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Int J Diabetes Dev Ctries (April–June 2013) 33(2):115–119 DOI 10.1007/s13410-012-0108-9

ORIGINAL ARTICLE

Effect of olive, and on cardiovascular risk factors in type 2 diabetic patients

Fatemeh Kaseb & Maryam Rashidi & Mohammad Afkhami-Ardekani & Hossein Fallahzadeh

Received: 13 December 2011 /Accepted: 3 December 2012 /Published online: 1 May 2013 # Research Society for Study of Diabetes in India 2013

Abstract Several studies have demonstrated the benefits of Introduction on cardiovascular risk factors in diabetes. The goal of the present study was to compare the effects of olive, Saturated fatty acids have been associated with a higher risk almond and walnut oil on serum glucose, lipids and blood of CHD, whereas monounsaturated fatty acids (MUFAs) pressure in type 2 diabetic patients. In this cross over clinical and n-3 polyunsaturated fatty acids have protective effects study 24 hypercholesterolemic type 2 diabetic patients were against CHD [1]. Nuts provide substantial amounts of die- recruited. Subjects consecutively assigned to consume 40 cc tary PUFA, and nut consumption is inversely associated olive, almond and walnut oil daily over a 4-week period with the risk of type 2 diabetes [2]. There are mechanistic with a two-week washout period, accompanied by the Step I explanations for the influence of dietary polyunsaturated fatty diet. Anthropometric measurements, HbA1c, lipid profile acid (PUFA) on insulin action and energy metabolism [3, 4], and serum glucose and blood pressure were measured ini- and cohort studies of women in the U.S. have demonstrated a tially and at the end of the study. Serum levels of total reduced risk of developing type 2 diabetes with dietary PUFA cholesterol (TC) and LDL-cholesterol at baseline and at replacing trans or saturated fatty acids (SFAs) [5, 6]. the end of trial differed significantly after (P0 are rich in ω-9 fatty acids, which have demon- 0.007, P00.02) and triglyceride (TG) after almond oil (P0 strated beneficial effects on lipoprotein profiles [7–9], and 0.02). When the differences of these laboratory levels be- their proteins have an arginine-rich amino acid profile that is tween olive, almond and walnut were tested, no significant thought to be cardioprotective [10]. A growing number of differences were found. Our findings showed olive oil could human nutritional studies have revealed that almonds have a reduce significantly serum levels of TC and LDL. Almond cholesterol lowering effect [7–9]. consumption could decrease TG significantly. Our research are distinguished from other nuts by virtue of could not show significant reduction in blood pressure. their higher polyunsaturated content and importantly their α-linolenic acid (ALA) content combined with antiox- Keywords Type 2 diabetes . Olive oil . Almond oil . idants in the form of α-tocopherol. Walnut oil The olive products constitute a rich source of polyphe- nols such as oleuropein and its derivatives, including hydroxytyrosol, which scavenge free radicals and inhibit the chemical oxidation of LDL [11, 12]. In addition, a diet rich in olive oil reduces the thrombotic propensity[13], and may slow the development of coronary atherosclerosis [14]. Treatment trials have demonstrated the benefits of replacing F. Kaseb (*) : M. Rashidi : M. Afkhami-Ardekani Yazd Diabetes Research Center, Jomhoori Boulevard, dietary SFA with monounsaturated (MUFA) [15, 16], Afshar Alley, but the effects of dietary PUFA have been less well studied Yazd, Iran in diabetic subjects. In the present study we compared e-mail: [email protected] effects of consuming olive, almond and walnut oil on serum H. Fallahzadeh glucose, lipid profile and blood pressure in type 2 diabetic Shahid Sadoughi University of Medical Science, Yazd, Iran patients. 116 Int J Diabetes Dev Ctries (April–June 2013) 33(2):115–119

Material and methods compare before and after metabolic responses paired t-test and for comparing variable differences between three In this cross over clinical trial 24 hypercholestrolemic type 2 groups one-way ANOVA was used. Significance was con- diabetic patients 38 to 65 years of age who met inclusion sidered to be P<0.05. Results were given with their 95 % criteria were recruited from Yazd Diabetes Research Center. CIs. Data were presented as mean±SD. Individuals enrolled in the study included type 2 diabetics (according to ADA 2006) [17], taking hypoglycemic drugs or diet, with LDL-cholesterol more than 100 mg/dl. Exclusion criteria were insulin therapy, diabetic compli- Results cations requiring tight diabetes control, current consumption of nuts, food allergies, cigarette smoking, regular use of In this study 21 subjects (9 males and 13 females) were medication known to effect blood lipids and blood pressure, studied. Of these 21 subjects consumed olive oil, 19 subjects BMI>30 kg/m2, pregnancy and lactation. continued to consume almond oil and 8 subjects continued to The study protocol consisted of a two-week baseline consume walnut oil. The mean age of patients was 52.59± period during which the subjects consumed Step I diet 7.1 years and mean duration of diabetes was 5.34±4.52 years. recommended by a nutritionist and then were consecutively Among the 24 eligible diabetic patients, 2 dropped out of assigned to consume 40 cc olive, almond and walnut oil the study completely because of gastrointestinal side effects. daily over a 4-week period with a-two week washout period. Three subjects after using olive oil and one after using were permitted to be consumed with meals or added almond oil refused to continue. Eleven subjects could not to desserts or salads. Subjects returned for biweekly data be followed up after consuming almond and olive oil for collection and consultation with the investigators about ad- blood testing throughout the study. Table 1 shows charac- verse events and study related questions. teristic of type 2 diabetic patients. At baseline and at the end of each study period of four It was found in the present study that serum levels of TC weeks, anthropometric measurements, HbA1c, lipid profile and LDL-C at baseline and at the end of trial differ signif- and serum glucose and blood pressure were measured. icantly after olive oil (P00.007, P00.02). TG, TC, LDL, FBG and HbA1c diminished after almond oil but the reduc- tion of TG was significant (P00.02) (Table 2). There were Measurements no significant differences in the other parameter such as BMI, FBG, HbA1c, HDL-C after olive, almond and walnut Height and weight were taken using standard protocols with oil (P>0.05). When the differences of these laboratory the subjects in light clothing and without shoes. Body Mass parameters between olive, almond and walnut were test- Index (BMI) was calculated as weight (in kilograms) divid- ed, no significant difference was found (P >0.05) ed by height (in meters squared). Serum glucose, Total (Table 2). Cholestrol (TC) and High density lipoprotein cholesterol (HDL-C) were measured by colorimetric methods (GPO- PAP) with Photometer 5010 (Parsazmon kit, Iran). Low- Table 1 Characteristic of type 2 diabetic subjects studied density lipoprotein cholesterol (LDL) was calculated by Variables Mean±SD the Friedewald formula [18]. Glycated hemoglobin (HbA1C) was measured with DS5 Age (year) 52.59±7.1 analyzer and DS5 Pink Reagent kit. Systolic (SBP) and Sex 9 male and 13 female Diastolic blood pressure (DBP) were measured in three Diabetes duration(years) 5.34±4.52 positions (supine, sitting and upright) in 5 min pauses and Education (years) 6.54±5.49 the mean was recorded. BMI (Kg/m2) 26.94±2.89 Informed consent was obtained from all subjects and the Weight(Kg) 74.35±12.24 research project had the approval of the institutional review FBG (mg/dl) 180.86±60.75 board and ethics committee of the Yazd University of Med- HbA1c (%) 8.99±2.3 ical Sciences and was carried out in accordance with the TG(mg/dl) 184.48±73.56 Declaration of Helsinki. TC(mg/dl) 220.14±28.01 HDL(mg/dl) 61.57±18.09 Statistical analysis LDL(mg/dl) 121.67±22.72 Systolic blood pressure (mmHg) 126.6±15.59 Statistical analysis was performed using Statistical Package Diastolic blood pressure (mmHg) 81.43±11.08 for Social Sciences (SPSS version 12.0, Chicago IL).To Int J Diabetes Dev Ctries (April–June 2013) 33(2):115–119 117

Table 2 The comparison of means before and after olive, almond and walnut consumption by using one-way ANOVA at 95 % confidence

Olive (N021) Almond (N019) Walnut (N08) P valuea

Baseline 4 weeks Baseline 4 weeks Baseline 4 weeks Between groups

Weight (kg) 74.35±12.24 74.19±12.42 72.76±9.36 72.68±9.97 76.62±11.04 76.62±11.04 0.94 FBG (mg/dl) 180.86±60.75 157.76±65.23 172.79±66.96 160.58±62.21 154.75±46.22 161.75±41.94 0.35 HbA1c (%) 8.99±2.3 8.39±2.38 8.56±2.17 8.48±2.51 7.97±1.94 8.43±1.84 0.24 TG(mg/dl) 184.48±73.56 172.86±60.81 210.79±79.05 178.21±56.56b 165.5±46.22 188.13±51.33 0.11 TC(mg/dl) 220.14±28.01 199.19±29.77b 204.68±35.22 198.74±49.89 200.75±36.61 187.88±45.08 0.53 HDL(mg/dl) 61.57±18.09 58.95±19.2 50.84±15.9 57.37±18.72 46.5±11.79 46.5±11.21 0.27 LDL(mg/dl) 121.67±22.72 105.66±28.93b 113.18±31.7 105.93±46.94 121.15±42.01 103.75±47.32 0.78 Systolic BP 126.6±15.59 125±12.45 125.79±13.04 125.26±12.18 122.5±12.81 122.5±12.81 0.91 (mmHg) Diastolic BP 81.43±11.08 78.57±7.92 78.42±7.64 78.42±7.64 78.75±3.53 77.5±7.07 0.25 (mmHg) a One way ANOVA b Paired T-test used to compare before and after any trial (P<0.05)

Discussion We could not observe any significant change in BP, although Wien et al have reported significant reduction in In our study almond oil consumption decreased serum SBP after almond supplementation [25]. levels of TC, LDL and TG, but these reductions were The observation of the current study indicating olive oil statistically significant onlyinTGlevels.Nevertheless, could decrease TC and LDL-C significantly. That is in a recent meta-analysis [8] reviewed seven studies eval- accordance with several studies in general population [26, uating the effect of almonds on serum lipids and lip- 27] and diabetic patients [28]. oproteins and showed reductions in TC (7 %) and LDL Although metabolic studies have shown that olive oil (10 %) in individuals with baseline cholesterol 250 mg/ improves glycemic control [28] and insulin sensivity [29] dL. Kendall and co-workers also found that 50–100 g of in diabetic patients, we failed to show any significant asso- almonds/day lowered TC by 6 % and LDL by 9 % in hyper- ciation between FBG and HbA1c with olive oil consump- lipidemic men and women [19]. Hyson and coworkers tion in this study. showed that whole almonds and almond oil induce similar Olive oil consumption has been inversely associated with reductions in TC (4 %) and LDL (6 %) and concluded that the blood pressure in epidemiological studies [30] and has been cholesterol-lowering effect of almonds is due mainly to con- shown to lower blood pressure and reduce daily antihypertensive stituents of the lipid fraction [20]. drug dosage among hypertensives [31].In agreement with these Abbey et al. [21] observed decreases in total and LDL results, in our study SBP and DBP were decreased, but it was not cholesterol in normo-lipidemic men who consumed 84 g statistically significance. It may be attributable of duration of almonds/d compared with the values in men who consumed study which was not long enough to attain intended target. a –rich Western diet. In a study of hypercholes- Sabate et al. suggest that walnut consumption (from 4 gr terolemic men and women [22] the consumption of 100 g per week to 28 gr per day) would confer a cardio protective almonds/d produced a decrease in total and LDL-C concen- benefit by lowering the serum levels of LDL-C, TC and ratio trations compared with the consumption of a control diet of LDL-C to HDL-C in normal men [32]. Such a relation was high in saturated fat. seen in type 2 diabetic patients shown by Tapsell et al. In Lovejoy et al. observed a significant decrease in HDL-C Tapsell study the walnut group (30 gr per day for 6 months) in patients with type 2 diabetes who consumed almond- achieved a significantly greater HDL-C-to-TC ratio and HDL- enriched diets [23]. However, this reduction was not signif- C levels than the two other treatment groups (low fat, modi- icant in our study. fied low fat diet). A 10 % reduction in LDL was also achieved Jenkins et al. [24] showed almond could decrease post in the walnut group [33]. In our study TC and LDL-C de- prandial glycemia and insulinemia in healthy individuals. creased after walnut consumption, but it was not significant. Although in our study FBG and HbA1C decreased, but it Further, HDL-C did not change after walnut consumption that was not significant. contrasts with Tapsell et al. result. It might be due to longer 118 Int J Diabetes Dev Ctries (April–June 2013) 33(2):115–119 duration of walnut consumption in Tapsell study or low sam- 7. Spiller GA, Miller A, Olivera K, Reynolds J, Miller B, Morse SJ, ple size in our study. et al. Effects of plant-based diets high in raw or roasted almonds, or In current study there were no significant differences roasted almond on serum lipoproteins in humans. J Am Coll Nutr. 2003;22:195–200. after walnut consumption in body weight, FBG, HbA1c. 8. Fulgoni III VL, Abbey M, Davis P, Hyson D, Jenkins D, This is in line with the results of Tapsell et al. [33]. Walnut Lovejoy J, et al. Almonds significantly lower elevated blood consumption in our study could not change BP. Regardless, cholesterol and LDL-cholesterol but not HDL-cholesterol or several cross sectional studies suggest that consumption of triglycerides in human subjects: results of a meta-analysis. Proceedings of The Fourth International Congress on Vegetar- unsaturated fat decreases BP [34, 35]. However, controlled ian Nutrition. 2002;8–14. dietary trials have not provided clear support for the hypoth- 9. Jenkins DJA, Kendall CWC, Marchie A, Parker TL, Connelly PW, esis [36]. As Sabate et al. could not show any changes in BP Qian W, et al. Dose response of almonds on coronary heart disease in normotensive subjects [32]. risk factors: blood lipids, oxidized low-density lipoproteins, lipo- protein (a), homocysteine, and pulmonary nitric oxide a random- Our study showed no significant difference between al- ized, controlled, crossover trial. Circulation. 2002;106:1327–32. mond, walnut and olive oil on FBG, HbA1c, lipid profile 10. Kritchevsky D, Tepper SA, Czarnecki SK, Klurfeld DM. Athero- and BP in type 2 diabetic patients. genicity of animal and vegetable protein. Influence of the lysine to – The most important limitation was short duration of our arginine ratio. Atherosclerosis. 1982;41:429 31. 11. Stupans I, Kirlich A, Tuck KL, Hayball PJ. Comparison of radical study and small sample size. 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