Pistachio as a Regular Food | Encyclopedia MDPI

Pistachio as a Regular Food: Comparison

Please note this is a comparison between Version 1 by Luis Goya and Version 3 by Lindsay Dong.

The pistachio is regarded as a relevant source of biologically active components that, compared to other nuts, possess a healthier nutritional profile with low-fat content composed mainly of monounsaturated fatty acids, a high source of vegetable protein and dietary fibre, remarkable content of minerals, especially potassium, and an excellent source of vitamins, such as vitamins C and E. A rich composition in terms of phytochemicals, such as tocopherols, carotenoids, and, importantly, phenolic compounds, makes pistachio a powerful food to explore its involvement in the prevention of prevalent pathologies.

pistachio
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nutritional value
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1. Nutritional Value of Pistachios

The pistachio is a low-water (3–6%) and nutritionally rich nut mainly because of its high fat (48–63%) and protein concentration (18–22%), together with the dietary fibre (8–12%; Table 1) ^[1][2][14,15]. In fact, the daily intake of nuts recommended (1.5 oz equivalent to 42.5 g; 4) in the form of pistachios is approximately 15% of the Dietary Reference Intake (DRI) for proteins, 11–18% of DRI for male and female respectively for dietary fibre, and 24% of DRI for fat. Lipids, although present in great amounts, have an equilibrated content of mono- (56–77%) and polyunsaturated (14–33%; Table 1) fatty acids, that may help to reduce LDL-cholesterol and hence the coronary heart disease risk ^[3][4][5][2,16,17].

Table 1. Composition (g/100 g) in nutrients of dry roasted nuts. Source: USDA National Nutrient Database for Standard Reference (2020). MUFA: monousaturated fatty acids; SFA: saturated fatty acids; PUFA: polyunsaturated fatty acids.

g/100 g	Pistachio	Walnut	Almond	Hazelnut

^[9][23] (Table 2).

Table 2.

Total phenolic content and antioxidant activities of different varieties of pistachios.

Type of Pistachio	Status of Pistacho	TPP	Antioxidant Assay	Value of Antioxidant Capacity	References
Water	1.85
Larnaka (Spanish cultivar)	Natural	4.39	2.41	2.52
4900 mg/Kg fw	ORAC	330 mmol of TE/Kg	^[	¹⁰	^]	[24]	Energy (Kcal)	572	643	598	646
			DPPH	35 mmol of TE/Kg		Lipids	45.82	60.71	52.54	62.40
Kastel (Spanish cultivar)	Natural	1600 mg/Kg fw	ORAC	89 mmol of TE/Kg	^[10]	[24]	SFA	5.64	5.36	4.10	4.51
			DPPH	13 mmol of TE/Kg		PUFA	13.35	44.18	12.96	8.46
Kerman (Spanish cultivar)	Natural	1900 mg/Kg fw	ORAC	61 mmol of TE/Kg	^[10]	[24]	MUFA	24.53	8.37	33.08	46.61
			DPPH	10 mmol of TE/Kg		C16:0	8.0–13.0	6.0–8.0	4.0–13.0	4.0–9.0
Uzun (Turkish cultivar)	Natural	26.2 mg/100 g fw	DPPH	8.05 μmol of TE/g	^[11]	[27]	C18:0	0.5–2.0	1.0–3.0
	Roasted	2.0–10.0	1.0–4.0
32.4–42.4 mg/100 g fw	DPPH	C16:1	0.5–1.0	0.1–0.2	0.2–0.6	0.1–0.3
C18:1	45.0–70.0	13.0–21.0	48.0–80.0	66.0–85.0
C18:2	16.0–37.0	54.0–65.0	15.0–34.0	5.7–25.0
C18:3	0.1–0.4	13.0–14.0	N.D.	0.0–0.2
Proteins	21.05	14.29	20.96	15.03
Carbohydrates	28.28	17.86	21.01	17.60
Fiber	10.30	7.10	10.90	9.40
Sugars	7.74	3.57	4.86	4.89

Dry roasted pistachios have a lower fat content (45.82 g/100 g) than other nuts (Table 1), mainly monounsaturated fatty acid (24.53 g) followed by polyunsaturated fatty acid (13.35 g) and saturated fatty acid (5.64 g). Of the fatty acids, oleic is the main monounsaturated fatty acid (MUFA) in pistachios followed by linoleic acid (C18:2), which represents more than half of the total fatty acid content (<60 g) (Table 1). Pistachio shows a similar lipid profile to almonds and hazelnuts while walnut fat is headed by linoleic acid (54.0–65.0 g/100 g) followed by oleic (C18:2) and linolenic (C18:3) acids with similar contents. Pistachios are also a worthy source of vegetable protein (about 21%) as almonds (21%), and higher than other nuts, such as hazelnuts and/or walnuts. The amount of total carbohydrates is low to moderate (28%), but pistachios are rich in dietary fibre, mainly insoluble fibre (about 10% versus less than 1% of soluble fibre). Pistachio also contains a remarkable content of minerals, such as magnesium, calcium, potassium, and phosphorus, and is documented as an important dietary source of potassium (1025 mg/100 g versus ~700 mg of almond and hazelnut or 450 mg of walnut per 100 g dry roasted nuts). Pistachios are rich in vitamins, especially vitamins C (5.60 mg/100 g) and E (mainly as γ-tocopherol) (2.17 g/100 g). Others, such as vitamin A, vitamin B (except B12), vitamin K, and folate, are existent in pistachios, which could contribute to their respective Recommended Dietary Allowance (RDA).

2. Antioxidant Phenolic Composition of Pistachios

Nutrient databases, like the Phenol-Explorer and the flavonoid and proanthocyanidin databases (USDA) ^[6][7][21,22] report the content of polyphenol of many foods. Furthermore, the concentration of various families of phenolic components in nuts, including pistachio, as well as their antioxidant capacity and evidence for healthy effects have been recently summarizeviewed ^[8][9][1,23]. Walnuts, pecans, and pistachios are the kinds of nuts with the higher phenolic amounts, on the contrary almonds, peanuts, and hazelnut present lower levels (e.g., ^[8][9][1,23]. A variety-dependent content of total polar phenolics (TPP) is found in pistachios, ranging from 1600 mg/kg for the Kastel cultivars to more than three times more, 4900 mg/kg for Larnaka. As reported, polar phenolic components can be grouped into different families. Flavanols being the most abundant phenolics found (about 90% of total, from 1500 mg/kg to 4500 mg/kg), whereas the Kastel and Larnaka cultivars showed the lowest and highest concentrations, respectively ^[10][24]. Other families, e.g., anthocyanins (from 54 to 218 mg/kg), flavonols (from 76 to 130 mg/kg), flavanones (from 12 to 71 mg/kg), and gallotannins (from 4 to 46 mg/kg), are also measured. These findings are similar to those reported by Alasalvar & Bolling ^[8][1] or Chang et al.

9.76–11.5 μmol of TE/g
^[
¹¹
^]
[
27
]
Ohadi (Turkish cultivar)	Natural	9.23–10.55 mg/Kg GAE	DPPH	4.34–5.56 mmol TE/Kg	^[12]	[28]
			ABTS	4.11–5.95 mmol TE/Kg	^[12]	[28]
	Roasted	10.35–11.23 mg/Kg GAE	DPPH	3.53–6.32 mmol TE/Kg	^[12]	[28]
			ABTS	5.80–7.35 mmol TE/Kg	^[12]	[28]
Uzum (Turkish cultivar)	Natural	9.19–11.46 mg/Kg GAE	DPPH	7.16–13.58 mmol Trolox/Kg	^[12]	[28]
			ABTS	15.69–28.28 mmol Trolox/Kg	^[12]	[28]
	Roasted	10.46–12.73 mg/Kg GAE	DPPH	13.5–18.00 mmol Trolox/Kg	^[12]	[28]
			ABTS	26.81–35.86 mmol Trolox/Kg	^[12]	[28]

DPPH: 2,2′-diphenyl-1-picrylhydrazyl; FRAP: ferric reducing antioxidant power; ABTS: 2,2′-azino-bis(3-ethylbenzthiazoline-6-sulphonic acid); ORAC: Oxygen radical absorbance capacity; TPP: total polar phenolics; fw: fresh weight; GAE: gallic acid equivalent; TE: trolox equivalent.

3. Health Benefits of Pistachio Consumption

Pistachios have an exciting nutritional profile compared with the rest of the nuts due to their lower energy content and highest levels of γ-tocopherol, phytoesterols, carotenoids, minerals, such magnesium and potassium, and vitamins K and B. The nutrients mentioned above undoubtedly contribute to the evidence that the regular intake of pistachios improves health ^[2][15]. Cardiometabolic disease involves dyslipidemia, insulin resistance, hypertension, and excessive visceral fat, which are behind T2DM and CVD ^[13][30]. Epidemiological and/or clinical trials have shown that nut consumption has a positive influence on health, by reducing the risk of suffering CVD ^[2][14][15][15,31,32], hypertension ^[16][33], T2DM ^[17][34] and obesity ^[18][35], among others. These beneficial effects are a consequence of their unique composition since nuts are nutrient-dense foods with healthy MUFA and PUFA fatty acid composition, dietary fibre, high-quality vegetable protein, vitamins, and minerals, along with carotenoids, phytosterols, and phenolic compounds previously described, with recognized benefits to human health ^{[19][20][21][22]}[3,10,11,36]. Regarding pistachio, there is wide evidence confirming its beneficial health effects and, particularly, its positive contribution to minimizing the risk for CVD ^[20][21][10,11].

3.1. Effects of Pistachio Consumption on Blood Lipids

4.1. Effects of Pistachio Consumption on Blood Lipids

Hyperlipemia is an established risk for CVD. Pistachio intake has been related with the improvement of lipid profile, decreasing total cholesterol (TC) concentration ^{[23][24][25][26]}[37,38,39,40], TC/high-density lipoprotein (HDL) ratio and low-density lipoprotein (LDL)/HDL ratio ^{[23][24][25][27]}[37,38,39,41] in the pistachio-supplemented cluster compared with the control one, in both healthy ^[24][25][26][38,39,40] and patients with moderate hypercholesterolemia ^[23][27][37,41]. LDL concentrations also decreased significantly in the pistachio-supplemented group in some studies ^[25][26][28][39,40,42], whereas others observed a non-significant reduction ^[23][24][29][37,38,43]. Additionally, Sheridan et al. ^[27][41] observed a significant increase in circulating HDL concentration in those subjects who consumed pistachios. Recently, a systematic review of epidemiological evidence developed by Lippi et al. ^[30][44] showed the beneficial effects of pistachio intake for improving the blood lipid profile (Figure 1).

Figure 1.

Health benefits of pistachio consumption.

3.2. Effects of Pistachio on Blood Pressure and Endothelial Function

4.2. Effects of Pistachio on Blood Pressure and Endothelial Function

Several prospective studies have revealed an inverse relationship between nut consumption and blood pressure (BP) or hypertension. In the particular case of pistachio, a beneficial effect on BP has also been observed in a clinical trial conducted on 28 dyslipidaemic individuals who followed for four weeks either a low-fat control diet, a diet having 10% of the total energy from pistachios, or a diet with 20% of the total energy from pistachios. A significant systolic blood pressure (SBP) reduction was observed, particularly after following the diet supplemented with 10% of the total energy as pistachios, thus, no dose-dependent effect was observed. In addition, no difference in diastolic blood pressure (DBP) was recorded ^[31][49]. Another more recent study conducted on T2DM subjects by Sauder et al. ^[32][50] showed a decrease in SBP after consuming a diet with 20% energy from pistachios for four weeks. However, three additional controlled feeding trials evaluated the BP lowering effects of pistachios as a secondary outcome and non-significant differences in both SBP and DBP between those subjects supplemented or un-supplemented with pistachios were observed ^[26][27][33][40,41,51]. Finally, a recent review and meta-analysis of more than 20 RCTs found that despite the intake of mixed nuts may reduce DBP, pistachios seemed to have the most potent effect on reducing both DBP and SBP ^[16][33]. Therefore, although there is some evidence that suggests that pistachios may reduce BP the non-consistent results encourage continuing to investigate this aspect (Figure 1).

3.3. Effects of Pistachio on Glucose Metabolism

4.3. Effects of Pistachio on Glucose Metabolism

In recent years, animal studies have unequivocally shown the positive effect of pistachio feed on glucose homeostasis in altered situations such as diabetes and metabolic syndrome (MetS). Thus, the consumption of pistachio has favorable effects on avoiding hypertriglyceridemia, hyperglycemia, hypercholesterolemia, and inflammation characteristic of a MetS induced by a fructose overload ^[34][61]. Recently, the pistachio extract administered to diabetic rats for three weeks significantly improved the lipid profile, oxidative stress, and inflammation process by reducing lipid peroxidation and increasing total antioxidant capacity ^[35][62]. In the same year, a pistachio hull hydro-alcoholic extract, along with aerobic exercise, improved passive avoidance memory in streptozotocin-induced diabetic rats ^[36][63]. More recently, a pistachio extract also reverted most parameters altered by streptozotocin-induced diabetes in rats; not only markers related to glucose homeostasis, but also those associated to ovary damage and oxidative stress ^[37][64].

3.4. Effects of Pistachios on Satiety Regulation and Body-Weight Control

4.4. Effects of Pistachios on Satiety Regulation and Body-Weight Control

Although nuts, including pistachios, are still perceived by the general public to be fattening because of their high-fat content, there are several epidemiological studies that have provided strong evidence that nut consumption is associated with neither weight gain nor an increased risk of obesity ^[38][39][83,84]. Regarding pistachio, Li et al. ^[40][85] evaluated the effects of pistachio snack consumption on body weight and lipid levels in obese participants, which were randomly assigned to consume isocaloric weight reduction diets for 12 weeks with an afternoon snack of either 53 g of salted pistachios or 56 g of salted pretzels. Both groups lost weight, but the pistachio-supplemented group showed a higher BMI reduction than the pretzel-supplemented group. Among the various explanations of why the consumption of pistachios does not induce overweight, being a very energetic food, is their high satiating power, inefficiency in the absorption of the energy they contain, a possible increment in energy expenditure at rest and an increase in fat oxidation (revised by Tan et al. ^[39][84]). Moreover, the crunchy physical structure of nuts in general, and pistachio in particular, has demonstrated its positive influence on satiety ^[41][88]. In this sense, recently, a randomized controlled pilot study was carried out to assess the effects of a daily pistachio afternoon snack on next-meal energy intake, satiety and anthropometry in 30 healthy French women were tutored to consume either 56 g of pistachios or 56 g of isoenergetic/equiprotein savoury biscuit as an afternoon snack. Results revealed that both afternoon snacks provided a similar subjective feeling of satiety, and pistachios consumption did not affect body weight or composition ^[42][89]. Lately, pistachio treatment in obese mice fed a high-fat diet showed neuroprotective effects, including decreased brain apoptosis, decreased brain lipid, and oxidative stress with the improvement of mitochondrial function ^[43][90]. A recent meta-analysis of RCTs by Xia et al. ^[44][91] reported that a diet with pistachios reduced BMI and had no significant effects on body weight and waist circumference. Indeed, recent research has focused on pistachio’s applications as a plant-based snack, particularly for appetite control and healthy weight management ^[45][92]. Due to the importance of satiety regulation on body-weight control, clinical trials with pistachios need to be carried out in the future to establish this aspect fully.

3.5. Effect of Pistachios on Inflammatory State

4.5. Effect of Pistachios on Inflammatory State

Chronic low-grade inflammation has been related with insulin resistance, diabetes, atherosclerosis, obesity and MetS. A few research studies have evaluated the effects of nut intake on inflammation with different results. A previous study suggested that a diet supplemented with pistachio improved some inflammation biomarkers in healthy young men; by decreasing serum interleukin 6 but without changing CRP and tumour necrosis factor-alpha (TNFα) levels ^[26][40]. Recently, proanthocyanidins extracted from Sicilian pistachio was the major bioactive able to modulate the inflammatory response of human intestinal epithelial cells through the inhibition of nuclear factor kappa B (NF-κB) activation ^[46][93]. More recently, the anti-inflammatory effect in vivo of pistachio was shown in a rat model of ulcerative colitis inflammation ^[47][94]. In the same year, the results of another study showed that usual pistachio intake improved inflammation in obese mice, probably due to the positive modulation of the microbiota composition ^[48][95]. More recently, an aqueous leaf extract obtained from Pistacia lentiscus improved acute acetic acid-induced colitis in rats, which was associated with its ability to reduce inflammation and oxidative stress ^[49][96] (Figure 1).

3.6. Effects of Pistachios on Oxidative Stress

4.6. Effects of Pistachios on Oxidative Stress

Pistachios contain polyphenols that act as radical scavengers, neutralising reactive oxygen species (ROS) and enhancing endogenous antioxidant defences. Many studies have demonstrated the antioxidant activity of extracts obtained from different pistachio parts in both in vitro ^{[50][51][52][53][54]}[97,98,99,100,101] and in vivo models, such as in animals ^{[37][50][52][55][56][57][58][59][60][61]}[64,97,99,102,103,104,105,106,107,108] and humans ^{[2][62][63][64][65][66]}[7,15,54,55,76,109]. Therefore, antioxidants present in pistachios could have significant effects on the regulation of oxidative stress and a reduced risk of chronic diseases. Remarkably, previous research on the antioxidant capacity and chemo-preventive potential of pistachio phenolic compounds in cell culture models has been performed in cell types from thyroid, lung, skin, and monocyte/macrophage, but not in endothelial cells, which is the more suitable cell type to study endothelial dysfunction and its potential effect on cardiovascular capacity.

3.7. Effects of Pistachios on Cancer

4.7. Effects of Pistachios on Cancer

In cell culture studies, mastic gum resin has shown anticancer effect in bile duct cancer (cholangiocarcinoma) (KMBC), pancreatic carcinoma (PANC-1), gastric adenocarcinoma (CRL-1739), and colonic adenocarcinoma (COLO205) cells ^[67][112]. P. lentiscus extract showed moderate activity against liver cancer ^[68][113] as well as breast cancer ^[69][70][114,115]. Raw and roasted pistachio showed a chemo-preventive potential regarding colon cancer ^[71][116]. The essential oil from Pistacia lentiscus aerial parts induced oxidative stress and apoptosis in human thyroid carcinoma cells ^[51][98]. Pistachio green hull extract induced apoptosis through multiple signaling pathways by causing oxidative stress on colon cancer cells ^[72][117]; whereas the cytotoxic fraction from Pistacia vera red hull ethyl acetate extract showed anticancer activity on breast cancer both in cell culture and in mice ^[73][118]. Mastiha is a natural aromatic resin obtained from the trunk and branches of the mastic tree (Pistacia lentiscus L. var latifolius Coss or Pistacia lentiscus var. Chia). Similar to the results reported with green hull extracts by Koyuncu and coworkers, mastic has shown a powerful anticancer effect in colon cancer cells ^[74][119].

3.8. Effect of Pistachios on Intestinal Microbiota

4.8. Effect of Pistachios on Intestinal Microbiota

Dietary fibre and phytochemicals present in nuts can reach the proximal colon and modulate the microbiota composition. Effects of almond and pistachio consumption on gut microbiota composition were evaluated in a crossover RCT for 18 days with 0, 1.5, and three servings/day. Pistachio showed a higher effect than almond on gut microbiota, increasing the number of potentially beneficial butyrate-producing bacteria, whereas bifidobacteria were unaffected ^[75][126]. A more recent study led by Yanni et al. ^[76][127] in diabetic rats demonstrated that dietary pistachio for four weeks restored normal flora and enhanced the presence of beneficial microbes (lactobacilli and bifidobacteria, among others) in the rat model of streptozotocin-induced diabetes. Likewise, chronic intake of pistachio for 16 weeks significantly enhanced the level of healthy bacteria genera such as Parabacteroides, Dorea, Allobaculum, Turicibacter, Lactobacillus, and Anaeroplasma, and decreased bacteria related to inflammation, such as Oscillospira, Desulfovibrio, Coprobacillus, and Bilophila in mice fed a high-fat diet ^[48][95].

4. Conclusions

The pistachio is valued as an important source of bioactive components that, compared to other nuts, possesses a healthier nutritional profile with low-fat content composed mainly of MUFA, a high source of vegetable protein and dietary fibre, remarkable content of minerals, especially potassium, and an excellent source of vitamins, such as vitamins C and E. Its phytochemicals rich composition such as tocopherols, carotenoids and, importantly, phenolic compounds make pistachio an interesting food for its potential to prevent prevalent pathologies. The first health claim approved by the United States FDA in 2003 informed that there is scientific evidence that suggests, although does not demonstrate, that eating 1.5 oz (42.5 g) each day of nuts within a low saturated fat and cholesterol diet, may diminish the heart disease risk, was a turning point for nuts. A growing interest in confirming nuts effect on health has led to an increase in the quantity of research on nuts. Although pistachio has been less explored than other nuts (walnut, almonds, hazelnut, etc.), some studies provide evidence of its beneficial effects on CVD risk factors beyond the lipid-lowering effect. Different studies showed that diets supplemented with pistachios present a preventive effect to T2DM due to its effect of improving markers of glucose homeostasis, decreasing oxidative stress, alleviating post-prandial hyperglycemia and reducing the rate of gestational diabetes, among others. Regarding the most concern issue regarding pistachio intake, recent results showed neither weight gain nor obesity risk, but rather the opposite. A tendency to decrease and/or maintain weight as well as improve and/or maintain anthropometric parameters was observed and, in part, due to its positive effect on controlling appetite and enhancing satiety feeling, although more studies are needed to evaluate this aspect thoroughly. Likewise, the pistachio could play an important role in cancer prevention due to its ability to induce cytotoxicity and apoptosis in neoplastic cells, as well as the modulatory activity of signaling pathways involved in the regulation of cancer observed in carcinogenic cell models. The phytochemicals would be behind the demonstrated anti-inflammatory and antioxidant activities associated with pistachios, which would explain the ability to prevent the chronic diseases mentioned (CVD, T2DM, obesity, and cancer). Finally, there are more and more studies that inform about the pistachio’s ability to modulate the activity of gut microbiota, increasing the abundance of beneficial bacteria, although more studies are needed to gain robust conclusions.