Nut consumption has favorable effects on lipid profiles of Korean women with metabolic syndrome

N U TR IT ION RE S E ARCH XX ( 2 0 14 ) X XX– X XX

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Nut consumption has favorable effects on lipid profiles of Korean women with metabolic syndrome☆ Young Joo Lee a , Ga Eun Nam b,⁎, Ji A. Seo c , Taehyung Yoon a , Ilwon Seo a , Jin Hee Lee a , Donggil Im a , Kyeong-Nyeo Bahn a , Si An Jeong a , Tae Seok Kang a , Jae Hee Ahn c , Do Hoon Kim b , Nan Hee Kim c,⁎⁎ a b c

Nutrition and Functional Food Research Team, National Institute of Food and Drug Safety Evaluation, Chungcheongbuk-do, South Korea Department of Family Medicine, Korea University Ansan Hospital, College of Medicine, Korea University, Ansan-si, South Korea Department of Endocrinology and Metabolism, Korea University Ansan Hospital, College of Msedicine, Korea University, Ansan-si, South Korea

ARTI CLE I NFO

A BS TRACT

Article history:

Nut consumption has been studied for its cardioprotective effects. However, the findings of

Received 30 April 2014

clinical intervention studies are inconsistent; and no intervention studies have been

Revised 24 August 2014

conducted in the Korean population. We hypothesized that nut supplementation may have

Accepted 26 August 2014

favorable influence on metabolic markers. Therefore, this study aimed to investigate the effects of nut consumption on metabolic parameters and biomarkers related to

Keywords:

inflammation, oxidative stress, and endothelial function in Korean adults with metabolic

Nuts

syndrome. To this end, we designed a randomized, parallel, controlled dietary intervention

Metabolic syndrome

study (ClinicalTrials.gov NCT02023749). Subjects with metabolic syndrome and a body mass

Lipid profile

index of at least 23 kg/m2 were randomized to the Control group and the Nut group, which

Inflammation

received supplementation with 30 g/d of mixed nuts (walnuts, peanuts, and pine nuts) for

Oxidative stress

6 weeks. Sixty volunteers were included in the final analysis. Metabolic markers were evaluated

Endothelial function

at baseline and at the end of the study. Total cholesterol and non–high-density lipoprotein cholesterol levels significantly improved in the Nut group compared to those in the Control group (P = .023 and P = .016, respectively) in women. Biomarkers related to inflammation, oxidative stress, and endothelial function did not significantly change from baseline in either group. Thus, supplementing a usual diet with mixed nuts for 6 weeks had favorable effects on several lipid parameters in Korean women with metabolic syndrome. These findings present a possible mechanism for the cardioprotective effects of nut consumption. © 2014 Elsevier Inc. All rights reserved.

Abbreviations: BMI, body mass index; FBG, fasting blood glucose; HDL-C, high-density lipoprotein cholesterol; HOMA-IR, homeostasis model assessment of insulin resistance; LDL-C, low-density lipoprotein cholesterol; SD, standard deviation; TC, total cholesterol; TG, triglyceride. ☆ All authors disclose no financial or other substantive conflict of interest that might be construed to influence the results or interpretation of the results of this manuscript. ⁎ Correspondence to: Ga Eun Nam, MD, Department of Family Medicine, Korea University Ansan Hospital, College of Medicine, Korea University, 516 Gojan-dong, Danwon-gu, Ansan-si, Gyeonggi-do, 425-707, Korea. Tel.: +82 31 412 5360; fax: +82 31 412 5364. ⁎⁎ Correspondence to: Nan Hee Kim, MD, PhD, Department of Endocrinology and Metabolism, Korea University Ansan Hospital, College of Medicine, Korea University, 516 Gojan-dong, Danwon-gu, Ansan-si, Gyeonggi-do, 425-707, Korea. Tel.: +82 31 412 5952; fax: +82 31 412 6770. E-mail addresses: [email protected] (G.E. Nam), [email protected] (N.H. Kim). http://dx.doi.org/10.1016/j.nutres.2014.08.011 0271-5317/© 2014 Elsevier Inc. All rights reserved.

Please cite this article as: Lee YJ, et al, Nut consumption has favorable effects on lipid profiles of Korean women with metabolic syndrome, Nutr Res (2014), http://dx.doi.org/10.1016/j.nutres.2014.08.011

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1.

Introduction

Metabolic syndrome is a cluster of metabolic abnormalities including abdominal obesity, dyslipidemia, elevated blood pressure, and hyperglycemia; and it is associated with significant risk for cardiovascular disease [1]. Metabolic syndrome affects almost one-quarter of the adult population, and its prevalence is increasing globally [2]. Previous studies have indicated that dietary habits are important for the prevention and control of metabolic syndrome. For example, a Mediterranean diet, which includes nuts, is associated with a low risk of metabolic syndrome [3,4]. Nuts are complex foods that are rich in macronutrients including unsaturated and polyunsaturated fatty acids, micronutrients, fiber, and other bioactive phytonutrients [5]. Previous studies showed that the cardioprotective effects of nut consumption are attributed to the improved insulin sensitivity, endothelial function, or anti-inflammatory action of nuts [6,7]. Meanwhile, the association between nut consumption and metabolic syndrome has mainly been evaluated in epidemiologic studies. Although some clinical trials have investigated the beneficial effects of nut consumption on metabolic syndrome, their results were inconsistent [8–10]. Moreover, no such clinical trial has been conducted in a Korean population, in which the prevalence of metabolic syndrome is rapidly increasing [11]. We hypothesized that nut consumption may have a beneficial effects on metabolic variables. Therefore, this study aimed to investigate the effects of nut consumption on metabolic parameters and biomarkers related to inflammation, oxidative stress, and endothelial function in Korean adults with metabolic syndrome.

2.

Methods and materials

2.1.

Study subjects

Volunteers aged 35 to 65 years were screened for this study. We recruited study subjects who underwent a health examination at a university hospital and from advertising in Ansan, South Korea. According to the power calculations, a sample size of 31 subjects was needed to detect a mean difference of 12 mg/dL, with standard deviations (SD) of 15, in low-density lipoprotein cholesterol (LDL-C) to provide 80% power at a significance level of P < .05. Subjects were enrolled in this study if their body mass index (BMI) was at least 23 kg/m2 and they met the criteria for metabolic syndrome. Metabolic syndrome was defined according to the National Cholesterol Education Program Adult Treatment Panel III criteria [12]. Abdominal obesity was defined using the Korean-specific cutoff values (waist circumference ≥90 cm for men or ≥85 cm for women) [13]. Subjects were excluded if they had a nut allergy, peptic disorder, history of cancer, cardiovascular disease, chronic renal insufficiency, or cirrhosis. Subjects were also excluded for the following reasons:(1) receiving treatment with hypoglycemic agents for diabetes or having hemoglobin A1c level greater than 7%; (2) receiving corticosteroid treatment; (3) started antihypertensive or lipid-lowering agents, or

changed their doses within the previous month; (4) a weight change of greater than 5% of body weight during the 3 months prior to the study; (5) pregnancy; or (6) regular nut consumption (>15 g/d of nuts at least 3× a week). All participants gave written informed consent, and the study was approved by the institutional review boards of Korea University Ansan Hospital and National Institute of Food and Drug Safety Evaluation (ClinicalTrials.gov NCT02023749).

2.2.

Study design and dietary intervention

A randomized, controlled, parallel, 6-week dietary intervention study was designed. Of the 116 individuals who participated in the screening test, 55 people did not meet the inclusion criteria and 6 people withdrew consent. Sixty-one subjects were stratified by sex and age and randomly assigned to the Control group (dietary recommendations for prudent diet) or the Nut group (the same dietary recommendations supplemented with 30 g/d of mixed nuts (15, 7.5, and 7.5 g/d of raw walnuts, raw pine nuts, and roasted peanuts, respectively). At the baseline visit (0 week), the lifestyle characteristics of each subject were collected using a self-reported questionnaire. All subjects were provided dietetic support to help them maintain their usual diets, and they were instructed to write a daily self-record of their intake to monitor adherence to the interventions. They were also asked to keep their usual physical activity levels throughout the study. Subjects who used chronic medication, such as lipid-lowering agents or antihypertensive agents, at baseline were instructed to continue the same dosage during the trials. Anthropometric measurements, physical examinations, and fasting blood and random urine samplings were performed; and endothelial function was evaluated at baseline (0 week) and the end of the study (6 weeks). Three-day food records prior to baseline and the end of the study were collected and analyzed with a computer-aided nutritional analysis program (CAN-Pro 4.0 Korean Nutrition Society).

2.3.

Measurements

Height and body weight were measured while wearing light clothing and no shoes, and BMI was calculated as body weight divided by height squared (kg/m2). Waist circumference was measured using a measuring tape at the narrowest point between the lower rib margin and the iliac crest after exhalation with the subject standing. Blood pressure was measured manually with a mercury sphygmomanometer. Fasting serum concentrations of total cholesterol (TC), triglyceride (TG), high-density lipoprotein cholesterol (HDL-C), and LDL-C were measured with a Hitachi Automatic Analyzer 7600-210 (Hitachi, Tokyo, Japan) using the enzyme method. Fasting blood glucose (FBG) was measured using the hexokinase method, and high-sensitive C-reactive protein was measured using the Latex immune complex turbidimetry method. Hemoglobin A1c was measured with Tosoh G8 (Tosoh, Tokyo, Japan) using high-performance liquid chromatography, and insulin levels were measured with a Cobas 8000 e602 (Roche Diagnostics, Basel, Switzerland) using the electrochemical luminescent immunoassay. Insulin resistance was calculated using the homeostasis model assessment of

Please cite this article as: Lee YJ, et al, Nut consumption has favorable effects on lipid profiles of Korean women with metabolic syndrome, Nutr Res (2014), http://dx.doi.org/10.1016/j.nutres.2014.08.011

N U TR IT ION RE S E ARCH XX ( 2 0 14 ) X XX– X XX

insulin resistance (HOMA-IR), where HOMA-IR = fasting insulin (mU/mL) × FBG (mg/dL)/405 [14]. Adiponectin, interleukin-6, markers for oxidative stress including malondialdehyde and oxidized low-density lipoprotein, and factors related to endothelial function, such as vascular cell adhesion molecule-1 and intercellular adhesion molecule-1, were measured using Versa Max (Molecular Device, Sunnyvale, CA) by the enzyme-linked immunosorbent assay method. Endothelial function was also assessed using a finger plethysmograph based on noninvasive peripheral artery tonometry (EndoPAT 2000; Itamar-Medical Ltd, Caesarea, Israel). The EndoPAT index was calculated as the ratio of the pulse wave amplitude during reactive hyperemia to the preocclusion baseline.

2.4.

Statistical analyses

All statistical analyses were performed using SAS version 9.2 for Windows (SAS Institute, Cary, NC), and P < .05 was considered to be statistically significant. If necessary, logarithmic transformation was conducted to achieve a normal distribution. Data are presented as means ± SD or geometric means (95% confidence intervals). Differences in baseline

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values between the 2 diet groups were tested using independent t test, and differences in the changes between groups were tested using paired t test. Differences between the baseline and final values within groups were tested using independent t test. Then, for metabolic parameters with P of intervention effect <.15, we conducted analysis of covariance after adjusting for baseline values. We also performed sexspecific analysis for those variables.

3.

Results

Of the 61 randomized participants, 1 withdrew from the study for personal reasons. Sixty subjects (30 in the Nut group and 30 in the Control group) completed the study and were included in the final analyses (Fig. 1). Compliance with the dietary intervention was calculated as 98% based on the daily self-record. At baseline, age, lifestyle characteristics, anthropometric and biochemical parameters, total daily energy, and nutrient intake were similar between the 2 intervention groups. Table 1 shows the baseline levels and 6-week changes in metabolic and nutritional parameters according to the intervention group. After the intervention period, no significant differences were

Fig. 1 – Flow diagram of subject screening and selection for the nut study. Please cite this article as: Lee YJ, et al, Nut consumption has favorable effects on lipid profiles of Korean women with metabolic syndrome, Nutr Res (2014), http://dx.doi.org/10.1016/j.nutres.2014.08.011

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Table 1 – Baseline levels and changes in nutritional and metabolic variables in the Nut and Control groups Nut group Baseline Weight (kg) BMI (kg/m2) WC (cm) SBP (mm Hg) TC (mg/dL) HDL-C (mg/dL) LDL-C (mg/dL) TG (mg/dL) Non–HDL-C FBG (mg/dL) Insulin (mU/mL) HOMA-IR HbA1c (%) Nutritional intake Energy (kcal/d) Carbohydrate (g) Protein (g) Fat (g) Fiber (g)

a

72.99 ± 11.34 27.19 ± 2.11 92.68 ± 5.31 130.93 ± 13.14 210.40 ± 36.52 41.70 ± 8.82 129.57 ± 32.42 201.98 (162.60, 250.89) 168.70 ± 33.72 94.47 ± 9.53 9.83 (8.43, 11.47) 3.10 (2.76, 3.49) 5.80 ± 0.26 1736.9 ± 576.4 247.9 ± 58.8 73.4 ± 24.6 45.9 ± 27.5 22.2 ± 7.0

Control group b

Baseline

a

Change

P

0.01 ± 1.14 0.00 ± 0.46 −0.42 ± 1.28 −5.23 ± 8.26 −8.73 ± 15.00 0.07 ± 4.69 −1.50 ± 15.39 −54.87 ± 107.41 −8.80 ± 15.05 0.40 ± 7.19 −0.33 ± 4.25 0.00 ± 1.21 0.04 ± 0.19

.994 .674 .689 .810 .239 .901 .426 .503 .211 .439 .077 .064 .624

72.97 ± 11.12 26.96 ± 2.16 93.25 ± 5.58 129.97 ± 17.47 198.23 ± 42.50 41.33 ± 13.33 122.10 ± 39.40 173.32 (138.06, 217.60) 156.90 ± 38.38 92.73 ± 7.58 7.73 (6.47, 9.23) 2.60 (2.29, 2.95) 5.76 ± 0.36

27.0 ± 412.3 −16.1 ± 48.5 −6.5 ± 21.4 11.1 ± 22.6 −1.0 ± 8.4

.693 .626 .556 .977 .539

1682.1 ± 488.0 256.9 ± 63.7 66.1 ± 26.4 42.7 ± 22.2 21.3 ± 9.3

Intervention effect Change

P

b

Pc

0.00 ± 1.10 0.00 ± 0.50 0.20 ± 1.30 −4.80 ± 11.10 1.90 ± 24.90 1.50 ± 6.60 1.90 ± 24.30 −17.83 ± 161.60 0.40 ± 22.72 1.00 ± 7.67 0.00 ± 2.91 0.01 ± 0.71 −0.04 ± 0.26

.981 .637 .583 .879 .876 .710 .646 .752 .778 .670 .211 .178 .141

.872 .759 .491 .854 .051 .346 .517 .301 .070 .756 .255 .958 .177

99.9 ± 285.8 5.6 ± 43.0 2.9 ± 16.7 1.5 ± 17.3 0.7 ± 8.0

.897 .013 .584 .196 .627

.429 .070 .363 .378 .697

WC, waist circumference; SBP, systolic blood pressure; HbA1c, hemoglobin A1c. Values present the means ± standard deviation, geometric mean (95% confidence interval), or mean change ± standard deviation. a No significant differences between groups at baseline using independent t test. b Differences from baseline within groups were assessed using paired t test. c Differences in changes between groups were assessed using independent t test.

observed in the changes of metabolic variable and nutrient intake. The changes of TC and non–HDL-C levels in the Nut group showed borderline significance from those in the Control group (P = .051 for TC and P = .070 for non–HDL-C). However, after adjusting for baseline lipid concentration, the intervention effects were not significant (P = .098 for TC and P = .136 for non– HDL-C). Interestingly, in sex-specific analysis, TC and non– HDL-C levels in the nut group were significantly decreased only in women; and their intervention effects in both groups were significantly different (P = .023 for TC and P = .016 for non–HDL-C) (Fig. 2). The proportion of subjects with each component of metabolic syndrome did not change after the 6-week intervention in either group. Table 2 lists the baseline levels and 6-week changes in biomarkers related to inflammation, oxidative stress, and endothelial function. There were no significant changes in inflammation markers, oxidative stress biomarkers, and adhesion molecules in both groups. This intervention did not affect endothelial function as measured using EndoPAT.

4.

Discussion

In this 6-week, parallel, randomized, controlled dietary intervention trial in Korean adults with metabolic syndrome, a diet supplemented with 30 g of mixed nuts improved several lipid parameters including TC and non–HDL-C in women; but it had no effect on biomarkers related to inflammation, oxidative stress, and endothelial function. The fatty acids, other specific lipids, and bioactive macronutrients present in nuts have the potential to improve metabolic

and cardiovascular outcomes. The essential micronutrients present in nuts have antithrombotic and antioxidant properties; and the mineral characteristics of nuts might contribute to protection against arterial hypertension, insulin resistance, and overall cardiovascular risk [15]. Although the lipid-lowering effects of nuts, mainly on TC and LDL-C levels, have been studied previously, the effects have differed according to the type, amount, duration of consumption, study design, and characteristics of the study subjects [16,17]. Moreover, few studies of nutrition intervention with nuts have been conducted in patients with metabolic syndrome. A recent clinical trial investigating the effects of supplementing a healthy diet with nuts or with walnuts and cashews in patients with metabolic syndrome failed to show any changes in lipid parameters [8,9]. It is possible that nuts are less effective at improving lipid profiles in subjects with obesity and metabolic syndrome because obesity promotes the endogenous production of cholesterol in relation to insulin resistance [18]. Additionally, the ability of nuts to lower cholesterol levels by interfering with intestinal cholesterol absorption could be blunted because of the reduced intestinal cholesterol absorption associated with obesity and metabolic syndrome [19,20]. However, our study demonstrated a beneficial effect of nuts on lipid profile in women compared to previous clinical studies [8,9]. This discrepancy may be attributed to the lower baseline LDL-C and BMI levels of the subjects in this study or to differences in ethnicity. Although there have been no study on the effects of nut consumption on metabolic syndrome with sex-specific analyses, a recent randomized controlled trial that compared the effects of almond-enriched diet and nut-free diet on overweight or obese women in a

Please cite this article as: Lee YJ, et al, Nut consumption has favorable effects on lipid profiles of Korean women with metabolic syndrome, Nutr Res (2014), http://dx.doi.org/10.1016/j.nutres.2014.08.011

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Fig. 2 – The relative changes in the levels of TC and non–HDL-C after the nut intervention for all subjects and in women and men.

weight reduction program showed significant improvements of TC and TG levels in the almond group [21]. The results of our study are partly in accordance with these findings. Sex-specific

effects of nut consumption on lipid profiles have not been evaluated yet, and further studies are needed to reveal the underlying mechanisms.

Table 2 – Baseline levels and changes in inflammatory markers and endothelial function markers in the Nut and Control groups Nut group

WBC (×103/μL) hsCRP (mg/L) IL-6 (pg/mL) Adiponectin (μg/mL) Serum MDA (pmol/mg) Urine MDA (pmol/mg) oxLDL (U/L) VCAM-1 (ng/mL) ICAM-1 (ng/mL) EndoPAT index

Control group

Intervention effect

Baseline a

Change

Pb

Baseline a

Change

Pb

Pc

5.69 (5.24, 6.17) 0.11 (0.09, 0.14) 2.18 ± 1.44 6.84 ± 2.07 1.28 ± 0.22 1.70 ± 0.37 51.22 ± 13.58 638.80 ± 105.86 203.88 ± 58.59 1.92 ± 0.56

−0.06 −0.00 0.31 −0.14 −0.02 0.10 0.10 −21.13 −0.07 −0.06

.125 .755 .419 .962 .951 .234 .315 .066 .748 .595

5.16 (4.71, 5.65) 0.12 (0.08, 0.16) 1.93 ± 0.97 6.81 ± 2.77 1.28 ± 0.23 1.61 ± 0.24 47.40 ± 15.52 699.30 ± 141.21 209.53 ± 75.90 1.99 ± 0.48

−0.10 −0.01 −0.15 −0.08 −0.00 −0.08 0.44 −33.33 −2.07 −0.16

.096 .937 .153 .971 .745 .208 .291 .106 .842 .781

.869 .610 .194 .811 .445 .394 .885 .461 .793 .482

± 0.89 ± 0.08 ± 1.79 ± 0.96 ± 0.06 ± 1.15 ± 9.34 ± 62.01 ± 28.30 ± 0.65

± 0.67 ± 0.06 ± 0.67 ± 0.75 ± 0.10 ± 0.14 ± 8.59 ± 65.14 ± 30.44 ± 0.52

WBC, white blood cell; hsCRP, high-sensitive C-reactive protein; IL-6, Interleukin-6; MDA, malondialdehyde; oxLDL, oxidized low-density lipoprotein; VCAM, vascular cell adhesion molecule; ICAM, intercellular adhesion molecule. Values presented the means ± standard deviation, geometric mean (95% confidence interval), or mean changes ± standard deviation. a No significant differences between groups at baseline using independent t test. b Differences from baseline within groups was assessed using paired t test. c Differences in changes between groups was assessed using independent t test.

Please cite this article as: Lee YJ, et al, Nut consumption has favorable effects on lipid profiles of Korean women with metabolic syndrome, Nutr Res (2014), http://dx.doi.org/10.1016/j.nutres.2014.08.011

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The complex components of nuts beneficially influence blood pressure [22,23]. However, a majority of clinical trials reported that nut consumption had no significant effect on blood pressure, which is in accordance with the results of this study [8,9,24]. In addition, high-fat diets enriched with unsaturated fatty acids are associated with improvement in insulin sensitivity compared to low-fat or high–saturated fatty acid diets [25]. In addition, the considerable amount of magnesium present in nuts might be associated with a lower risk of diabetes [26]. However, few clinical trials have investigated the effects of nut consumption on glucose control or insulin response; and their findings have been inconsistent [8,9,27]. In the current study, fasting glucose, insulin and HOMA-IR values were unchanged after the intervention. The possible mechanisms underlying the beneficial effects of nuts are due to their anti-inflammatory and antioxidant actions and their ability to improve endothelial function [28,29]. However, clinical trials have reported conflicting results on this topic [8,15,28–32]. Similarly, we did not observe any significant differences in these markers between the 2 groups. The present study has some limitations. First, we conducted the study over a relatively short duration; so the effects of chronic nut consumption could not be examined. Second, although subjects were instructed to maintain their usual diet and adherence was monitored, we cannot ignore the possibility of residual effects of unconscious and unreported food consumption. Third, the beneficial effects of different nuts may vary; but our study did not differentiate between specific types of nuts. Lastly, the post hoc power was calculated as 60%; and the relatively small sample size may be another reason for the limited beneficial effect of nuts. In conclusion, a diet supplemented with mixed nuts for 6 weeks produced favorable effects on several lipid parameters in Korean women with metabolic syndrome. Further studies with larger sample sizes and longer durations are needed to examine the role of nut consumption in the prevention and management of metabolic syndrome.

[5]

[6] [7]

[8]

[9]

[10]

[11]

[12]

[13]

[14] [15] [16]

Acknowledgment This research was supported by a grant (12161MFDS118) from the Ministry of Food and Drug Safety in 2012. The authors declare no conflicts of interest.

[17]

[18]

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Please cite this article as: Lee YJ, et al, Nut consumption has favorable effects on lipid profiles of Korean women with metabolic syndrome, Nutr Res (2014), http://dx.doi.org/10.1016/j.nutres.2014.08.011