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Review Article

A review on pistachio: Its composition and benefits regarding the prevention or treatment of diseases

Ghaseminasab Parizi M, BSc1, Ahmadi A, MSc2, Mazloomi SM, PhD3*

1- Student of MSc in Nutrition Sciences, Student Research Committee, School of Nutrition and Food Sciences, Shiraz University of Medical Sciences, Shiraz, . 2- Faculty Member, Research Center for Health Sciences, Dept. of Clinical Nutrition, Faculty of Nutrition and Food Sciences, Shiraz University of Medical Sciences, Shiraz, Iran. 3- Associate Prof., Nutrition and Food Sciences Research Center, Dept. of Food Hygiene and Quality Control, School of Nutrition and Food Sciences, Shiraz University of Medical Sciences, Shiraz, Iran

Abstract Received: January 2016, Accepted: March 2016

Background: The pistachio is a produced by about 20 of . Present-day studies show the health benefits of pistachio in preventing or treating diseases such as , cardiovascular diseases (CVDs), cancer, multiple sclerosis (MS), and erectile dysfunction. Materials and Methods: MEDLINE / PubMed, and Google Scholar databases were searched using the keywords of vera, Pistacio, chemical composition, anticancer, anti-inflammation, antidiabetic, and antioxydative. Relevant articles published in the last decade were identified and reviewed. Results: The chemical composition (macronutrients, micronutrients) of pistachio and the main outcomes of treatment with pistachio species were categorized. The possible mechanisms of action of treatment with pistachio species are discussed in this article. Numerous studies have been conducted to investigate the beneficial effects of nuts such as pistachio on health, lipid profile, and diseases. Conclusions: It is commonly believed that pistachio can be used in the prevention and treatment of diseases such as diabetes, metabolic syndrome, coronary heart disease (CHD), cancer, inflammatory diseases, and MS. This study showed that nuts such as pistachio have many beneficial effects on health, and can be used for controlling different diseases. It seems that the pistachio may have anti- inflammatory, anti-diabetic, anti-hyperlipidemia, and anti-proliferation effects and may be recommended for the prevention, improvement, or treatment of diseases such as diabetes, CVD, inflammatory bowel disease (IBS), cancer, and MS.

Keywords: Pistachios, Composition, prevention, Treatment, Disease.

Introduction Central and Eastern areas of Iran. Kerman has 45.5% and Rafsanjan 20.6% of the total global Several species of the genus Pistacia are pistachio orchards (2). Pistachios comprised referred to as pistachio. The pistachio is a nut 2% of the total nut consumption in 2005; thus, produced by about 20 species of shrub such as greater attention* should be paid to its the Pistacia vera, , Pistacia properties. Although the pistachio is popular, it terebinthus, Pistacia khinjuk, and Pistacia has not been investigatedsufficiently as an lentiscus that belong to the edible nut. Other nuts have been investigated () family. Pistachio (Pistacia more than the pistachio (3). Some diseases vera) is cultivated in Iran, the Middle East, such as diabetes mellitus type 2, cancer, United States, and Mediterranean countries metabolic syndrome, hyperlipidemia, and (1).

Iran is the largest pistachio producer in the * Corresponding author: Seyed Mohammad Mazloomi, world, yielding about 40% of the total global Nutrition and Food Sciences Research Center, Dept. of production in the year 2009. The U.S. is the Food Hygiene and Quality Control, School of Nutrition second largest after Iran with 27% of the total and Food Sciences, Shiraz University of Medical Sciences, Shiraz, Iran. global production. Pistachio is produced in the Email: [email protected]

57 JOHE, Winter 2015; 4 (1) Ghaseminasab Parizi et al cardiovascular diseases (CVDs) cause many constituents of 100 g of kernel consisted of complications leading to death. Nuts, such as 55.2-60.5% oil, 15.0-21.2% , and 14.9- pistachio, have dietary fibers, magnesium, and 17.7% (10). Pistachios are one of low sodium contents. Fibers produce a feeling the richest sources of fiber (10.3 g/100 g), and of satiety, thus preventing . Magnesium 100 g of pistachio has 600 (11). In decreases hypertension via its effect on addition, pistachio contains a high level of vasodilation. Thus, pistachio may have energy (12). beneficial effects on weight and lowering II. Micronutrients (minerals) hypertension. On the other hand, in many The composition of minerals in pistachio studies pistachio consumption (30-80 g/day) kernels was: 4.0 mg sodium, 1048-1142 mg has decreased total cholesterol up to 10.1% , 120-150 mg , 494-514.5 and low-density lipoprotein-cholesterol (LDL- mg , 5.8-11.4 mg iron, 1.0-1.4 mg C) up to 8.6% (4-7). copper, 157.5-165.0 mg magnesium (10), and Pistachio is an important source of energy and 9.3 mcg/100 g selenium (12). many nutrients, minerals, antioxidants, and III. and Antioxidants vitamins that are essential for human health Pistachios are a good source of numerous (8). Moreover, pistachio kernel has been found antioxidants, including , carotenes, to have some medical properties due to its lutein, selenium, flavonoids, and antioxidant and antimicrobial activities (9). phytoestrogens (5,6beta-carotene,alfa- The aim of this review study was to report the carotene, and cryptoxanthin) which are chemical composition of pistachio and its important sources of A. Flavonoids, a health benefits in preventing or treating subclass of , constitute a large diseases such as diabetes, cardiovascular group of food constituents, many of which diseases (CVD), cancer, and multiple sclerosis alter metabolic processes and have positive (MS). impacts on health. Pistachios are the richest source of (279 mg total Materials and Methods phytosterols/100 g; sitosterol 210 mg/100 g, as the predominant ) (13), vitamin B-6 MEDLINE/PubMed, and Google Scholar (1.3 mg/100 g), lutein and (1205 databases were searched using the keywords of g/100 g), carotenes (157g/100g), tocopherols Pistacia vera, chemical composition, (22.5 mg/100 g) (14), and isoflavones anticancer, anti-inflammation, antidiabetic, (anthocyanins, chalcones, dihydrochalcones, and antioxydative. Relevant articles published dihydroflavonols, flavonols, flavanones, in the last decade were identified and flavones, and isoflavonoids) (3.63 mg/100 mg) reviewed. In total, 16000 articles were found. (15-18). Some studies have found eriodictyol After filtering the obtained texts using the and anthocyanin in pistachios (19). aforementioned criteria, 30 articles were The pistachio is also a good source of selected and the main subjects of each study unsaturated fatty acids (, linolenic were selected in this review. acid, and ) that are essential for the

body. Nuts such as pistachios contain a high Results rate of monounsaturated fatty acids (MUFA) Chemical composition (> 55%) (20). I. Macronutrients The effect of micronuteirents present in The chemical composition of pistachio pistachio on health depends on , rootstock, maturity at Pistachios are rich in phosphorus which helps harvest, and moisture content. The to break down meat and other proteins into composition of pistachio kernels of various amino acids. Phosphorus is necessary for has been previously studied (10). The

58 JOHE, Winter 2015; 4 (1) Pistachio and health

hormone production and helps the body use B has an important role in cellular metabolism. It vitamins (12). is essential for cell growth and differentiation. Phosphorus deficiency can cause glucose Inadequate dietary iron intake results in intolerance and abnormally low serum inflammatory anemia. phosphate level (hypophosphatemia), resulting Furthermore, pistachios are rich in Mg which in loss of appetite, anemia, muscle weakness, helps to prevent osteoporosis, and nervous bone pain, rickets (in children), osteomalacia system and immune system diseases (24). Mg (in adults), increased susceptibility to infection is involved in more than 300 essential (21), numbness and tingling sensation in the metabolic reactions and plays an essential role extremities, and difficulty walking (21). in a wide range of important biologic Calcium has an important function in the reactions. The clinical symptoms of its human body as a structural element, and deficiency are hypocalcemia, neuromuscular cofactor for enzymes and proteins, and in cell hyperexcitability, hypokalemia, cardiac signaling, mediation of the constriction and dysrhythmias, and acute myocardial infarction relaxation of blood vessels, nerve impulse (AMI). Pistachios are also rich in K (24). A transmission, muscle contraction, and the low serum K level can be life threatening secretion of hormones like insulin (22). The because of potential negative changes in maximum calcium levels in the examined cardiac rate, rhythm, and conduction, as well pistachio cultivars were about 400-1350 as numerous structural and functional mg/kg. Pistachio nuts are rich and absorbable alterations in various organs, especially sources of calcium (23). Pistachio is rich in skeletal muscles. The high rate of non-heme iron (24). Iron is essential to in pistachio prevents heart disease, LDL- development and health. Iron is a key oxidation, diabetes, and cancer and promotes component of proteins that carry oxygen and the immune system.

Table 1: The main outcomes of pistachio intake summarized in order of each study and its properties Author/s Type of study and Pistachio species Objectives Main outcomes (year) sample size dose/duration ↓ (sLDL-P), ↓ non-HDL-P i.e. Pistachio- VLDL-P plus LDL-P), The supplemented diet (57 percentage of sHDL-P increased Hernández- RCCT, 54 subjects with g/day), controlled diet, Anti-hyperlipidemia by 2.23% compared with a Alonso et al. prediabetes, 2 groups 4 months each, 82 reduction of 0.08% after the CD, /(2015) separated by a 2-week the overall size of HDL-P wash-out ↓in the PD ↓: WC, FBG , total Body composition, metabolic, RCT, 60 individuals Unsalted pistachios cholesterol, LDL, hs-CRP, TNF- Gulati et inflammatory, and oxidative with metabolic (20% energy) for 24 86 a, FFAs, TBARS, and al. /(2014) stress parameters syndrome weeks adiponectin levels ↓Systolic BP, ↓total peripheral RCCT, 30 adults (40 to P, 20% of total energy resistance, ↑cardiac output, Sauder et al. - 74 years of age) with 65 for 4 weeks improved some measures of /(2014) type 2 diabetes heart rate variability reduced 75-km cycling time trial RCT, 19 adults in two performance and increased post- Inflammation, oxidative stress, Nieman et 75-km cycling time Pistachio nut, 3 exercise plasma levels of immune dysfunction, metabolite 87 trials oz./day, 2 weeks raffinose, sucrose, and al. /(2014) shifts metabolites related to leukotoxic effects and oxidative stress HPE ↓d prostaglandin (PG) E2 production, IL-6 and IL-8 Effects of HPE and its release, and cyclooxygenase Gentile et al. (PPF) in a cell model RCT Pistacia vera L. 88 (COX)-2 expression, inhibited /(2014) the increase in paracellular by reduced NF-jB activation

59 JOHE, Winter 2015; 4 (1) Ghaseminasab Parizi et al

Evaluation of the cytoprotection, ROS formation, Cytoprotective activity of Experimental study, Extracts and bioactive lipid peroxidation, protein Pistacia vera extracts against Shahraki et Male Sprague–Dawley compounds in Pistacia 12 carbonylation, mitochondrial oxidative and carbonyl stress in al. /(2014) rats (280–300 g) vera, 100 μl and lysosomal membrane type 2 diabetes damages in cell toxicity models Fresh nuts (, Case-control, 113 , , and Bagheri et 89 - patients with MS and pistachio) in the diet, had a protective role for MS al. /(2014) 113 healthy women more than five times a week ↑ HDL-C and a ↓LDL-C, total 40 g or 1.5 oz shelled RCT, 60 adults with cholesterol to HDL-C ratio and Kasliwal et Effect on vascular health pistachios every day 64 mild dyslipidemia FBS, improvements in vascular al. /(2014) for three months stiffness ↓sdLDL levels following the RCT, 28 individuals Control diet (25% Effects on the cardiometabolic 2PD, ATP-binding cassette Holligan et with elevated LDL TF); (1PD; 30% TF); al. 52/(2014) profile transporter A1-mediated serum levels (2PD; 34% TF) cholesterol efflux capacity Five study meals Three meals had 50 g available CHO: Effect on postprandial glucose Pistachio reduced postprandial (WB50g), and insulin levels, gut hormones RCT, 20 subjects with glycemia, increased glucagon- Kendall et (WB+B+Ch) and 63 related to satiety and endothelial metabolic syndrome like-peptide levels and may have al. / (2014) (WB+P) function insulin-sparing properties Two meals had 12 g white bread and pistachios, 5-10 weeks ↓FBS, insulin, and HOMA of Reducing the prediabetes stage insulin resistance, ↓fibrinogen, RCT, 54 subjects, two Pistachios, 57 g/day, Alonso et al. and improving its metabolic risk oxidized LDL, and platelet 69/(2014) diets for 4 months profile factor 4, ↑ glucagon-like peptide-1 Link between high nut A cross-sectional survey , , consumption and lower total Askari et Lipid profile of 9660 adults aged +19 pistachios, and 59 cholesterol al. /(2013) years

Overview of the current Associated with a variety of state of research relating Fischer et Metabolic diseases and cancer Nut health promoting effects 62 to the health potential of al. / (2013) nuts Glutathione peroxidase levels Experimental study, 28 did not have significant effect on Pistacia atlantica Farzanegi et and total oxidative capacity of female rats (weight: antioxidant and lipid profile 90 extract, 8 weeks al. /(2013) liver and plasma lipid profile 155.8 ± 2.7 g), 4 groups levels ↓TC and LDL-C fractions, a London et 50 Blood lipid profile Review Pistachios intake beneficial change in TC/HDL-C al. /(2013) and LDL-C/HDL-C of rats Protein content for examined Most important cultivars varied between 13.75 Davarynejad commercially Concentration of nutrient and 28.13 g/100 g, and N: 2.2- 23 - cultivated pistachio in et al. / elements 4.5 g/100 g, P: 350-550 mg/100 Iran, Pistacia atlantica, (2012) g, K: 500-1100 mg/100 g, and Pistacia vera Ca: 40-135 mg/100 g No significant changes in body 42 g pistachios (RSG), Impact of different dosages of weight or BMI and waist-to-hip a 70 g pistachio pistachios on body weight, RCT, 90 subjects with ratio in any groups, serum TG Wang et al. (HSG), and no 43 blood pressure, blood lipids, metabolic syndrome sign lower in the RSG group, no /(2012) pistachios (DCG) for blood glucose, and insulin significant change in HSG or 12 weeks DCG groups

Quantified the release of Raw, roasted and polyphenols, Beneficial relation between Mandalari salted pistachios, and et al. (lutein), and tocopherols from - pistachio consumption and muffins made with 91 pistachios during simulated health-related outcomes /(2012) raw pistachios human digestion

60 JOHE, Winter 2015; 4 (1) Pistachio and health

lowered LDL-C, no significant Baer et al.37/ Pistachio, 0, 42 and 84 Metabolisable energy contained RCT, 16 volunteers change in total plasma g/day for 3 weeks (2012) cholesterol, HDL, or TAG pistachios on their RCT, 118 faculty and Subjects in condition one Determine fullness and desks for an 8-hour Kennedy et staff at a mid-western consumed significantly fewer 41 satisfaction period on two separate al. /(2011) university calories days ↓ Glucose, LDL, total cholesterol, and TG, decreased Antidiabetic, RCT, 32 healthy young Pistacia vera L., 20% serum interleukin-6, TOS, lipid antihyperlipidemia, men (age range: 21–24 Sari et al. of daily caloric intake hydroperoxide, MDA, and 4 antioxidative stress, and anti- years) /(2010) for 4 weeks increased superoxide dismutase, inflammatory effects no significant change in C- reactive protein and TNF-a RCCT, 28 adults with 1 PD; 10%; 2 PD; Increases in serum lutein and g- Serum antioxidants and Kay et al. hypercholesterolemia 20% energy from tocopherol ↓serum oxidized- 40 biomarkers of oxidative status /(2010) pistachios for 4 week LDL 53 g (240 cal) of RCT, 59 Participants to salted pistachios (n = Both groups lost weight, Effects on body weight and consume 1 of 2 Li et al. 31) or 56 g of salted ↓triglycerides in the pistachio 39/(2010) lipid levels in obese participants isocaloric weight pretzels (220 cal; n = group reduction diets 28) for 12 weeks Effects on blood lipids, ↑TC,TG, sialic acid and Alturfan et Experimental study, antioxidant activity, oxidative Pistachio, for 8 weeks thiobarbituric acid-reactive 27 high--fed rats al. /(2008) stress, and sialic acid levels substances 1 PD; 10% of energy, ↓ Total cholesterol, LDL, non- RCCT, 28 individuals 2 PD; 20% of energy HDL-C, apo B, apo B/apo A-I , CVD risk factors, dose-response with LDL-C 2.86 from pistachios; 34% and plasma SCD activity Gebauer et relations, and lipid-lowering mmol/l consumed 3 25 total fat; 8% SFAs, The 1 PD and 2 PD, ↓total al. /(2008) mechanisms isoenergetic diets for 4 15% MUFAs, and 8% cholesterol/HDL-C (1% and weeks each PUFAs 8%), LDL-C/HDL-C Effects on lipids and 2 doses of pistachios The 1 PD and 2 PD, elicited a Gebauer et lipoproteins, apo L, and plasma RCCT, 28 (1 PD; 10%, 2 PD; dose-dependent lowering of al. 25/(2008) fatty acids, cholesteryl ester hyperlipidemia 20% of energy), for 4 TC/HDL, LDL/HDL, and non- transfer protein and SCD weeks each HDL/HDL Pistachios 10%, 20%, Consumption of pistachio as Experimental study, Effects on lipid oxidation and and 40% of daily 20% of daily caloric intake leads Aksoy et al. Rats, three groups (n = 92 serum antioxidant levels caloric intake for 10 to ↓HDL and TC/HDL ratio and /(2007) 12 for each) weeks inhibits LDL-C oxidation ↓Oxidative stress, and improved RCT, 24 healthy men total cholesterol and HDL levels Antihyperlipidemia, Pistachio nuts for 20% and 20 healthy women HDL and AOP levels, and Kocyigit et antioxidative stress, and anti- of their daily caloric 29 (mean age of 33.4 AOP/MDA ratios were al /(2006) inflammatory effects intake for 3 weeks years) significantly increased, triglyceride and LDL

MS: Multiple sclerosis; TNF-a: Tumor necrosis factor-a; TOS: Total oxidant status; MDA: Malondialdehyde; RCT: Randomized controlled trial; RCCT: Randomized cross-over clinical trial; sLDL-p: Small low-density lipoprotein particles; non-HDL-P: Non-high-density lipoprotein particles; CD: Control diet; PD: Pistachio diet; ↑: Increased significantly; ↓: Decreased significantly; IIEF: International Index of Erectile Function; PCDU: Penile color Doppler ultrasound; PUFAs: Polyunsaturated fatty acids; PPF: Polymeric proanthocyanidin fraction; HPE: Hydrophilic extract from Sicilian pistachio nut; DB-RCCT: Double-blind, randomized, placebo-controlled, crossover trial; FBG: Fasting blood glucose; CRP: C-reactive protein; sBP: Systolic blood pressure; apo L: Apo lipoprotein; SCD: Indexes of plasma stearoyl-CoA desaturase activity; sdLDL: Small and dense LDL; 1PD: One serving of pistachios per day; 2PD: two servings of pistachios per day; WB: White bread; (WB+B+Ch): White bread, butter, and cheese; WB+P: white bread and pistachios

Pistachio and Lipids profiles good effects on lipid profile and decreases the Epidemiologic and clinical studies have serum LDL-C, but it does not significantly demonstrated that nut consumption decreases affect triglycerides or HDL-C (26). The the risk of different diseases. Many studies decrease in serum LDL-C may be caused by (Table 1) have shown the beneficial effects of phytosterols in nuts. Phytosterols decrease pistachios (15–20% of energy) on lipids and cholesterol via binding to it in the body, and lipoproteins in the body (25). Some studies pistachio is rich in phytosterols (214 mg/100 have shown that the regular intake of nuts has g) (27). The effects of nut consumption on

61 JOHE, Winter 2015; 4 (1) Ghaseminasab Parizi et al blood lipids and other biomarkers have been either a high dose or recommended dose of investigated in more than 40 intervention pistachio nuts for 12 weeks, compared with a trials. Interventional studies on pistachios have control group, resulted in no changes in the shown its beneficial effects on lipids (28-30). body mass index (BMI) or waist-to-hip ratio. Studies have shown that pistachios can These results were consistent with those in improve blood lipid profiles in subjects with other populations (30-34). Nuts may be helpful moderate hypercholesterolemia, and in turn, in the regulation of body weight through reduce the risk of CVDs (31). When pistachios inhibiting the appetite and fat absorption (40- were given to (32) healthy young men for 4 43). weeks, significant decreases in blood glucose, Other studies have shown that the lipid in nuts total cholesterol, and serum interleukin-6 were (pistachios) is more poorly absorbed than other observed, with improved endothelium food sources. Baer et al. reported that the vasodilation and total antioxidant status (33). measured energy density of pistachios was The consumption of pistachios has been shown 22.6 kJ/g, which is 5% less than the currently to significantly decrease oxidative stress, and accepted energy value of 23.7 kJ/g calculated improve total cholesterol and its LDL levels in using the Atwater general factors (43). healthy volunteers (34). Li et al. showed that The decrease in weight gain is because of the pistachio consumption decreased plasma fiber content, slower digestion, and protein in triacylglycerols and body weight when pistachio, which increase satiety (42). compared with a carbohydrate snack in obese Although pistachio has a high fat content, it is subjects (35), and also revealed that among 50 the source of unsaturated fatty acids. The foods, pistachio contains the highest amount of unsaturated fatty acids and high protein antioxidants (36). Studies have shown that its content of pistachios can cause an increase in kernel protects hepatocytes against oxidative resting energy expenditure and diet-induced stress. The consumption of pistachios for a thermogenesis (43). However, several other long duration of time has a useful nutritional bioactive compounds are present in pistachio effect during the prediabetic states. Studies which can decrease weight gain (44). have shown that pistachios have a glucose- Pistachio effect on diseases lowering and insulin-lowering effect, thus, Pistachio and metabolic syndrome, diabetes promoting a healthier metabolic profile (37, and coronary heart disease 38). Metabolic syndrome consists of metabolic Consumption of pistachio nuts, as a snack, has abnormalities, including abdominal obesity, beneficial effects on glycemic control, blood increased blood pressure, and blood glucose pressure, obesity, and inflammation markers in and lipid abnormalities often known as diabetic patients (28). The beneficial effect of prediabetes. Obesity and metabolic syndrome pistachios on lipid profiles may be due to are common in developing countries, (45) and essential fatty acids (EFAs) in its composition. are associated with diabetes and increased Pistachio and weight gain CVD mortality (46). Aminotransferase levels Nut consumption may lead to weight gain in in obesity are associated with insulin the population at large, especially in obese resistance and metabolic syndrome and the subjects and those with high lipids profiles due aminotransferase level was significantly to its high fat content. Li et al. reported that the lowered with the consumption of pistachios daily consumption of a defined quantity of (47, 48). Epidemiological evidence has shown pistachio nuts, when compared to an isocaloric that continuous ingestion of nuts is beneficial refined carbohydrate snack, did not interfere in the reduction of risk factors of coronary with weight loss and improved triglyceride heart disease (CHD) (49). Increased levels in a weight loss trial (39). Some results consumption of pistachios has been shown to (33) indicate that the daily consumption of improve the blood glucose level, endothelial

62 JOHE, Winter 2015; 4 (1) Pistachio and health function, and some indices of inflammation lipid parameters, but also results in and oxidative status in healthy young men improvements in vascular stiffness and (50). Data suggest that pistachios have a endothelial function (66). glucose-lowering and insulin-lowering effect, A moderate-fat diet containing pistachios promote a healthier metabolic profile, and modestly improves some cardiovascular risk reverse certain metabolic deleterious factors in adults with well-controlled type 2 consequences of prediabetes (51). Some of diabetes (67). Protein, , potassium, these beneficial effects may be related to the magnesium, , g-tocopherol, and a antioxidants naturally present in pistachio, number of phytochemicals are beneficial for since pistachio consumption has been shown the heart, and are abundant in pistachios (68). to reduce oxidative stress markers in healthy Replacement of low-fat snacks with pistachios subjects (29). Pistachios have a low glycemic about 20% of the daily energy intake modifies index. The study conducted by Josse (52) systemic hemodynamics, increases heart rate indicated that, when consumed together with variability, and reduces ambulatory blood high carbohydrate foods, pistachios decreased pressure in adults with well-controlled type 2 the absorption of carbohydrate, and diabetes (69). Nutrients in pistachios postprandial blood glucose (43). Some clinical (monounsaturated fatty acids, antioxidants trials with statins suggest that this will result in such as , lutein, b-carotene, and a reduction of 9-12% in the risk of CHD (53). proanthocyanidins) have antioxidant properties Prospective studies show that total (29, 40) and may protect the liver against cholesterol/HDL-C and LDL-C/HDL-C ratios oxidative stress (43). are more powerful predictors of CVD risk than With pistachio-enriched diets there were LDL-C alone (54-56). Some studies, using higher plasma lutein, a-carotene, and b- doses of 15-20% of total energy of pistachios, carotene concentrations than the baseline diet found no significant changes in LDL-C, and higher lutein and g-tocopherol in 2 PD VLDL-C, triacylglycerols, apo A-I, or apo B only. Pistachio-enriched treatment diets (57-59). Perhaps, they relied on participants to significantly decreased serum oxidized-LDL in consume pistachios (and replace other foods) participants; this was related to the control of under free-living conditions and assessed their diet. Oxidized-LDL is recognized as a intake by diet records. contributing factor in the initiation and It can be concluded that regular consumption progression of CVD (70, 71). The decrease in of nuts (pistachio, and etc.), particularly 4 oxidized-LDL was related to a significant times a week, may result in lower dyslipidemia increase in serum concentrations of occurrences and may have cardio-protective antioxidants; thus, pistachios have a beneficial effects (60). effect on concentrations of serum antioxidants The provision of 20% of total calories by (72). consumption of pistachios (61) or 40% of the Frequent pistachio consumption is a useful required fat by consumption of walnuts and nutritional strategy for the prediabetic state. almonds (62) showed no effect on blood Data suggest that pistachios have a glucose- pressure in healthy individuals (61, 63) and lowering and insulin-lowering effect, create a subjects with hypercholesterolemia (16). In a healthier metabolic profile, and reverse certain one-year trial, the participants; blood pressure metabolic deleterious consequences of was lowered significantly (64). Compared with prediabetes (73). white bread, pistachio consumption reduced The beneficial effect of pistachio on CHD, postprandial glycemia, increased glucagon-like metabolic syndrome, and diabetes may be due peptide levels, and might have had insulin- to the EFAs and antioxidants in its sparing properties (65). Frequent consumption composition. of pistachios not only improves glycemic and

63 JOHE, Winter 2015; 4 (1) Ghaseminasab Parizi et al

Pistachio and Multiple sclerosis (MS) 27%) (80), pancreatic cancer (81), and breast MS is a disease of the central nervous system cancer. However, it had a stronger effect on (CNS). Lesions make it difficult to send postmenopausal breast cancer than messages from the brain to the body. These premenopausal breast cancer. lesions are formed when the immune system Pistachio consumption produced more gut attacks the protective covering of the nerves microbiota composition that produced called the myelin. Oligodendrocyte damage potentially beneficial butyrate-producing and subsequent axonal demyelination is a bacteria in comparison to almond hallmark of this disease. The cause of MS is consumption. Although the number of unknown. Studies show that nutrition is bifidobacteria was not affected by the effective in controlling the progression of the consumption of the two nuts, pistachio disease (74). Polyunsaturated fatty acids consumption decreased the number of lactic (PUFAs) exert immunosuppressive actions acid bacteria. Increasing the consumption of through their incorporation in immune cells nuts, such as pistachios, has an effect on and may affect CNS cell function. increasing gut microbiota composition (81). Antioxidants and PUFAs have the potential to Hypotheses that explain the anticancer decrease disease symptoms through specific effects of nuts, e.g. pistachios which contain pathomechanisms. EFAs have been linked to many antioxidant and anti-inflammatory improvement of immune responses (75, 76). substances, provide growing evidence Pistachios are rich in EFAs, i.e. they can have indicating the key role of inflammation and beneficial immune response (51). Previous oxidative stress in the development of specific studies have shown that n-6 PUFAs can affect cancer types. Since reprogramming of energy oligodendrocytes membrane composition, and metabolism has been recently recognized as a myelin formation in the rat brain can be key feature of cancer cells, nuts may affect accelerated by dietary lipids. Although the cancer progression through their ability to alter protective effects of pistachios on cellular lipid profiles and cell metabolism (82). metabolism may be due to other nutrients such Prostate cancer cells appear to use acyl as iron, potassium, and phosphorus, cholesterol acyltransferase (ACAT) to remove respectively. The data available are the excess cholesterol and store it as insufficient to assess any potential benefit or cholesteryl ethers in order to maintain the harm from PUFA supplementation (77). uptake of LDL and associated fatty acids, Pistachio and cancer including the arachidonic acid that is involved Although the pistachio contains vitamins and in cell proliferation and growth by lowering micronutrients that have potential biological cholesterol levels. They can reduce the mechanisms of action for reducing the risk of accumulation of cholesteryl ethers in cancer cancer, epidemiological evidence on the cells, and therefore, possibly reduce the uptake effects of pistachio on the risk of cancer in of LDL and EFAs, ultimately resulting in humans is still limited and insufficient. In one inhibition of cancer cell proliferation and study, pistachio in the diet following tumor growth (81). However, pistachio anticancer drugs such as cisplatin and consumption may have anti-proliferative vincristine had a protective effect against effects. anticancer drug-induced disruptions in the Pistachio and inflammatory bowel disease motor and cognitive functions (78). (IBD) Recent studies showed that consumption of Pistachios are important sources of nuts such as pistachio reduced cancer mortality antioxidants that reduce inflammation and and nuts may protect individuals from prostate oxidative stress (29, 50) via inhibiting cancer (about 31%) (79), colorectal and colon interlukin-1B that increases the expression and cancers in women, endothelial cancer (about realization of inflammatory mediators (82).

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Antioxidants in the pistachio inhibit improvement, or treatment of diseases such as prostaglandin E2 and interlukin-1B-induced diabetes, CVD, IBD, cancer, and MS. COX-2 protein expression that promotes colorectal tumor growth by stimulating Acknowledgements angiogenesis, cell invasion, cell growth, and The authors would like to thank the Center for survival in humans (81). Development of Clinical Research of Nemazee Pistachios contain proanthocyanidins, which is Hospital and Dr. Nasrin Shokrpour for her a subclass of polyphenolic compounds found editorial assistance. in and have anti-inflammatory activity, radical scavenging activity, and antioxidant Conflict of interest: None declared. effects (83).

On the other hand, antioxidants in pistachios References increase the expression of the Anti- inflammatory gene by repressing the 1. Bozorgi M, Memariani Z, Mobli M, Salehi Surmaghi MH, Shams-Ardekani MR, Rahimi transcription rate of interferon-induced protein R. Five pistacia species (P. vera, P. atlantica, P. with tetratricopeptide repeats (TPR) that terebinthus, P. khinjuk, and P. lentiscus): a causes inflammation in the intestine (84). review of their traditional uses, phytochemistry, and pharmacology. ScientificWorldJournal 2013; 2013:219815. Conclusions doi: 10.1155/2013/219815. eCollection 2013. 2. Zomorrodi A. Improvement of Studies show that nuts such as pistachio have competitiveness: the case of Iranian pistachio. many beneficial effects on health, and can be World Journal of Social Sciences 2014; used for controlling different diseases. 4(1):237-50. Numerous studies have been conducted to 3. Switzerland. World Health Organization. Noncommunicable Diseases Country Profiles. investigate the beneficial effects of nuts such Geneve: World Health Organization; 2011 Sep. as pistachio on health and lipid profile, and 209 p. diseases such diabetes, metabolic syndrome, 4. Sari I, Baltaci Y, Bagci C, Davutoglu V, Erel CHD, cancer, inflammatory diseases, and MS. O, Celik H, et al. Effect of pistachio diet on It is commonly believed that pistachios can be lipid parameters, endothelial function, inflammation, and oxidative status: a used to prevent and treat these diseases. As prospective study. Nutrition 2010; 26(4):399- previously discussed in this article, pistachio 404. has anti-inflammatory effects; therefore, 5. Damasceno NR, Perez-Heras A, Serra M, consuming pistachios could be helpful in the Cofán M, Sala-Vila A, Salas-Salvadó J, et al. Crossover study of diets enriched with virgin improvement of metabolic syndrome olive oil, walnuts or almonds. Effects on lipids complications. and other cardiovascular risk markers. Nutr Pistachios can delay gastric emptying time Metab Cardiovasc Dis 2011; 21(1):S14-20. which could result in a prolonged digestion 6. McKiernan F, Lokko P, Kuevi A, Sales RL, process and reduced feeling of hunger, which Costa NM, Bressan J, et al. Effects of processing on body weight and fasting plasma may manage weight well. Pistachio contains lipids. Br J Nutr 2010; 104(3):418-26. essential unsaturated fatty acids, fiber, 7. Colpo E, Vilanova CD, Brenner Reetz LG, antioxidants, and many nutrients. Thus, if Medeiros Frescura Duarte MM, Farias IL, taken adequately and frequently, it improves Irineu Muller E, et al. A single consumption of high amounts of the Brazil nuts improves lipid health. However, it seems that pistachio may profile of healthy volunteers. J Nutr Metab have anti-inflammatory, anti-diabetic, anti- 2013; 2013:653185. doi:10.1155/2013/653185 hyperlipidemic, and anti-proliferation effects. 8. Baynes JW. Role of oxidative stress in Further studies on pistachio are suggested in development of complications in diabetes. order to understand whether this nut can be Diabetes 1991; 40(4):405-12. 9. Goldin A, Beckman JA, Schmidt AM, Creager recommended for the prevention, MA. Advanced glycation end products:

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