Food as Medicine: Pistachio (Pistacia vera, Anacardiaceae)

HerbalEGram: Volume 15, Issue 3, March 2018 Editor’s Note: Each month, HerbalEGram highlights a conventional food and briefly explores its history, traditional uses, nutritional profile, and modern medicinal research. We also feature a nutritious recipe for an easy-to-prepare dish with each article to encourage readers to experience the extensive benefits of these whole foods. With this series, we hope our readers will gain a new appreciation for the foods they see at the supermarket and frequently include in their diets. The basic materials for this series were compiled by dietetic interns from Texas State University in San Marcos and the University of Texas at Austin through the American Botanical Council’s (ABC’s) Dietetic Internship Program, led by ABC Education Coordinator Jenny Perez. We would like to acknowledge Perez, ABC Special Projects Director Gayle Engels, and ABC Chief Science Officer Stefan Gafner, PhD, for their contributions to this project. By Hannah Baumana and Erika Martinezb a HerbalGram Associate Editor b ABC Dietetics Intern (Texas State, 2017) Overview The pistachio (Pistacia vera) is the only commercially grown species in its genus, which belongs to the Anacardiaceae family. Members of the genus Pistacia are among the oldest flowering nut trees and are small to medium in size, and characterized by their ability to exude mastic (plant resin).1,2 Other economically important plants in Anacardiaceae include cashew (Anacardium occidentale) and mango (Mangifera indica). Pistachio trees are temperate, deciduous trees adapted to the dry, hot, drought-prone climates of the Middle East.1,2,3 The pistachio tree can grow to a height of 10 meters (about 33 feet) and has pinnately compound leaves containing three to seven leaflets.3,4 The trees are dioecious; both male and female Pistacia verapistachio trees produce their own flowers.4 Female trees are wind-pollinated and produce green and brown flowers with no petals during the early summer.1,5 Female pistachio trees produce clusters of nuts, botanically known as drupes, after being pollinated by a nearby male tree.1 The pistachio tree matures at a slow pace and typically bears fruit after seven to 10 years.1,5 Similar to almonds and other drupes, the pistachio fruit matures in clusters that resemble grapes. Pistachio fruit has multiple parts: the nutmeat (kernel), which is enclosed in a thin, hard shell (endocarp) surrounded by a fleshy hull (mesocarp and exocarp).1 By the beginning of fall, the pistachio nuts are ripe and their hulls begin to crack open, revealing the pistachio kernels inside.5 Pistacia vera cultivars are currently grown in many temperate parts of the world, including Mexico, Israel, Australia, California, Italy, Greece, North Africa, and South Africa.3,4 In 2014, pistachio nuts represented 6% of the world’s total production of tree nuts.2 Iran and California produce the majority of the global supply of pistachio nuts.3 California, Arizona, and New Mexico comprise all of the commercial pistachio production in the United States, with California producing 99% of the total 312,000 acres planted.6 In 1976, the first commercial crop of pistachios in the United States was 1.5 million pounds and has dramatically increased to a record 2016 crop of more than 900 million pounds. Phytochemicals and Constituents The pistachio nut is nutrient-dense with less fat than other nut varieties. The nut has a total fat content of 12.7 g per ounce, of which 1.5 g is saturated fat (SF), 3.8 g is polyunsaturated fatty acids (PUFAs), and 6.7 g is monounsaturated fatty acids (MUFAs).3 Oleic acid, a MUFA, and linoleic acid, a PUFA, make up approximately 88% of the fatty acid profile. The high concentrations of unsaturated fatty acids and low concentration of saturated fat in pistachios may be associated with cardioprotective effects.3,7 The nut also contains protein and all nine essential amino acids, which is of particular importance for those who follow vegetarian and vegan diets.7 Moreover, pistachios are a good source of insoluble fiber, making up 80% of the total fiber content per ounce.3 Pistachio’s vitamin content includes fat-soluble vitamins A, C, E, and K, as well as many B vitamins: thiamin (B1), riboflavin (B2), niacin (B3), pantothenic acid (B5), and pyridoxine (B6).5,7 The thiamin content found in pistachios is relatively high.7 Pistachio is a good source of vitamin K, which is necessary for good bone health. Clinical studies have demonstrated that intake of vitamin K may result in decreased incidences of type 2 diabetes mellitus, cancer, and cardiovascular disease (CVD). Pistachio nut also provides an array of minerals including potassium, magnesium, calcium, copper, manganese, zinc, and selenium.7 The potassium content in pistachios may be helpful in stabilizing blood pressure in hypertensive subjects, as maintaining a healthy sodium-potassium ratio can help offset the hypertensive effects of sodium. Zinc and selenium are two important minerals with distinct antioxidant properties that may play a role in reducing the incidences of CVD and certain forms of cancer. Researchers have isolated and identified several bioactive compounds in pistachios including cholesterol-lowering phytosterols, carotenoids, phenolic compounds, and γ-tocopherol.7 In comparison with similar portions of other nuts, pistachios contain higher amounts of phytosterols per one-ounce serving.3 These include in beta-sitosterol, stigmasterol, and campesterol.7,8 The chemical structures of phytosterols resemble cholesterol, and they may interfere with its absorption.3 Pistachio’s distinctive green color is imparted by the carotenoids lutein and zeaxanthin; these carotenoids are found in high concentrations within the retina, and dietary intake may help protect the eye from oxidative damage and delay age-related vision degeneration.7,9 γ-tocopherol, a powerful antioxidant, targets reactive nitrogen species and may reduce inflammation by inhibiting the activity of the enzyme cyclooxygenase-2 (COX-2).3 Pistachio also contains phenolic compounds, including anthocyanins, proanthocyanidins, gallic acid, ellagic acid, flavonoids, phenolic acids, and stilbenes.10 However, the majority of the phenolic compounds are more concentrated in the inedible hulls than in the pistachio kernel.7 Historical and Commercial Uses The pistachio tree is native to central and southwest Asia.11 Archeological evidence suggests that humans were consuming pistachios in what is now modern-day Turkey by 7,000 BCE, and pistachio trees were cultivated in the gardens of Babylon under the rule of King Merodach-Baladan II around 700 BCE.3 A legend about the Queen of Sheba holds that she confiscated all of Assyria’s pistachio nuts for her personal consumption, declaring them an exclusive royal delicacy.3,5 Couples in Persia would stand underneath pistachio trees by the moonlight in order to listen to the sound of cracking pistachio shells, which was considered a symbol of prosperity.5 By the first century CE, Syrian trade introduced pistachios to the Romans,5 who transported pistachios throughout the Mediterranean and across the Asian continent to China. By the 16th century, pistachios were introduced to England. In 1854, the pistachio arrived in the United States as an experiment directed by a seed supplier named Charles Mason, and in 1875, American botanist William Whitehouse successfully cultivated pistachio from seed and developed the “Kerman” variety in California.5,11,12 Kerman pistachio trees were later commercially planted throughout California during the 1960s and early 1970s, where they remain a successful food crop.3 Consumption of pistachio nuts has been mentioned as a traditional folk remedy in Jordanian folk medicine to treat jaundice.5 They also were consumed in traditional Iranian medicine to treat hepatic, renal, cardiovascular, and respiratory diseases.12 Some evidence suggests that pistachios were consumed to treat bruises, chest pain, circulatory disorders, rheumatism, and liver sclerosis.13 Other records indicate that pistachios were historically consumed to soothe tooth pain.14 In Assyria and Greece, the pistachio was used as a powerful aphrodisiac and consumed as a remedy to counteract the effects of animal venom.15 Other parts of the pistachio tree were used traditionally, as well. Some European and Middle Eastern countries used the resin from the trunk to stop heavy bleeding, and in India, the pistachio shells were used in the making and processing of hides.14 Iranians often use pistachio shells as compost and livestock feed.11 The oil from the pistachio nut is utilized in Iran for the manufacture of cosmetic products. Currently, pistachios are commercially harvested and processed, and available roasted, salted or unsalted, and flavored.3 Pistachios often are used in baked goods and as a flavoring for candies and ice cream.11 Pistachio nuts have also been gaining popularity as a source for nut butter. The nut’s complete amino acid profile has made pistachio a popular addition to vegan and vegetarian protein products such as powders, bars, and drink mixes. Modern Research The pistachio nut can be considered an important part of a balanced diet due to its nutritional profile. Emerging evidence suggests a correlation between the bioactive compounds found in pistachio and the prevention of chronic health conditions, including cardiovascular disease, diabetes, obesity, and cancer. Cardiovascular Disease A prospective, randomized, crossover human clinical trial replaced 15% of total fat calories in subjects’ diets with those provided by pistachio nuts.16 After four weeks, the subjects who consumed two to three ounces of pistachio nuts daily had significantly improved ratios of total cholesterol to high density lipoprotein (HDL) cholesterol, low-density lipoprotein (LDL) cholesterol to HDL cholesterol, and B-100 to A-1 (proteins associated with cholesterol levels) over baseline. Although the mechanism of action by which pistachio nuts can improve serum lipid levels is still unclear, researchers hypothesize that pistachio’s low saturated fat content, impressive mineral profile, and bioactive compounds, such as phytosterols, may have played a role in the reduction of cholesterol levels in the subjects.16 Diabetes In a randomized, controlled, crossover clinical trial, subjects diagnosed with prediabetes who consumed two ounces (57 g) of pistachio nuts daily for a period of four months displayed significant positive changes in LDL and HDL cholesterol levels compared to those who consumed a nut-free diet. Researchers also reported that subjects consuming the pistachio-supplemented diet displayed significantly lower fasting glucose levels and improved insulin resistance.17 Pistacia vera without shellsResearchers hypothesized that the consumption of pistachios can potentially impact insulin production by elevating the levels of glucagon-like peptide-1 (GLP-1), a hormone present in the stomach.17 GLP-1 modulates insulin release and inhibits the release of glucagon to stabilize glucose levels in the blood. The authors of this study found that the subjects who included pistachios in their diets exhibited a significant decrease in inflammatory markers, including oxidized LDL, fibrinogen, and platelet factor-4 (PF-4), when compared to control. The favorable changes in inflammatory markers can be explained by the elevated serum levels of lutein and γ-tocopherol (antioxidant substances found in high amounts in pistachios) in the participants from the pistachio group. Further studies are warranted specifically in the pre-diabetic population to validate a correlation between pistachio consumption and blood glucose management. Weight Management A randomized, isocaloric weight-loss trial compared weight loss and body mass index (BMI) measurements in overweight and obese participants who consumed either a serving of pistachios or a pretzel as a snack for a 12-week period.3 Although the participants from each group exhibited some level of weight loss, those who consumed the pistachio snack had a significantly higher reduction in body weight and BMI than the pretzel group. Furthermore, those in the pistachio group had significant reductions in serum triglyceride levels compared to the pretzel group. Researchers hypothesized that pistachio consumption increased feelings of fullness by stimulating satiety cues. Two studies have investigated the correlation between consuming pistachios in the shell versus shelled pistachios and the amount consumed. Both studies observed that participants consumed fewer calories when presented with pistachios in the shell, and researchers hypothesized that this result could be due to the visual representation of the shells left on the table as participants consumed the nuts. Researchers also noted that when participants had to take the time to open the shells, it appeared that on average, participants reported a 40% reduction in calories that would otherwise have been consumed if the participants were provided with the pistachio nuts without their shells.3 Other Uses Pistachio leaves, resin, and all parts of the nut have traditional medicinal uses, and modern in vitro studies suggest that these plant parts demonstrate anti-inflammatory, antioxidant, anti-microbial, and photoprotective activities.12 Recently, researchers have focused on the potential therapeutic properties of the pistachio hull and skin, both of which are often discarded byproducts of the commercial pistachio industry. When compared to other parts of the pistachio tree, the hull has higher levels of phenolic, antioxidant, and anti-mutagenic activity.12 Aqueous extracts of the pistachio hull have been analyzed for their ability to induce apoptosis (normal, pre-programmed cell death) as well as their cytoprotective effects and ability to prevent cell membrane peroxidation of both red and white blood cells.12,18 Pistachio hull extract is rich in flavonols (like quercetin), phenolic acids (like gallic acid), and flavan-3-ols (like catechin), and in vitro evidence has shown that pistachio hull extract can induce apoptosis in HepG2 cells. In vitro research also suggests that pistachio skin and hull extracts have photoprotective properties. Plant-derived phenols have been shown to exhibit photo- or UV-protective activity when taken orally or applied topically. There is evidence that anthocyanins, which accumulate in the pistachio skin in the presence of strong sunlight, can function as efficient UV-absorbing agents.19 In addition to the antioxidant properties of phenolic compounds, they also exhibit a significant anti-inflammatory effect. All of these factors support its potential use as a low-cost ingredient with high added value in UV-protective products. Consumer Considerations Studies have demonstrated that levels of all antioxidant and phenolic compounds present in pistachio nuts decrease when roasted, with the anthocyanin content being most significantly reduced by these post-harvest practices.20 These results indicate that the pistachio skin plays an important role in protecting the seed/kernel from becoming oxidized and rancid. Consumers should purchase raw pistachios in the shell in order to obtain the most nutrients from the nut. Like other tree nuts, pistachio nut can induce immunoglobulin E (IgE)-mediated allergic reactions in sensitized/allergic individuals, especially due to its genetic relationship to cashew nut.2 In terms of clinical presentation, allergic reactions to pistachio are typically immediate (within minutes after ingestion or contact) and can result in moderate-to-severe clinical symptoms, which may include hives, rash, eczema, lip swelling, vomiting, abdominal pain, nasal congestion, or hypotension.2 Another concern regarding consuming pistachio and other tree nuts is the potential post-harvest contamination with mycotoxins or aflatoxins. These are highly toxic secondary metabolites that are produced by Aspergillus fungal species common in hot, humid climate conditions.2 The most commonly affected tree nuts are almonds (Prunus dulcis, Rosaceae), hazelnuts (Corylus americana, Betulaceae), and pistachios. Aflatoxins are very resistant to the most common food processing techniques and present a potentially serious threat to both human and animal health. The maximum allowable amount of aflatoxin amounts on pistachio, almond, or hazelnut is 8-10 µg/kg of daily dietary exposure.21 The United States’ strict standards for aflatoxin contamination have significantly decreased consumer exposure to aflatoxins. Nutrient Profile22 Macronutrient Profile: (Per 1 ounce raw pistachios [approx. 49 kernels]) 159 calories 5.7 g protein 7.7 g carbohydrate 12.9 g fat Secondary Metabolites: (Per 1 ounce raw pistachios [approx. 49 kernels]) Excellent source of: Vitamin E: 6.83 mg (45.5% DV) Vitamin B6: 0.5 mg (29.4% DV) Thiamin: 0.25 mg (20.8% DV) Very good source of: Manganese: 0.3 mg (13% DV) Vitamin A: 635 IU (12.7% DV) Phosphorus: 139 mg (11.1% DV) Dietary Fiber: 3 g (10% DV) Good source of: Magnesium: 34 mg (8.1% DV) Potassium: 291 mg (6.2% DV) Iron: 1.1 mg (6.1% DV) Also provides: Riboflavin: 0.05 mg (3.9% DV) Folate: 14 mcg (3.5% DV) Vitamin K: 3.7 mcg (3.1% DV) Niacin: 0.4 mg (2.5% DV) Calcium: 30 mg (2.3% DV) Vitamin C: 1.6 mg (1.8% DV) DV = Daily Value as established by the US Food and Drug Administration, based on a 2,000-calorie diet. Recipe: Chickpea and Pistachio Salad with Citrus Vinaigrette Adapted from Cooking for 223 Ingredients: 3 tablespoons orange juice 3 tablespoons extra virgin olive oil 1 tablespoon lime juice 1 small garlic clove, minced 1/4 teaspoon ground cumin (Learn more about the benefits of cumin here.24) 1/8 teaspoon cayenne pepper 1 15-ounce can of chickpeas, drained and rinsed (Learn more about the benefits of chickpea here.25) 3 radishes, thinly sliced One carrot, shredded or finely chopped (Learn more about the benefits of carrot here.26) 2 green onions, thinly sliced 1/4 cup pistachios, chopped 1/3 cup chopped parsley 3 cups salad greens Directions: Whisk the first six ingredients together. Season with salt to taste. In a medium bowl, combine dressing, chickpeas, radishes, carrot, green onions, pistachios, and parsley and stir gently. Serve over salad greens. Image captions/credits (top to bottom): Pistacia vera nuts in the shell “Kerman” variety pistachio nuts at Springs Preserve in Las Vegas, Nevada; photo courtesy of Stan Shebs Shelled and blanched pistachio nuts References Ferguson L, Polito V, Kallsen C. The pistachio tree; botany and physiology and factors that affect yield. Most. 1980:31-39. Costa J, Silva I, Vicente AA, Oliveira MBPP. Pistachio nut allergy: an updated overview. Crit Rev Food Sci Nutr. 2017;19:1-17. doi:10.1080/10408398.2017.1379947. Dreher ML. Pistachio nuts: Composition and potential health benefits. Nutr Rev. 2012. doi:10.1111/j.1753-4887.2011.00467.x. Van Wyk B-E. Food Plants of the World. Portland, OR: Timber Press; 2006. Murray M. The Encyclopedia of Healing Foods. New York, NY: Atria Books; 2005. American Pistachio Growers. The Power of Pistachios: History. American Pistachio Growers website. Available at: www.americanpistachios.org/power-of-pistachios/history. Accessed February 8, 2018. 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United States Department of Agriculture. Basic Report: 12151, Nuts, pistachio nuts, raw. National Nutrient Database for Standard Reference Release 28. May 2016. Available at: https://ndb.nal.usda.gov/ndb/foods/show/3687. Accessed February 26, 2018. Chickpea crab salad with citrus vinaigrette. Cooking for 2. 2008(Summer):31. Available at: www.tasteofhome.com/recipes/chickpea-crab-salad-with-citrus-vinaigrette. Accessed February 26, 2018. Bauman H, Woo T. Food as Medicine: Cumin (Cuminum cyminum, Apiaceae). HerbalEGram. 2016;13(10). Available at: http://cms.herbalgram.org/heg/volume13/10October/FAMCumin.html. Accessed February 26, 2018. Bauman H, Houck M. Food as Medicine: Chickpea (Cicer arietinum, Fabaceae). HerbalEGram. 2015;12(11). Available at: http://cms.herbalgram.org/heg/volume12/11November/FoodAsMedicine_Chickpea.html. Accessed February 26, 2018. Bauman H, MacLean K. Food as Medicine: Carrot (Daucus carota, Apiaceae). HerbalEGram. 2014;11(12). Available at: http://cms.herbalgram.org/heg/volume11/12December/December2014FaMcarrots.html. Accessed February 26, 2018.