2010 effect of pistachio diet on lipid parameters, endothelial function

Nutrition 26 (2010) 399–404
www.nutritionjrnl.com
Applied nutritional investigation
Effect of pistachio diet on lipid parameters, endothelial function,
inflammation, and oxidative status: A prospective study
Ibrahim Sari, M.D.a,*, Yasemin Baltaci, M.D.b, Cahit Bagci, M.D.b, Vedat Davutoglu, M.D.a,
Ozcan Erel, M.D.c, Hakim Celik, M.D.c, Orhan Ozer, M.D.a, Nur Aksoy, M.D.d,
and Mehmet Aksoy, M.D.a
a
Cardiology Department, Gaziantep University, School of Medicine, Gaziantep, Turkey
b
Physiology Department, Gaziantep University, School of Medicine, Gaziantep, Turkey
c
Biochemistry Department, Harran University, School of Medicine, Sanliurfa, Turkey
d
Biochemistry Department, Gaziantep University, School of Medicine, Gaziantep, Turkey
Manuscript received December 15, 2008; accepted May 30, 2009.

Abstract Objective: Recent studies have suggested that nuts have favorable effects beyond lipid lowering. We
aimed to investigate effect of the Antep pistachio (Pistacia vera L.) on blood glucose, lipid parameters,
endothelial function, inflammation, and oxidation in healthy young men living in a controlled
environment.
Methods: A Mediterranean diet was administered to normolipidemic 32 healthy young men (mean
age 22 y, range 21–24) for 4 wk. After 4 wk, participants continued to receive the Mediterranean
diet but pistachio was added for 4 wk by replacing the monounsaturated fat content constituting
z20% of daily caloric intake. Fasting blood samples and brachial endothelial function measurements
were performed at baseline and after each diet.
Results: Compared with the Mediterranean diet, the pistachio diet decreased glucose (P < 0.001,
À8.8 6 8.5%), low-density lipoprotein (P < 0.001, À23.2 6 11.9%), total cholesterol (P < 0.001,
À21.2 6 9.9%), and triacylglycerol (P ¼ 0.008, À13.8 6 33.8%) significantly and high-density
lipoprotein (P ¼ 0.069, À3.1 6 11.7%) non-significantly. Total cholesterol/high-density lipoprotein
and low-density lipoprotein/high-density lipoprotein ratios decreased significantly (P < 0.001 for
both). The pistachio diet significantly improved endothelium-dependent vasodilation (P ¼ 0.002,
30% relative increase), decreased serum interleukin-6, total oxidant status, lipid hydroperoxide, and
malondialdehyde and increased superoxide dismutase (P < 0.001 for all), whereas there was no
significant change in C-reactive protein and tumor necrosis factor-a levels.
Conclusion: In this trial, we demonstrated that a pistachio diet improved blood glucose level,
endothelial function, and some indices of inflammation and oxidative status in healthy young men.
These findings are in accordance with the idea that nuts, in particular pistachio nuts, have favorable
effects beyond lipid lowering that deserve to be evaluated with prospective follow-up studies.
Ó 2010 Published by Elsevier Inc.

Keywords: Pistachio; Endothelium; Lipid; Inflammation; Oxidation

Introduction (CHD). Compared with people who consumed nuts less
than one time per week, people who ate nuts at least five
Epidemiologic studies have shown that frequent nut times per week showed a 50% reduction in risk [1–4]. Nuts
consumption decreases the risk of coronary heart disease are rich in monounsaturated fatty acid (MUFA) and polyun-
saturated fatty acid (PUFA), which are known to have favor-
Financial support of the present study was provided by the Pistachio able effects on the lipid profile [5]. However, the potential
Investigation Group of the Gaziantep Chamber of Commerce. benefits of the nuts on decreasing CHD are not limited to their
*Corresponding author. Tel.: 90-342-360-6060; fax: 90-342-360-3928.
E-mail address: drisari@yahoo.com (I. Sari).
effects on lipid parameters. Nuts are also a good source of

0899-9007/10/$ – see front matter Ó 2010 Published by Elsevier Inc.
doi:10.1016/j.nut.2009.05.023

400 I. Sari et al. / Nutrition 26 (2010) 399–404

dietary fiber, vitamins, micronutrients, antioxidants, amino history of eating nuts frequently (more than once a week),
acids (e.g., arginine), and plant stenols [5]. a history of a food or nut allergy, regular use of any drugs
The majority of the nut studies were performed with wal- including vitamin supplements, and a history of any known
nuts, almonds, and peanuts. Thus far, to our knowledge, disease. Subjects with concomitant inflammatory diseases
only three studies have been conducted in humans investigat- such as infections, recent surgical procedures, or dyslipide-
ing the effects of pistachio nuts, which were performed as out- mia were also excluded from the study. Participants were
patient dietary intervention trials [6–8]. Investigators are more requested to abstain from coffee products and alcohol
focused on the favorable effects of nuts beyond their effects on consumption during the recruitment period. The study proto-
lipid parameters. Endothelial dysfunction is an early key event col was approved by the ethical committee of Gaziantep
in the atherosclerotic process that predicts future CHD devel- University and all participants gave informed consent.
opment [9,10]. Endothelial function measurement can be Participants were offered free pistachios but no monetary
non-invasively performed. A recent study has demonstrated compensation.
that substituting walnuts for MUFA in a Mediterranean diet
improved endothelium-dependent vasodilation (EDV) in hy- Protocol
percholesterolemic subjects as a measurement of endothelial
function [11]. Like the walnut, the pistachio is a good source Before the study, students were eating the same kind of
of L-arginine, which is a precursor of endogenous vasodilator regular diet (total energy from protein 20%, carbohydrate
nitric oxide. To our knowledge, there are as yet no data regard- 47%, and fat 33%) prepared in the school kitchen. Although
ing the effect of a pistachio diet on endothelial function. they were eating the same kind of food, the amount was not
Inflammation and oxidation play an important role in the standardized for each student. They were allowed to eat as
pathogenesis and progression of CHD. Some studies have much as they wanted if the food remained. To overcome
shown that nuts have favorable effects on inflammation and the disparities across the food intakes of the participants
oxidative status; however, our knowledge about the impact (amount, calories, proportions of protein, fat, carbohydrate,
of pistachios on inflammatory and oxidative balance is etc.), we accepted the recruitment period as a run-in period.
limited. In this study we therefore investigated the effect of A Mediterranean-type diet was administered for 4 wk. After
an Antep pistachio (Pistacia vera L.) diet on lipid parameters, 4 wk, the participants continued to receive the Mediterra-
endothelial function, inflammation, and oxidative status in nean-type diet but pistachio was added by replacing the
healthy young men living in a controlled environment, which MUFA content constituting z20% of daily caloric intake.
has not been studied previously. Because diet-induced lipoprotein changes stabilize in less
than 4 wk, we planned the diet periods as 4 wk [12]. The
protocol description was summarized in Table 1.
Materials and methods The Mediterranean-type diet was composed of natural
food stuff. It was rich in vegetable and fish, whereas red
Study population meat, fat products, and egg products were limited. The pista-
chio diet was similar to the Mediterranean-type diet, but
To our knowledge, previous nut studies were organized as pistachio partly replaced MUFA-rich foods. Prepackaged,
outpatient dietary modification studies. Although all of the roasted unsalted pistachios (60 to 100 g) were administered
previously published studies have reported good compliance as an appetizer during the second 4-wk period. In the pistachio
of the participants to the administered diet, we believe that diet, pistachio contributed z20% of total energy and replaced
subjects living in a controlled environment would provide 32% of the energy obtained from MUFAs in the control diet
a better sample population in a dietary intervention study.
After providing the required legal permissions, we performed
Table 1
the study in the vocational police education school of Gazian-
Protocol description in summary
tep, Turkey. In the vocational police education school of
Gaziantep, all students were living in a controlled environ- Weight, blood pressure, / 33 healthy young men living in
laboratory and endothelial a controlled environment
ment and eating in the same place. Sleeping and waking function measurements
hours and daily activities of the students were similar. They Mediterranean diet
were not allowed to go outside the school borders and they Y 4 wk
were not provided any additional food other than that served Weight, blood pressure, / Pistachio was added to the
during meal times, except unlimited water. laboratory and endothelial Mediterranean diet by
function measurements replacing 32% of energy
Thirty-three healthy students (mean age 22 y, range obtained by monounsaturated
21–24) were included in the study. All enrolled subjects fatty acid
were free of acute or chronic medical disorders and were of Y 4 wk
normal body habitus. All subjects underwent a detailed Weight, blood pressure, / 32 participants finished the
medical history and physical examination by the investigator laboratory and endothelial protocol
function measurements
physicians. Exclusion criteria were smoking any amount,

I. Sari et al. / Nutrition 26 (2010) 399–404 401

(Table 2). The pistachio diet was equivalent to the Mediterra- a 2% mean absolute difference in EDV and endothelium-
nean diet in total calory intake and proportions of carbohy- independent vasodilation as significant, 25 subjects would
drate and protein intakes; however, saturated fatty acid and need to complete the study.
PUFA intakes were lower (P ¼ 0.02 and P < 0.001, respec- The measurements were performed as previously
tively) and MUFA and fiber intakes were higher (P < 0.001 described [13]. The brachial artery was imaged longitudi-
and P < 0.001, respectively). According to the data provided nally, 2 to 5 cm above the antecubital crease. An occluding
by the Pistachio Investigation Institute, Gaziantep, the com- cuff placed proximally on the forearm was inflated to a pres-
position of 100 g of pistachio was 18.3 g of protein, 52.7 g sure of 200 mmHg for 5 min and rapidly deflated to induce
of fat (saturated fatty acid 6.7 g, MUFA 36.2 g, and PUFA reactive hyperemia. Brachial artery scans were obtained 30
9.8 g), 20 g of carbohydrate, and 7.4 g of fiber. s before cuff inflation (first baseline), at 60 to 90 s after
During the study period a registered dietitian supervised cuff deflation to assess EDV, after a 10-min rest (second
mealtimes and ensured the complete intake of the respective baseline), and 3 min after 0.4 mg of sublingual glyceryl trini-
meals. The components of the food during the study period trate to evaluate endothelium-independent vasodilation.
were prepared and served by a food company (Tam Sofra Arterial diameter was measured with ultrasonic calipers at
Inc., Gaziantep, Turkey) under the supervision of the regis- end diastole, incident with the R wave on the electrocardio-
tered dietitian. The participants ate their breakfast, lunch, gram. Three cardiac cycles were analyzed for each scan,
and dinner in the same field. Leftover foodstuffs were and measurements were averaged. Reliability of the measure-
collected and weighed by the dietitian to determine compli- ments was qualified by having them remeasure a random
ance. Any deviations from the study protocol were recorded sample of 15 subjects.
and reviewed by the investigators during the study.
Fasting blood sample collection, endothelial function, Laboratory measurements
body weight, and blood pressure measurements were
performed three times (during the run-in period, after 4 wk Venous blood samples of the participants were collected
[4 wk after the Mediterranean-type diet], and after 8 wk from the antecubital vein while patients rested in a supine
[4 wk after pistachio diet administration]). Because the position after an overnight fast. Serum and ethylenediaminete-
school program and the activities of the participants were pre- tra-acetic acid plasma samples were stored at À80 C and an-
planned for the entire education year, there was no change in alyzed at the end of the study period. Total cholesterol (TC),
daily activities of the participants during the study period. high-density lipoprotein (HDL), and triacylglycerol (TG)
levels were determined by enzymatic–colorimetric methods.
Endothelial function measurement Low-density lipoprotein (LDL) was calculated by the Friede-
wald formula. Oxidized LDL was calculated by a monoclonal
Endothelial function measurements were performed by the antibody–based immunoassay. Apolipoproteins (Apo) Al and
same examiner who was unaware of the stage of the study. B were determined by turbidimetry. Homocysteine was deter-
Each subject was studied in the morning hours (08:00 to mined by fluorescence polarization immunoassay.
10:00) after fasting 8 h before the examination. Studies High-sensitivity C-reactive protein (hs-CRP) was mea-
were performed in a quiet, semi-dark, temperature-controlled sured by chemiluminescent immunometric assay. Interleu-
room (20–25 C) with the subject lying in a supine position. kin-6 and tumor necrosis factor-a were determined by
Images were obtained using a commercially available device enzyme-linked immunosorbent assay. Total oxidant status
(Vivid 7, GE Vingmed Ultrasound AS, Horten, Norway) with (TOS) was determined as previously described [14]. Serum
a 12-MHz linear array transducer. According to the power cal- lipid hydroperoxide level was determined by the ferrous
culation, to provide 80% power at 5% significance to detect ion oxidation–xylenol orange method. Malondialdehyde
(MDA) was measured by a standard high-performance liquid
chromatographic method. Superoxide dismutase (SOD)
Table 2
Comparison of nutritional status of subjects during the Mediterranean and
levels were performed by a commercially available SOD
pistachio diets kit. All laboratory analyses were done in duplicate.
Variable Mediterranean diet Pistachio diet P
Statistical analysis
Total calories (kcal/d) 1966 6 224 1983 6 241 0.1
CHO (% energy) 48.7 6 3.2 49.2 6 2.8 0.1
Continuous variables are expressed as mean 6 standard
Protein (% energy) 17.1 6 1.5 16.8 6 1.7 0.1
Fat (% energy) 33.5 6 2.2 33.1 6 1.9 0.1 deviation and categorical data are expressed as percentages.
SFA 5.9 6 1.1 4.8 6 1.4 0.02 Two-tailed t test for paired samples was used to compare
MUFA 13.3 6 1.6 20.2 6 2.3 0.001 changes in outcome variables in response to diets. The differ-
PUFA 14.2 6 1.3 7.1 6 1.0 0.001 ences between the compositions of the Mediterranean and
Fiber (g) 6.4 6 2.1 11.3 6 2.4 0.001
pistachio diets were tested with unpaired t test or chi-square
CHO, carbohydrate; MUFA, monounsaturated fatty acid; PUFA, polyun- test. Because hs-CRP was highly skewed, a logarithmic
saturated fatty acid; SFA, saturated fatty acid. transformation was used to obtain a normal distribution


before analysis. Values were then transformed back and Discussion
reported in their original form for presentation. Two-tailed
P 0.05 was considered statistically significant. All statisti- In this 8-wk dietary intervention trial, we demonstrated
cal studies were carried out with SPSS 11.5 (SPSS Inc., that a pistachio diet had favorable effects on glucose level,
Chicago, IL, USA). lipid parameters, endothelial function, and some indices of
inflammation and oxidative status in healthy young men.
Results Most of the nut studies were performed with walnuts,
almonds, and peanuts. Thus far, to our knowledge, only three
Of the 33 participants initially included into the study, studies have been conducted in humans investigating the
1 subject had to undergo a urologic operation; therefore, effects of pistachio nuts, which were performed as outpatient
32 subjects (mean age 22 y, range 21–24) completed the pro- dietary intervention trials [6–8]. Therefore, we believe that
tocol. Table 3 presents body weight, blood pressure, glucose, our study is unique in its design because it was conducted
and lipid parameters of the participants at baseline and at the in a population living in a controlled environment. Previous
end of each diet. Body weight and blood pressure of the par- studies about the effect of pistachio on lipid parameters have
ticipants remained unchanged during the study. Compared shown favorable effects [6–8]. Edwards et al. [6] demon-
with the Mediterranean diet, the pistachio diet caused signif- strated that 3 wk of a pistachio diet caused significant
icant decreases in glucose levels (P 0.001, À8.8 6 8.5%). decreases in TC, TC/HDL ratio, and LDL/HDL ratio and
Pistachio produced significant decreases in LDL (P 0.001, a significant increase in HDL in moderately hypercholester-
À23.2 6 11.9%), TC (P 0.001, À21.2 6 9.9%), and TG olemic patients. TG and LDL levels remain unchanged.
(P ¼ 0.008, À13.8 6 33.8%) and a non-significant decrease Kocyigit et al. [7] reported that 3 wk of a pistachio diet caused
in HDL (P ¼ 0.069, À3.1 6 11.7%; Fig. 1) when compared significant decreases in TC, TC/HDL ratio, and LDL/HDL
with the Mediterranean diet. There were significant reduc- ratio and a significant increase in HDL in normolipidemic
tions in ApoA1 and ApoB levels and ratios of TC/HDL healthy volunteers. TG and LDL levels remained unchanged.
and LDL/HDL (P 0.001 for all), whereas oxidized LDL Sheridan et al. [8] reported that 4 wk of a pistachio diet caused
and homocysteine levels and the ApoB/ApoA1 ratio re- significant decreases in TC/HDL ratio and LDL/HDL ratio
mained unchanged (Table 3). but a significant increase in HDL in subjects with moderate
Suitable brachial artery endothelial function measure- hypercholesterolemia. TC, LDL, and TG remained un-
ments were available for all 32 subjects who completed the changed. In our study we demonstrated significant decreases
study. The pistachio diet produced significant improvement in glucose, TC, TG, LDL, TC/HDL ratio, and LDL/HDL
in the EDV (P ¼ 0.002, 30% relative increase), whereas ratio in normolipidemic healthy young men. Although there
endothelium-independent vasodilation remained unchanged was a trend of a decrease in HDL level, it was not statistically
when compared with the Mediterranean diet (Table 4, Fig. 2). significant. The present study is the first demonstrating
The pistachio diet caused significant decreases in serum in- a decrease in LDL and TG levels with a pistachio diet. In
terleukin-6, TOS, lipid hydroperoxide, and MDA and an in- addition, the three previous pistachio studies were associated
crease in SOD (P 0.001 for all), whereas there were no with an increase in HDL, whereas the present study showed
significant changes in hs-CRP and tumor necrosis factor- a non-significant decrease. One interesting result of the
a levels when compared with the Mediterranean diet (Table 5). present study is the significant decrease in blood glucose

Table 3
Body weight, blood pressure, glucose, and lipid parameters at baseline and at the end of each diet
Variable Baseline Mediterranean diet Pistachio diet P
Weight (kg) 69.3 6 4.9 69.7 6 5.0 69.5 6 5.1 0.1
Systolic BP (mmHg) 117 6 8 119 6 8 117 6 6 0.1
Diastolic BP (mmHg) 73 6 8 74 6 7 73 6 7 0.1
Glucose (mg/dL) 91 6 8 92 6 8 84 6 6 0.001
TC (mg/dL) 199.6 6 41.8 190.7 6 30.1 149.4 6 26.5 0.001
TG (mg/dL) 91.2 6 39.7 112.1 6 45.5 91.1 6 38.1 0.008
HDL (mg/dL) 43.3 6 9.7 43.5 6 9.2 41.7 6 7.38 0.069
LDL (mg/dL) 142.0 6 37.4 124.5 6 24.5 95.0 6 23.2 0.001
Oxidized LDL (ng/mL) 355.1 6 109.9 331.4 6 95.6 346.2 6 82.7 0.1
TC/HDL 4.86 6 1.0 4.40 6 0.8 3.78 6 0.7 0.001
LDL/HDL 3.39 6 0.9 2.88 6 0.7 2.30 6 0.6 0.001
ApoA1 (g/L) 1.24 6 0.17 1.34 6 0.18 1.20 6 0.20 0.001
ApoB (g/L) 0.65 6 015 0.64 6 0.14 0.57 6 0.15 0.001
ApoB/ApoA1 0.53 6 0.15 0.49 6 0.13 0.48 6 0.14 0.1
Homocysteine (mmol/L) 10.7 6 3.2 10.6 6 3.8 11.0 6 3.7 0.1
Apo, apolipoprotein; BP, blood pressure; HDL, high-density lipoprotein; LDL, low-density lipoprotein; TC, total cholesterol; TG, triacylglycerol.

I. Sari et al. / Nutrition 26 (2010) 399–404 403

Table 4
Brachial endothelial function at baseline and at the end of each diet
Variable Baseline Mediterranean Pistachio P
diet diet
Baseline artery 3.22 6 0.23 3.26 6 0.25 3.26 6 0.24 0.1
diameter (mm)
EDV (%) 7.19 6 1.65 7.86 6 2.28 10.29 6 2.76 0.002
EIDV (%) 13.53 6 3.20 13.33 6 3.41 14.65 6 2.43 0.1
EDV, endothelium-dependent vasodilation; EIDV, endothelium-indepen-
dent vasodilation.

study, we demonstrated that a pistachio diet resulted in an im-
provement in EDV in normolipidemic healthy young men
similar to a walnut diet. Although the specific mechanism
is unknown, several possible mechanisms can be proposed.
First, cholesterol lowering as in the present cohort is known
to improve endothelial function [21]. Second, the high
L-arginine content of pistachios might contribute to the
improvement in EDV, which is a precursor of endogenous
Fig. 1. A pistachio diet resulted in significant reductions in LDL vasodilator nitric oxide [22]. Third, the favorable effects of
(* P 0.001, À23.2 6 11.9%), TC (* P 0.001, À21.2 6 9.9%), and TG a pistachio diet on inflammatory and oxidative statuses,
(** P ¼ 0.008, À13.8 6 33.8%) and a non-significant reduction in HDL which were demonstrated in the present study, and the fiber,
(*** P ¼ 0.069, À3.1 6 11.7%) when compared with the Mediterranean vitamin, micronutrient, and phytosterol content of pistachio
diet. HDL, high-density lipoprotein; LDL, low-density lipoprotein; TC, total
cholesterol; TG, triacylglycerol.
might improve EDV.
Inflammation and oxidation play an important role in the
pathogenesis and progression of atherosclerosis. To date,
there are no data about the effect of pistachio on inflammatory
level with the pistachio diet, which warrants further studies
parameters. A pistachio diet did not cause significant changes
especially in the diabetic population.
in hs-CRP and tumor necrosis factor-a levels. However, there
It is known that a diet rich in MUFA has favorable effects
was a significant decrease in interleukin-6 level, which is also
on CHD risk profile and pistachio is an excellent source of
MUFA [15,16]. Dietary fiber intake is associated with a lower
risk of CHD and fiber content was high in the pistachio diet
[17–19]. These might explain the favorable effects of pista-
chio on lipid parameters. Most nut studies were performed
based on an isoenergetic diet with a control group so that
nuts were replaced with MUFA content constituting
z15–20% of daily caloric intake. In our recent report, in
an experimental model of rats, consumption of pistachio as
20% of daily caloric intake had beneficial effects on lipid
parameters and LDL oxidation that were blunted when pista-
chio intake was increased to 40% of daily caloric intake [20].
Therefore, pistachio intake as 20% of daily caloric intake
seems reasonable. Blood pressure and body weight of the
participants did not change during the study and this was
compatible with the data of previous nut studies.
Although it has been documented that a pistachio diet has
favorable effects on lipid parameters, investigations have
found that their cardioprotective effect has some other mech-
anisms beyond their hypolipidemic effects. Endothelial
dysfunction is an early key event in the atherosclerotic
process that predicts future CHD development [9,10]. The
effect of pistachio on endothelial function has not been stud- Fig. 2. Endothelial-dependent vasodilation in brachial arteries of 32 men. A
ied previously. In a recent study, substituting walnuts for pistachio diet produced a significant improvement in endothelial-dependent
MUFA in a Mediterranean diet resulted in an improvement vasodilation (30% relative increase) when compared with the Mediterranean
in EDV in hypercholesterolemic adults [11]. In the present diet.


Table 5 References
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operating during the study period. They also appreciate the [20] Aksoy N, Aksoy M, Bagci C, Gergerlioglu HS, Celik H, Herken E, et al.
help of the administration of vocational police education Pistachio intake increases high density lipoprotein levels and inhibits low-
school of Gaziantep and the Gaziantep police department. density lipoprotein oxidation in rats. Tohoku J Exp Med 2007;212:43–8.
[21] Vogel R. Cholesterol lowering and endothelial function. Am J Med
They appreciate the help of Nilgun Dogruer Kalkanci from
1999;107:479–87.
the Pistachio Investigation Institute, Gaziantep, for providing [22] Preli RB, Klein KP, Herrington DM. Vascular effects of dietary
the data about the Antep pistachio (Pistacia vera L.). L-arginine supplementation. Atherosclerosis 2002;162:1–15.

2010 effect of pistachio diet on lipid parameters, endothelial function

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