidis Rhizopus stolonifer , colonization observed in histopathology evaluations , g/disk), and kanamycin (30 g/mL against the strains of 𝜇 𝜇 No inhibiting activity was observed against flavus Dose dependent activity against aureus comparison with gentamicin (10 (10 Klebsiella pneumoniae Delayed not block fungal growth in Penicillium sp constituents of leaf inhibited only thesp growth of very significanteffect at 10 Aspergillus flavus Activity against the aeruginosa Proteus vulgaris Gram-positive bacteria including Staphylococcus aureus, Streptococcus faecalis, Staphylococcus epidermidis, Bacillus subtilis Gram-negative bacteria including Salmonella typhimurium, Serratia marcescens, Pseudomonas aeruginosa, Alcaligenes faecalis, Enterobacter aerogenes Pseudomonas fluorescens, Porphyromonas gingivalis and corpus of the micepylori stomach. Visible reduction in The MIC values for the50 components ranged from 0.1 to The acidic fraction exhibitedHelicobacter the highest activity against pylori fraction Moderately reduced IC50 of 3.4 positive controls artemisinin and chloroquine had3.6 IC50s and of 89 nM, respectively to the extract. Salmonella typhi Against all tested bacteria mentioned invalues previous for row, essential MIC oil and pure 500–1000 mg/mL Neither solid nor liquid mastic hadcompared to any positive anti-HIV controls activity Activity against melaninogenica Observations L, and 𝜇 g/mL 𝜇 L 𝜇 g/mL; liquid 𝜇 g/mL 𝜇 (50, 100, 500 1mL)ofethanolic extract (0.338 g/mL) 25, 50 and 75 mg/mL ND MEWP: 0.049 to 1.560 mg/mL, fractions: 0.060 to 1.920 mg/mL 180 ND Solid mastic: 0–200 mastic: 0–0.0006% 0.8 and 4.9 Dose or concentration Table 3: Continued. -pinene Methanol, ethanol, ethanol + water, and water extracts Essential oil, 𝛼 Isolated components of the acidic fractions of the gum Total masticwithout polymer extract (TMEWP), acidic and neutral fractions Total masticwithout polymer extract (TMEWP) Solid and liquid mastic Flavone 3- methoxycarpachromene from ethyl acetate extract Extract/essential oil/isolated component H]-hypoxanthine 3 ;viablecellnumber IIIB Disc diffusion Ethanolic extract Disk diffusion method Disc diffusion Ethanolic extract and 5 10 Microdilution In vivo administration of extract in infected mice with H. pylori Modified [ determination by MTT assay incorporation assay ND Liquid mastic 2% liquid mastic Human T-cell leukemia MT-4 cells infected with HIV-1 Leaf and fruit derm Leaf Leaf and gall Disc diffusion Essential oils Final 0.1% v/v Gall Disc diffusion Aqueous extract 4.9 mg Gum ND Gum Broth microdilution Gum Leaf and twig Gum , chia sp. . ) var. (sp mutica P. atl antikurdica) ca ( P. l e ntiatlantica s c u s , P. cabulica, kurdica and P. atl anti ca Pistacia lentiscus P. l e nti s c u s Plant Plant part Assay Pharmacological activity The Scientific World Journal 21 ] ] ] ] ] ] ] ] ] ] 15 12 91 93 38 84 90 94 153 140 [ [ [ Ref. [ [ [ [ [ [ [ ; , S. S. P. g/mL, and Klebsiella 𝜇 compared and (MIC = g/mL against ,water 𝜇 ,and ,and s E. coli ,and -butanolic fraction 1.56 mg/mL. L. major n S. aureus ≤ Yersinia enterocolitica, Bacillus subtilis, , Streptococcus pyogenes Corynebacterium xerosis, were sensitive to the Pseudomonas aeruginosa g/mL Mycobacterium smegmatis 𝜇 Trypanosoma Enterococcus faecalis, , ,and , E. coli. ,and followed by number of parasitologicaly with a MIC: were susceptible to 0.5 ↓ g/mL) , and methanolic extract on at 4.8 ; 𝜇 g/mL Saccharomyces cerevisiae 𝜇 1 E. coli Escherichia coli − , and S. aureus B. megaterium , Helicobacter pylori (𝑃 0.05) < S. dysenteriae, E. coli, B. subtilis (MIC = 0.02–0.5 mg/mL) and fungi including (𝑃 0.01) < Klebsiella oxytoca S. epidermidis , (all in 75 mg/mL) had higher antibacterial activity was tolerant to this concentration Skin lesion size in mice infected with St. aureus Kluyveromyces fragilis Rhodotorula rubra Candida albicans All isolates of essential oil (MIC: 1.55 Dose dependent activities against Bacillus brevis Micrococcus luteus Leishmania donovani Dried leaf extract displayed notable activityPlasmodium against falciparum ↓ E. coli, Staphylococcus aureus Hydroalcoholic extract of fruits derm on extract on aureus than tobramycin and same as gentamicin and kanamycin Not any significant inhibitory potentialagainst Trypanosoma cruziRemarkable activity of branches extract at 4.8 Most active against pyogenes. E. coli with control positive mice Activity against Observations were sensitive to 10 No inhibitory activitybrucei against rhodesiense S. aureus and S. pyogenes Activity of essential oil against allBacillus tested subtilis, bacteria Salmonella including typhi, Escherichia coli, Staphylococcus epidermidis 0.06–0.4 mg/mL). Chloroform extractfungi inhibited more than growth others of activity of nonpolar smoke fractionespecially on on all of strains aeruginosa No antimicrobial effect on pneumoniae Candida albicans Active against Gram-positive and Gram-negative bacteria especially Activity against bacteria including Enterococcus faecalis, Staphylococcus aureu Staphylococcus epidermidis, Escherichia coli g/mL g/mL 𝜇 𝜇 ,and 3 3 ) − − L g/mL 𝜇 𝜇 ,10 ,10 2 2 − − ) g/mL 𝜇 S. aureus ,10 ,10 1 4 1 − − − 1/10, 1/20, 1/40, 1/80, and 1/100 v/v Locally rubbed on lesions 10 10 10 0.024, 0.049, 0.097, 0.19, 0.78, 1.56, and 25 mg/mL (for 0.049–12.5 mg/mL (for E. coli Dose or concentration 0.5, 1, 1.5, and 2 ND ND Table 3: Continued. Essential oil Essential oil of 2 and 4 Gum Extract/essential oil/isolated component Lipophylic extracts 0.8 to 9.7 Essential oil and gum smoke Ethanolic extract and its fractionsChloroform, ethyl acetate, ethyl alcohol, and ND diethyl ether extracts Hole-plate, agar dilution Agar-disc diffusion, broth microdilution, and broth susceptibility Mice infected with Leishmania major Agar disc diffusion Essential oil Disc diffusion Methanolic extract 25, 50, 75 mg/mL Maruzzella method In vitro study on four parasitic protozoa Inhibitory quantity (MIQ) method Disc diffusion, microdilution Disc diffusion, microdilution Gum Gum Gum derm Leaf Microdilution Hydroalocholic extract Leaf, branch, stem, seed Gum Not mentiond Leaf Microdilution Leaf, fruits var. P. atl antikurdica ca P. te rebinthu s Plant Plant part Assay P. v e ra P. khinju k Pharmacological activity 22 The Scientific World Journal ] ] ] ] ] 95 95 95 89 150 [ Ref. [ [ [ [ C. Herpes simplex virus and Parainfluenza virus C. parapsilosis and edema nonsignificantly at 96 by h 32% ↓ swelling by 40% similar to standard (carbamazepine) activity of the enzyme by 73% activity of the enzyme by 75% Inhibition of leukotriene B4 production incompounds rat PMNL by all ↓ Oleanonic acid: ineffective at both 24acid: and 96 h; oleanolic Oleanonic acid: significanteffect witholeanolic 45% inhibition; acid: inactive Observations Gram positive bacteria were the most sensitive ↓ 31% and 38% nonsignificant inhibitionmasticadienolic acid andof edema morolic by acid, whereas masticadienonc acid was inactive Inhibition of swelling and neutrophil infiltrationcompounds by all albicans Extracts of shell skin and freshactivity against kernel had significant same as the acyclovir Greater activity against Gram positiveGram-negative; bacteria remarkable than antifungal activity against ↓ M 𝜇 g/mL 80% inhibition of enzyme activity by all the compounds 𝜇 g/plate 𝜇 0.3 mg/ear 1mg/ear Noactivityontheedema 0.5 mg/ear 0.5 mg/ear0.5 mg/ear A nonsignificant 28% inhibition Dose or concentration 1200 12.5–100 30 mg/kg0.3 mg/ear Inhibition of edema by all triterpenes 1mg/ear 200 mg/kg Inhibition of edema 1 mg/ear1 mg/ear Inhibition of edema1 by mg/ear 44%. ND Nonsignificanteffect 58% inhibition of chronic inflammatoryswelling Table 3: Continued. Oleanolic acid and its semisynthetic 3-oxo-analogue acids Extract/essential oil/isolated component Aqueous Masticadienonic acid, masticadienolic acid, and morolic acid from methanolic extract Methanolic extract Lipophylic extracts 256 and 512 mg/mL Mouse ear inflammation induced by multiple topical applications of TPA Ethyl phenylpropiolate-induced mouse ear oedema Delayed type hypersensitivity induced by fluorobenzene in mouse ear Oleanolic and oleanonic Mouse ear edema induced by TPA Mouse edema induced by DPP Disk diffusion test Inhibition of the production of LTB4 from rat polymorphonuclear leukocytes (PMNL) Phospholipase A2 (PLA2)-induced hind-paw mouse edema Mouse ear edema induced by multiple topical applications of TPA Myeloperoxidase assay 10–100 Ethyl phenylpropiolate (EPP) induced mouse ear edema Phospholipase A2 (PLA2) induced hind-paw mouse edema In vitro antiviral assay Agar dilution methodMicrodilution 0.5 to 10 mg/mL Myeloperoxidase assay ND Ethyl phenylpropiolate (EPP) induced mouse ear edema 12-O-Tetradecanoylphorbol- 13-acetate (TPA)-induced mouse ear edema Mouse ear edema induced by multiple topical applications of TPA In vitro phospholipase A2 activity assay Hull Gall Leaf, branch, stem, kernel, shell skins, and seeds Plant Plant part Assay P. te rebinthu s Pharmacological activity Anti-inflammatory The Scientific World Journal 23 ] ] ] ] ] ] ] ] 97 98 103 105 107 146 106 104 Ref. [ [ [ [ [ [ [ [ , 𝛼 ↓ TNF- ↓ macrophage ↑ )and 𝛼 -stimulated human aortic 𝛼 in vascular adhesion molecule ↓ M) 𝜇 , MPO, and lipid peroxidation; not significantly 𝛽 Crohn’sdiseaseactivityindexandplasmainflammatory weight loss caused by the disease phosphorylation of NFkB p65 number of mouse abdominal constrictions induced by adhesion of U937 cells to TNF- leukotriene B4 (IC50: 17 edema by 61% edema by both compounds intensity of gastric mucosal damage in all models macroscopic and microscopic colonic damage; migration inhibitory factor ↓ mediators such as C-reactive protein, interleukin-6without (IL-6) any side effects; immunomodulatory effecttumor by necrosis factor-alpha (TNF- Delayed the onset and progression↓ of acute colitis and ↓ 1 (VCAM-1) and intracellular adhesion molecule(ICAM-1) 1 expression Among all extracts, only the oleoresinantinociceptive displayed activity with 32.1% inhibition atand 500 21.7% mg/kg inhibition at 250 mg/kg Dose-dependent antinociceptive activity after 30–60 mintreatment of Significant and dose-dependent anti-inflammatory activity ↓ acetic acid significant dose-dependent ↓ endothelial cells Among all extracts, only the oleoresindose-dependent exhibited anti-inflammatory a activity ↓ ↓ ↓ Inhibition of neutrophil infiltrationoleanolic 84%by oleanonic and and 67%, respectively Observations ↓ ↓ IL-1 increase in antioxidant power of colon P. resin g/mL M 𝜇 𝜇 2.22 g/day (6 caps/d, 0.37 g/cap) 0.20 g/kg chow (0.02%) 2.0 g/kg chow (0.20%) 0.4 g/Kg 0.35, 0.5 g/Kg 0.4, 0.28 g/kg 0.35, 0.5 g/Kg 250, 500 mg/kg 0.4 and 0.5 g/Kg Extract: 25, 50, 100, 200 Tirucallol:0.1,1,10, 100 250, 500 mg/kg ND 30 mg/kg 30 mg/kg Dose or concentration An oral dose of 500 mg/kg 50, 100, and 200 mg/kg of formula with 4% lentiscus Table 3: Continued. Capsules of fine powder Powder Powder 350 mg TID Improved the feeling of symptoms significantly Aqueous extract, ethanolic extract Aqueous extract ethanolic extract Aqueous extract, ethanolic extract Neutral extract and isolated phytosterol tirucallol Ethanolic and aqueous extracts Extract/essential oil/isolated component Powder finely suspended in corn oil Powder in polyherbal formulation 4-week pilot study on 10 patients with Crohn’s disease and8controls Dextran-sulfate sodium (DSS) model of colitis in mice 3-week double-blind randomised placebo controlled study on patients with functional dyspepsia U937 cell adhesion assay Xylene-induced ear edemaChronic anti-inflammatory Aqueousactivity extract (granuloma pouch method) Writhing test 0.4, 0.16, 0.28 g/kg Significant anti-inflammatory activities Measurement of NFkB p65 phosphorylation by ELISA Modification of VCAM-1 and ICAM1 expression by ELAISA Hot plate test p-Benzoquinone-induced abdominal constriction test in mice Carrageenan-induced hind paw edema Inhibition of leukotriene B4 production from rat polymorphonuclear leukocytes Bradykinin-induced mouse paw edema Oleanonic acid Myeloperoxidase assayPhospholipase A2-induced hind paw mouse edema ND Pyloric ligation-, Aspirin-, phenylbutazone-, and reserpine-induced and cold-restraint stress ulcer in rat Resin Resin Resin Gum Leaf Fruits, leaf, branches, peduncles, and oleoresin Resin Resin TNBS-induced colitis in rats . var. var var. var. . . . P. l e ntichia s c u s P. l e ntichia s c u s P. v e ra Plant Plant part Assay P. l e nti s c u s P. l e nti s c u s P. l e ntichia s c u s P. l e ntichia s c u s Pharmacological activity Effects on Gastrointestinal disorders 24 The Scientific World Journal ] ] ] ] ] ] ] ] ] ] ] ] ] 8 76 111 113 115 112 114 110 116 [ 155 154 108 109 Ref. [ [ [ [ [ [ [ [ [ [ [ [ )in Bsignal 𝜅 𝑃 = 0.003 macrophage ↑ and 𝛼 -amylase in vitro; no 𝛼 TNF- ↓ BactivityandtheNF- 𝜅 -glucosidase comparable to acarbose 𝛼 -amylase and growth factor from K562 andconcentration-dependent inhibition B16 of mouse endothelial melanoma cell cell; proliferation without affecting cell survival; significant decrease of microvessel formation Immunomodulatory activity migration inhibitory factor (MIF) in these patients Observations Significant inhibitory effect on Inhibited proliferation and induced apoptosiscolorectal of tumor human cells The most cytotoxic effect againstHL-60 promyelocytic among leukemia 13 human cell types;apoptosis inhibition of of oral natural polymorphonuclear leukocytes Anticancer activity via its delay effectcolorectal on tumorsthe developed growth from of HCT116 xenograftedmice into Remarkable potency to decrease thefunction expression and of the androgen receptorprostate in cancer androgen-responsive cell line (LNCaP) In vitro: significant dose dependent dual𝛼 inhibition of significant hypoglycemic activity normoglycemic in and hyperglycemic rats In vivo: significant acute postprandialactivityantihyperglycemic comparable to metformin and glipizideimproved and glucose intolerance in oral starch tolerance test Significantly decrease (3.1 mg/dL month, per serum glucose level among male subjects Inhibited proliferation and blocked the cellprogression cycle in androgen-independent prostate cancer PC-3 cells by suppressing NF- Significant inhibition tumor on growth withouttoxicity signs related of to apoptosis induction, reduced neovascularization, and inhibiting chemokine expression pathway A time-dependent modification in theexpression genes and of 925 phenomena in Lewisantiproliferative, lung proapoptotic, carcinoma and cells anti-inflammatory by its activities Antiproliferative and proapoptotic effect on K562leukemia human cells; inhibited the release of vascular endothelial ) g/mL g/mL IncreasedmaspinexpressioninLNCaPcells 𝜇 𝜇 g/mL (solid 𝜇 g/mL 𝜇 2.22 g/day (6 caps/d, 0.37 g/cap) Dose or concentration 2mLplantextract equivalent to 200 mg of starting material 0–200 mastic) or 0–2 (v/v)% of liquid mastic 200 mg/kg administered daily for 4 consecutive days (followed by 3 days without treatment 2, 4, 6, 8, 10,12 and 1,5,10,12.5,25,50,and 100 mg/mL 125, 250, and 500 mg/kg 0.7 g per day 45 mg/kg intraperitoneally, 3 times a week for 3 weeks Table 3: Continued. Capsules of fine powder Extract/essential oil/isolated component Aqueous extract Ethanol extract ND Liquid and solid resin Hexane extract ND Aqueous extract Powder diluted in 250 mL of water ND 2, 4, 6, and 8 ND 10, 20, and 30 Essential oil 0.01–0.1% v/v 4-week pilot study on 10 patients with crohn’s disease and8controls In vitro and in vivo (normoglycemic and streptozocin-induced hyperglycemic rats) In vitro study on human colon cancer cells (HCT116) In vitro study on human leukemic cell line In vivo human colon cancer/immunodeficient mouse model Human cell line (androgen-responsive prostate cancer cell line) In vitro enzymatic starch digestion and rat model Human prostate cancerlines cell (LNCaP and DU-145), RT-PCR, and Western blotting were used to detect maspin expression The human prostate cancer cell lines (PC-3), MTT assay, gene assay, RT-PCR, and Western blotting Immunocompetent mice Essential oil Lewis lung carcinoma cells Essential oil 0.01% v/v Cells line and the in vivo chicken embryo CAM angiogenesis model Resin Leaf Resin Resin Resin Human study Fruit var. sub. var. var. P. l e ntichia s c u s Plant Plant partP. atl anti Assay ca P. l e ntichia s c u s P. l e nti s c u s P. l e ntichia s c u s P. atl antikurdica ca Pharmacological activity Antidiabetic Antitumor The Scientific World Journal 25 ] ] ] ] ] ] ] ] ] ] ] ] ] ] ] 13 85 111 117 121 119 123 125 125 122 127 124 156 126 120 [ Ref. [ [ [ [ [ [ [ [ [ [ [ [ [ [ g/mL) 𝜇 HDL after weeks 3 use ↑ g/mL) against all of the tested cell lines, 𝜇 oil-treated rabbits showed none of those changes bilirubin and activity of 3 enzymes including alkaline total cholesterol, total cholesterol/HDL ratio, and exceptforMCF7(IC50:13.5 Moderate cytotoxic effect against breast(MCF7), cancer hepatocellular cell carcinoma cell line line (HEPG2),cancer cervix cell line (HELA), andn-hexane normal fraction melanocytes showed (HFB4); strong cytotoxic(IC50: effect 3.15–4.17 Promoted the preneoplastic lesionswith development increasing in liver rat relative liver weight Inhibited the development of the atheroscleroticthe lesions thoracic in artery Observations ↓ phosphatase (ALP), alanine aminotransferase (ALT), and aspartate aminotransferase (AST) BeneficialeffectsonHDL,LDL,andaorticintimal thickness. The methanolic extractadditionally showedantioxidant activity an and remarkable decrease insurface aortic lesions Strong acetylcholinesterase (AChE) inhibition Restored intracellular antioxidant glutathione (GSH) levels and downregulated CD36 mRNA expression resultedantioxidant in and antiatherogenic effects Hepaticfibrosis,aninflammatoryresponse,mild cholestasis, and depletion of reduced glutathione associated with an increase in its oxidizedadministration form in for healthy five rats; weeks in thioacetamide-inducedliver rat lesions, it aggravated the inflammatory,glutathionefibrotic, depleting and responses without affecting theof extent lipid peroxidation Serum total cholesterol, LDL, total cholesterol/HDLlipoprotein, ratio, apolipoprotein A-1, apolipoprotein B, AST, ALP, and gamma-GT were reduced in human subjects Mercury induced toxicity in rabbits causedlevel increase of in ALP, AST, and the urea serum,P. while it l was e reported nti that s c u s No inhibitory activity against AChE andselectively tyrosinase while inhibited butyrylcholinesterase (BChE) at moderate levels (below 50%) at the tested concentrations ↓ LDL/HDL ratio and Inhibited the development of hydropic degenerationfatty and changes in the liver andeffect demonstrated hypolipidemic g/mL 𝜇 g/mL g/mL 𝜇 𝜇 ND Methanolic extract (1% v/w) cyclohexane extract (5% v/w) Dose or concentration 4mL/kg (contained 1.946 g of solid matter) 5, 10, 15, 20, and 25 0.1 mg/mL Relatively weak AChE inhibitory activity 5g 25, 50, 100, and 200 O (70 : 30) 0.7 mg/mL 50% growth inhibition similar to 500 nM of doxorubicin 2 oil 5% -butanol n Table 3: Continued. Crud methanolic extract fractionated against petroleum ether, chloroform, and Powder in diet 0, 0.01, 0.1 and 1% Methanolic and cyclohexane extracts Extract/essential oil/isolated component Aqueous extract Aqueous extract Ethanol : H Total polar extract 2.7, 27, and 270 Methanol and ethyl acetate extracts Aqueous extract 15 mg/kg and 75 mg/kg Powder diluted in one glass (250 mL) of water Ethyl acetate and methanol extracts Pistacia Nut 20% in diet In vitro cytotoxic activity against human cell lines Rat liver medium-term carcinogenesis bioassay (Ito-test) Rat model using Carbon tetrachloride TLC bioautography assay, Ellman’s colorimetric method human colon carcinoma HT29 cells Cell culture (peripheral blood mononuclear cell, PBMC); cell viability assessed via MTT assay Rat model using Thioacetamide Ellman’s colorimetric method and the modified dopachrome method Rabbit model, mercury induced toxicity Human model (10 patients with moderate hypercholesterolemia) Resin Fruit Rabbit model Fruit 1 g/kg Leaf Fruit Rabbit model leaf Resin Leaf Ellman’s colorimetric method Resin Human model Fruit Seeds oil Fruit (roasted, unsalted pistachio nuts) Fruit Rabbit model Fruit 1 g/kg var. P. v e ra P. te rebinthu s Plant Plant part Assay P. l e nti s c u s P. v e ra P. atl anti ca P. l e nti s c u s P. atl anti ca P. l e ntichia s c u s P. te rebinthu s P. l e nti s c u s P. v e ra P. te rebinthu s Pharmacological activity Effects onliver and serum biochemical parameters Effects on atherosclerosis Anticholinesterase activity 26 The Scientific World Journal

[32]. P. v e ra fruit revealed significant antioxidant activity indicated acceptable antifungal activity but moderate anti- similar to the synthetic antioxidant [81]. Lipophilic extract bacterial effect. Among some of its major compounds, (±)- from P. v e ra nuts showed lower antioxidant potential that linalool and 𝛼-terpineol had the highest antimicrobial effect than of hydrophilic extract [82]. One survey showed P. v e ra [33]. skins had a better antioxidant activity compared to seeds by Essential oil from leaf and gum of P. atl anti ca showed means of four different assays because of higher content of acceptable antibacterial and antifungal activities [90–92]. antioxidant phenolic compounds in skins [44]. Antioxidant However, leaf ethanolic extract had no distinct antimicrobial activity has been also reported from other parts of P. v e ra [83]. activity [88]. In one study, the extract from P. te rebinthu s leaf had A remarkable inhibitory activity of different extracts and nearly 12-fold higher antioxidant capacity than those of essential oil from P. l e nti s c u s leaves was observed against BHA and ascorbic acid [84]. P. te rebinthu s fruits showed Salmonella typhimurium; additionally, essential oil showed noticeable metal-chelation properties as compared to EDTA significant inhibitory effects against S. enteritidis and Staphy- and high radical scavenging activity similar to the standards. lococcus aureus [86, 87]. Antioxidant activity of the fruits may be elevated by roasting As reported by Adams et al. [55],theleavesandtwigsofP. process [85]. atlantica and its active substance 3-methoxycarpachromene showed antiprotozoal activity against Plasmodium falci- 4.2. Antimutagenic Activity. Essential oil and different parum. P. atl anti ca var. kurdica gum controlled cutaneous extracts from P. l e nti s c u s leaves indicated significant inhibito- leishmaniasis in mice infected with Leishmania major [93]. ry effect on mutagenicity in vitro [86, 87]. Gallic acid, digallic Extract from P. v e ra branch had significant inhibitory activity acid, and 1,2,3,4,6-pentagalloylglucose, polyphenols isolated against Leishmania donovani and leaf extract inhibited Plas- from the fruits of P. l e nti s c u s , induced an inhibitory activity modium falciparum without cytotoxicity on mammalian cells against mutagenicity and genotoxicity in in vitro assays [94]. [47, 52]. 4.4. Anti-Inflammatory and Antinociceptive Activity. Anti- 4.3. Antimicrobial and Antiviral Activities. Pistacia species inflammatory and antinociceptive activity of five mentioned have demonstrated significant antibacterial activity against Pistacia species have been shown in Table 3. various Gram positive and Gram negative bacteria as shown P. te rebinthu s gall showed anti-inflammatory activity in in Table 3. Antimicrobial activity of Pistacia lentiscus resin, different in vivo models of acute and chronic inflammation the essential oil and gum from P. atl anti ca var.kurdica [95]. Masticadienonic acid (26), masticadienolic acid (27), and its major constituent 𝛼-pinene and P. v e ra gum against and morolic acid (28), three triterpene isolated from P. te re - Helicobacter pylori were recorded [15, 33]. A study indicated binthus gall,seemtoberesponsibleforitsanti-inflammatory that antibacterial activity of P. l e nti s c u s gum oil can be activity [43]. Additionally, oleanonic acid (29)fromthegalls attributed to combination of several components rather than of P. te rebinthu s , reduced the production of leukotriene B4 to one particular compound. Verbenone, R-terpineol, and from rat peritoneal leukocytes and showed antiedematous linalool showed high antibacterial activity against Escherichia activity in mice [96]. Oleoresin and leaf extract from P. v e ra coli, Staphylococcus aureus, and Bacillus subtilis which is showed significant anti-inflammatory and antinociceptive comparable to that of mastic oil itself [19]. P. l e nti s c u s activity [97]. gum revealed selective antibacterial activity against Porphy- Extract of the resin of P. l e nti s c u s var.Chiaand its iso- romonas gingivalis and Prevotella melaninogenica and had lated phytosterol tirucallol (31) showed anti-inflammatory antiplaque activity on teeth by inhibiting bacterial growth in activity on human aortic endothelial cells and had significant saliva [76]. inhibitory activity on adhesion molecules expression in TNF- Significant antifungal activity was seen from essential oil 𝛼-stimulated human aortic endothelial cells [98]. It was of P. l e nti s c u s leaf and gum, different extracts of P. khinju k leaf, proposed that the anti-inflammatory effect of P. l e nti s c u s var. and essential oil of P. v e ra gum [15, 19, 38, 88]. Evaluating the chia gummayberelatedtoinhibitionofproteinkinaseC effect of P. v e ra gum essential oil on growth of 13 bacteria which leads to decrease in superoxide and H2O2 production and 3 yeasts demonstrated inhibitory effect on all of them by NADPH oxidase [99]. except Bacillus cereus, Pseudomonas aeruginosa,andKleb- siella pneumonia and more effective yeasticide than nystatin. 4.5. Effects on Gastrointestinal Disorders. One of the most Carvacrol was found to be the most effective constituent important traditional uses of gums from Pistacia species is for [12, 15]. Lipophylic extracts from different parts of P. v e ra management of gastrointestinal disorders. Moreover, there showed a little antibacterial activity and noticeable antifungal are several scientific studies that confirm this property100 [ – one against C. albicans and C. parapsilosis. Kernel and seed 102]. Resin of P. l e nti s c u s significantly reduced the intensity of extracts showed significant antiviral activity [89]. gastric mucosal damage induced by pyloric ligation, aspirin, Some active constituents of essential oil from the aerial phenylbutazone, reserpine, and restraint with cold stress parts of P. khinju k responsible for its antibacterial and anti- via its antisecretory and cytoprotective activities [103]. In fungal activity are 𝛼-pinene, 𝛽-pinene, myrcene, beta-cary- one double-blind placebo controlled trial, P. l e nti s c u s gum ophyllene, Germacrene B, and Spathulenol [38]. improved the feeling of symptoms significantly in patients Organic fraction of mastic water obtained during the with functional dyspepsia [104]. Moreover, Pistacia species steam distillation of resin from Pistacia lentiscus var. chia exerted significant antibacterial activity on Helicobacter pylori The Scientific World Journal 27

[15, 33]. Supplementation with P. l e nti s c u s oil in experimental been reviewed comprehensively with special attention to the model of colitis delayed the onset and progression of acute probable anticancer mechanisms [118]. colitis and led to decrease weight loss caused by the disease The fruit extract of P. atl anti ca sub. kurdica showed [105]. A polyherbal formula that contains P. l e nti s c u s gum growth inhibition in human colon carcinoma cells similar to caused significant decrease in colonic damage and biochem- Doxorubicin [119]. P. v e ra oleoresin demonstrated moderate ical markers related to pathophysiology of IBS in rat model cytotoxic effect against breast cancer cell line, hepatocellular of colitis [106]. Adminstration of P. l e nti s c u s var. chia resin carcinoma cell line, cervix cancer cell line, and normal to patients with established mild to moderate active crohn’s melanocytes [120]. disease (CD) for 4 weeks caused significant reduction in CD activity index and plasma inflammatory mediators without any side effects and also as an immunomodulator resulted in 4.8. Effects on Liver and Serum Biochemical Parameters. significantly reduction in tumor necrosis factor-alpha (TNF- P. l e nti s c u s leaf demonstrated significant hepatoprotective 𝛼) and enhanced macrophage migration inhibitory factor in activity against carbon tetrachloride induced hepatotoxicity these patients [107, 108]. in rats by reducing the level of bilirubin and activity of liver enzymes [121]. However, another study reported hepatic 4.6. Antidiabetic Activity. Aqueous leaf extract from P. atl an - fibrosis, mild cholestasis, and depletion of reduced glu- tica showed significant inhibitory effect on 𝛼-amylase and tathione by long-term administration of aqueous leaf extract 𝛼-glucosidase in vitro [109, 110]. It demonstrated significant in healthy rats [122]. Administration of P. l e nti s c u s var. chia acute postprandial antihyperglycemic activity comparable to gum for 18 months in healthy volunteers caused reduction in metformin and glipizide in starch-fed rats. It also improved liver enzymes and exerted hypolipidemic effect [111]. Extracts glucose intolerance [110]. However, another study on this from P. v e ra fruits have shown beneficial effects on HDL and extract did not show significant hypoglycemic activity when LDL level in rabbit model of atherosclerosis [123]. Positive tested in normoglycemic and streptozocin-induced hyper- changes in lipid profile were recorded after three-week use of glycemic rats [109]. Administration of P. l e nti s c u s var. chia P. v e ra nuts in patients with moderate hypercholesterolemia. gum to human subjects for 12 months caused significantly The decrease in triglyceride and LDL levels was not signif- decrease in serum glucose level among male subjects. Serum icant [124]. P. te rebinthu s fruit demonstrated hypolipidemic glucoseinwomenwasnotaffected[111]. effect in hypercholesterolemic rabbits [125].

4.7. Antitumor Activity. Among mentioned species of Pista- 4.9. Effects on Atherosclerosis. More over than the antihyper- cia, P. lentiscus is the most investigated for antitumor activity lipidemic activity that described above, Pistacia species exerts (Table 3). P. l e nti s c u s var. chia gum inhibited proliferation their antiathesclerotic effects by direct activity on atheroscle- and induced apoptosis of human colorectal tumor cells in rotic lesions moreover than their antihyperlipidemic activity. vitro [112]. The resin exerted the most cytotoxic effect against Both methanolic and cyclohexane extracts from P. v e ra promyelocytic leukemia among 13 human cell types and also fruits have shown beneficial effects on HDL, LDL, and inhibited the natural apoptosis of oral polymorphonuclear aortic intimal thickness in rabbit model of atherosclerosis. leukocytes [76]. The gum demonstrated anticancer activity The methanolic extract additionally showed an antioxidant via delaying the growth of colorectal tumors developed from activity and remarkable decrease in aortic surface lesions human colon cancer cells xenografted into mice8 [ ]. It also [123]. P. te rebinthu s fruits inhibited the development of the increased maspin (a mammary serine protease inhibitor with atherosclerotic lesions in the thoracic artery [125]. P. l e nti s c u s tumor suppressive activity for prostate cancers) expression resin that downregulated CD36 mRNA expression (as the in responsive prostate cancer cells and inhibited cell pro- oxLDL receptor in macrophages that play a pivotal role in liferation and blocked the cell cycle progression [113, 114]. atherosclerotic foam cell formation) resulted in antiathero- Essential oil of P. l e nti s c u s demonstrated significant inhibition genic effects [126]. on tumor growth in immunocompetent mice without signs of toxicity, related to apoptosis induction, reduced neovas- cularization, and inhibiting chemokine expression [115]. In 4.10. Anticholinesterase Activity. Aqueous extracts from P. addition, it had antiproliferative and proapoptotic effect on atlantica and P. l e nti s c u s leaves showed strong acetyl- human leukemia cells and inhibited the release of vascular cholinesterase (AChE) inhibition [13]; additionally, both the endothelial growth factor from these cells [116]. Despite methanol and ethyl acetate extracts of P. atl anti ca leaf showed many reports on antitumor activities of P. l e nti s c u s ,one relatively weak AchE inhibitory activity [127]. However, one in vivo study showed that the high dose of P. l e nti s c u s study showed that ethyl acetate and methanol extracts of gum promoted the preneoplastic lesions development in rat various commercially terebinth coffee brands (an oily brown- liver with increasing liver relative weight which proposed coloured powder produced from the dried and roasted fruits that desirable anticarcinogenic effects of mastic could be of P. te rebinthu s ) and the unprocessed fruits of P. te rebinthu s obtained at relatively low doses [117]. In one recent study, did not have inhibitory activity against AChE and tyrosinase, the current data on the anticancer activities of gum, oil, while they selectively inhibited butyrylcholinesterase (BChE) and extracts of P. l e nti s c u s L. and its major constituent, have at moderate levels [85]. 28 The Scientific World Journal

5. Conclusion AST: Aspartate aminotransferase B(a)p: Benzo(a)pyrene In traditional Iranian medicine textbooks and papers, five BHA: Butylated hydroxyanisole species of Pistacia genus including P. v e ra , P. l e nti s c u s , BHT: Butylated hydroxytoluene P. te rebinthu s , P. atl anti ca , and P. khinju k had been introduced DMPD: N,N-dimethyl-p-phenylendiamine for treating the wide range of ailments. These species until DPPH: 2,2-Diphenyl-1-picrylhydrazyl now have been utilized in Iran by people for different EC50: Half maximal effective concentration nutritional and medicinal proposes. This review considered EDTA: Ethylenediaminetetraacetic acid findings about phytochemical and pharmacological proper- EPP: Ethyl phenylpropiolate ties of these five species and presents comprehensive analysis FRAP: Ferric reducing antioxidant power of papers published since the year 2000. Ethnopharma- Gamma-GT: Gamma-glytamyl transpeptidase cological data about these species may help us to know IC50: Thehalf maximal inhibitory concentration that many pharmacological aspects proposed nowadays for LOX: Lipoxygenase these species have been derived from traditional uses like MBC: Minimum Bactericidal Concentration antiseptic and antimicrobial, anti-inflammatory and anti- MDA: Malonaldehyde nociceptive, antihepatotoxic, and anticancer activities and MIC: Minimum inhibitory Concentration their beneficial effects in gastrointestinal disorders. Further- NF-kB: Nuclear factor kappa-light-chain-enhancer more, there are several pharmacological activities discussed ofactivated B cells in traditional medicine such as diuretic, lithontripic, anti- OxLDL: Oxidized low density lipoprotein tussive, antirheumatic, antiasthmatic, antihypertensive, and PLA2: Phospholipase A2 aphrodisiac activities which are not supported by any current SGOT: Serum glutamic oxaloacetic transaminase scientific documents, and so, they could be considered for SGPT: Serumg lutamic-pyruvic transaminase investigation by researchers. SOD: Superoxide dismutase Phytochemical studies provided evidence for traditional TBARS: Thiobarbituric acidre active substances applications of these species. With respect to phytochemical TBHQ: Tertiary Butyl hydroquinone assays, triterpenes found in the resin and monoterpens are TPA: 12-O-Tetradecanoylphorbol-13-acetate. the most abundant composition of the essential oil from dif- ferent parts of these species. Essential oil constituents might be valuable chemotaxonomic marker to ascertain different Conflict of Interests Pistacia chemotypes. Considering the therapeutic effect of The authors declare that they have no conflict of interests. isolated components, it can be concluded that terpenoids including mono, di-, and triterpenoids are associated with anti-inflammatory and antimicrobial effects. High amount of References natural phenols and flavonoids is related to potent antioxi- [1] V. Mozaffarian, Trees and Shrubs of Iran,FarhangMoaser, dant and anticancer activities. Tehran, Iran, 1st edition, 2005. Review on current researches about the genus Pistacia L. [2] C. Kole, Wild Crop Relatives: Genomic and Breeding Resources highlighting pharmacological studies on crude plant parts, Legume Crops and Forages, Springer, Heidelberg, Germany, extracts, and some pure metabolites has provided scientific 2011. evidence for traditional uses and has revealed this genus to [3] V. 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