European Journal of Clinical Nutrition (2011) 65, 696–702 & 2011 Macmillan Publishers Limited All rights reserved 0954-3007/11 www.nature.com/ejcn

ORIGINAL ARTICLE The impact of pistachio intake alone or in combination with high-carbohydrate foods on post-prandial glycemia

CWC Kendall1,2,3, AR Josse4, A Esfahani1,2,5 and DJA Jenkins1,2,6

1Clinical Nutrition and Risk Factor Modification Center, St. Michael’s Hospital, Toronto, Ontario, Canada; 2Department of Nutritional Sciences, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada; 3College of Pharmacy and Nutrition, University of Saskatchewan, Saskatoon, Saskatchewan, Canada; 4Department of Kinesiology, McMaster University, Hamilton, Ontario, Canada; 5School of Medicine, New York Medical College, Valhalla, New York, USA and 6Department of Medicine, Division of Endocrinology and Metabolism, St Michael’s Hospital, Toronto, Ontario, Canada

Background/Objectives: Dietary strategies that reduce post-prandial glycemia are important in the prevention and treatment of diabetes and coronary heart disease (CHD). This may be achieved by addition of high-quality protein and fat contained in pistachio nuts, to carbohydrate-containing foods or meals. Subjects/Methods: A total of 10 healthy volunteers (3 males, 7 females); aged 48.3±6.4 years; Body mass index (BMI) 28.0±4.8 kg/m2 participated in two studies. Study 1 assessed the dose-response effect of 28, 56 and 84 g pistachios consumed alone or co-ingested with white bread (50 g available carbohydrate); Study 2 assessed the effective dose (56 g) of pistachios on post-prandial glycemia consumed with different commonly consumed carbohydrate foods (50 g available carbohydrate). Relative glycemic responses (RGRs) of study meals compared with white bread, were assessed over the 2 h post-prandial period. Results: The RGRs of pistachios consumed alone expressed as a percentage of white bread (100%) were: 28 g (5.7±1.8%); 56 g (3.8±1.8%); 84 g (9.3±3.2%), Po0.001. Adding pistachios to white bread resulted in a dose-dependent reduction in the RGR of the composite meal; 28 g (89.1±6.0, P ¼ 0.100); 56 g (67.3±9.8, P ¼ 0.009); 84 g (51.5±7.5, Po0.001). Addition of 56 g pistachios to carbohydrate foods significantly reduced the RGR: parboiled rice (72.5±6.0) versus rice and pistachios (58.7±5.1) (P ¼ 0.031); pasta (94.8±11.4) versus pasta and pistachios (56.4±5.0) (P ¼ 0.025); whereas for mashed potatoes (109.0±6.6) versus potatoes and pistachios, (87.4±8.0) (P ¼ 0.063) the results approached significance. Conclusions: Pistachios consumed alone had a minimal effect on post-prandial glycemia and when taken with a carbohydrate meal attenuated the RGR. The beneficial effects of pistachios on post-prandial glycemia could, therefore, be part of the mechanism by which nuts reduce the risk of diabetes and CHD. European Journal of Clinical Nutrition (2011) 65, 696–702; doi:10.1038/ejcn.2011.12; published online 2 March 2011

Keywords: pistachios; nuts; glycemic index; glycemic load; diabetes

Introduction relative post-meal glycemic and insulinemic responses to mixed meals (McMillan-Price et al., 2006; Wolever et al., Post-meal hyperglycemia is an independent risk factor for 2006), and evidence suggests that lowering the GI of a diet can cardiovascular disease (CVD) (Levitan et al., 2004) and a positively affect post-meal plasma glucose excursions (Opper- condition that is common in patients with type 2 diabetes man et al., 2004) and as such, potentially reduce the risk of (Akbar, 2003; Bonora et al., 2006). Dietary glycemic index CVD and diabetes (Salmeron et al., 1997a, b; Liu et al., 2000) (GI) and glycemic load have been shown to reliably predict the Epidemiological and interventional studies have linked the intake of tree nuts to reduced risk of CVD and diabetes (Jiang et al., 2002; Li et al., 2009; Mente et al., 2009). This Correspondence: Dr CWC Kendall, Department of Nutritional Sciences, protective effect may in part be explained by the favorable Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada, impact of nuts on serum lipids (Griel and Kris-Etherton, M5S 3E2. 2006), oxidative stress (Jenkins et al., 2002) and markers of E-mail: [email protected] Received 11 August 2010; revised 13 December 2010; accepted 13 January inflammation (Jiang et al., 2006; Ros, 2009). However, owing to 2011; published online 2 March 2011 their low available carbohydrate content and favorable fat and Pistachios improve post-prandial glycemia CWC Kendall et al 697 protein profiles, nuts may also decrease the risk of CVD and week with at least one day in between tests. On each test day, diabetes by reducing post-prandial blood glucose excursions. subjects came to the research clinic in the morning after This mechanism has only been examined in a few clinical a 10–14 h overnight fast. After being weighed and having studies, which have shown that almonds eaten alone have a a fasting blood sample obtained by finger-prick using minimal effect on blood glucose, and when different doses are autolancets (Microlet, Bayer, Toronto, Canada), the subject consumed with a carbohydrate meal, the post-prandial glucose then consumed a study meal within 10 min, and further response is attenuated (Josse et al., 2007). finger-prick blood samples were obtained at 15, 30, 45, 60, 90 To further test the potential impact of nuts on post-meal and 120 min after the start of the meal. Subjects were given a hyperglycemia, we conducted two studies using pistachio choice of one or two cups of water, tea or coffee with or nuts. The first assessed the dose-response effect of pistachios without milk. The beverage consumed by each subject on post-prandial blood glucose when consumed alone, remained the same for each of their study days. Subjects and consumed with a white bread meal. The second were instructed not to consume nuts the day before each study assessed the effect of pistachios on post-prandial study day. blood glucose excursions when added to other commonly The study protocol was approved by the Western consumed carbohydrate-rich foods. Institutional Review Board. Written informed consent was obtained from all subjects before the start of the study. Subjects and methods

Subjects Meals and palatability A total of 10 overweight but otherwise healthy subjects (3 The tests meals in study 1 consisted of three different doses ± ± males and 7 females), aged (mean s.d.) 48.3 6.4 years with (28, 56 and 84g) of pistachio nuts either consumed alone or ± 2 a body mass index of 28.0 4.8 kg/m , were studied. Subjects together with white bread (50 g available carbohydrate) were not taking any medications that would interfere with (Table 1). In study 2, 50 g available carbohydrate portions glucose metabolism. of rice, pasta or instant mashed potatoes were consumed with or without 56 g of pistachios (Table 1). The control Protocol white bread was also consumed on three different occasions Subjects were recruited through local advertisement and to allow calculation of the relative glycemic response (RGR). through the clinic volunteer roster. Each subject underwent The control white bread was baked in a bread maker in loaves treatments on separate days, performing up to two tests per containing 250 g available carbohydrate. The ingredients for

Table 1 Macronutrient composition of the carbohydrate foods and pistachio test meals in both studies

Test meal Amount Energy Protein Fat Total Dietary Available (g) (kcal) (g) (g) CHO (g) fiber (g) CHO (g)

Study 1 White bread (50 g available CHO) 104 245 8 2 53 3 50 Pistachio 28g 28 165 6 13 9 3 6 Pistachio 56g 56 330 12 26 18 6 12 Pistachio 84g 84 495 18 39 27 9 18 White bread þ 28 g pistachios 104 þ 410 14 15 62 6 56 28 White bread þ 56 g pistachios 104 þ 575 20 28 71 9 62 56 White bread þ 84 g pistachios 104 þ 740 26 41 80 12 68 84

Study 2 White bread (50 g available CHO) 104 245 8 2 53 3 50 Parboiled rice 63 217 4 0 50 0 50 Parboiled rice þ 56 g pistachios 63 þ 547 16 26 68 6 62 56 Pasta 73 246 9 1 53 3 50 Pasta þ 56 g pistachios 73 þ 576 21 27 71 9 62 56 Instant mashed potatoes 59 221 4 1 50 0 50 Instant mashed potatoes þ 56 g pistachios 59 þ 551 16 27 68 6 62 56

Abbreviations: CHO, carbohydrate; total CHO: dietary fiber and available CHO.

European Journal of Clinical Nutrition Pistachios improve post-prandial glycemia CWC Kendall et al 698 each loaf (250 ml warm water, 340 g all-purpose flour, 7 g sugar, 4 g salt and 6.5 g dry yeast) were placed into the bread 8.0 28 g 56 g maker according to instructions, and the machine was 7.0 turned on. After the loaf was prepared, it was allowed to 84 g 6.0 cool for an hour, and then weighed and after discarding the WB crust ends, the remainder was divided into portion sizes 5.0 containing 50 g available carbohydrate. These portions were * * * * 4.0 frozen before use, and reheated in a microwave before consumption. Study meals were given in random order. 3.0 Palatability was rated on a 100 mm visual analog scale 0 30 60 90 120 anchored with ‘very unpalatable’ at one end and ‘very palatable’ at the other. The higher the number, the higher 4.0 was the perceived palatability of the product. 28gP+WB 56gP+WB 3.0 84gP+WB * Blood glucose analysis WB Blood samples were stored at À20 1C until analysis, which 2.0 * took place within 4 days of collection. Blood glucose was * (mmol/L) Blood Glucose (mmol/L) * analyzed using a Yellow Springs Instrument Model 2300 1.0 * STAT (Yellow Springs, OH, USA). * * *

Incremental Blood Glucose 0.0 * 0306090120 Data analysis Time (min) Incremental areas under the plasma glucose curves were calculated using the trapezoid rule, ignoring area beneath Figure 1 (a) Glycemic response to white bread (WB; 50 g of available carbohydrate) and increasing doses of pistachios (28, 56, the baseline value. The GI or RGR was calculated by 84 g) consumed alone. *Significantly different from white bread expressing each subject’s glucose incremental areas under (Po0.01). (b) Incremental glycemic response to white bread alone the plasma glucose curves for the test food as a percentage of (WB; 50 g of available carbohydrate) or white bread consumed with the same subject’s average response after consuming the 28, 56 and 84 g of pistachios. *Significantly different from white bread (P 0.01). reference white bread. The mean of the resulting values was o the RGR. To calculate the RGR, based on the glucose scale (that is, GI of glucose ¼ 100), the RGR bread scale values were multiplied by 0.71. The blood glucose concentrations at each time point and the incremental areas under the respectively; Po0.001) (Table 2). Similarly, adding increasing plasma glucose curve values were subjected to repeated- doses of pistachios to white bread significantly reduced the measures analysis of variance, examining for the effect of glycemic response at 30, 45, 60 and 90 min for the 84 g dose test meal. After demonstration of significant heterogeneity, (Po0.01), at 45, 60 and 90 min for the 56 g dose (Po0.01) the significance of the differences between individual and at 45 and 60 min for the 28 g dose (Po0.01) in means was assessed using Tukey’s test to adjust for multiple comparison with the white bread control (Figure 1b). When comparisons. In addition, the significance of the differences pistachio nuts were added to the white bread meal, only the between blood glucose concentrations and increments for higher doses, 56 and 84 g, resulted in significant reductions each test food and white bread were assessed by paired t-test. in the RGR in comparison with the white bread control To estimate the RGR lowering potential of 1 g of pistachios, (67.3±9.8 (P ¼ 0.009) and 51.5±7.5 (Po0.001) versus 100, the change in RGR for each study meal was averaged and respectively) (Table 2). calculated per gram of pistachio consumed. In study 2, the addition of 56 g of pistachios to other commonly consumed carbohydrate rich foods (parboiled rice, pasta and potatoes) resulted in reduced glycemic Results responses (Table 3). When the pistachio meals were com- pared with their respective control meals, the addition of Relative glycemic response 56 g of pistachios significantly lowered the RGR of both Mean fasting blood glucose was identical before each test parboiled rice (72.5±6.0 versus 58.7±5.1; P ¼ 0.031) and meal within each series. The glycemic response to all three pasta (94.8±11.4 versus 56.4±5.0; P ¼ 0.025), whereas doses of pistachios was significantly lower at 30, 45, 60 and the reduction approached significance for instant mashed 90 min after ingestion in comparison with the white bread potatoes (109.0±6.6 versus 87.4±8.0; P ¼ 0.063) (Table 3; control (Po0.01) (Figure 1a). Furthermore, 28, 56 and 84 g of Figure 2). The mean reduction in glycemic response observed pistachios had significantly lower RGR in comparison with per gram of pistachios consumed was found to be 0.35 U, white bread (5.7±1.8, 3.8±1.8 and 9.3±3.2 versus 100, that is, 1 g of pistachios added to a food lowered the RGR of

European Journal of Clinical Nutrition Pistachios improve post-prandial glycemia CWC Kendall et al 699 Table 2 Study 1: Palatability and relative glycemic response (RGR) of white bread and pistachio meals (N ¼ 10)

Test meal Code Palatability (mm) RGR (bread scale) (RGR)a (glucose scale)

White bread (50 g CHO) WB 81.8±3.8 100a 71a Pistachio 28g 28P 83.5±4.7 5.7±1.8b — Pistachio 56g 56P 81.7±5.8 3.8±1.8b — Pistachio 84g 84P 81.1±5.7 9.3±3.2b — White bread þ 28 g pistachios WB þ 28P 79.8±4.3 89.1±6.0a 63.2±4.2a White bread þ 56 g pistachios WB þ 56P 77.9±5.8 67.3±9.8c 47.8±6.9b White bread þ 84 g pistachios WB þ 84P 75.2±5.9 51.5±7.5c 36.6±5.3b

Values within a column not sharing a common alphabet are significantly different (Po0.01). aRGR is presented in both the bread and s glucose scale; to convert the bread scale to the glucose scale multiply by 0.71 (Atkinson et al., 2008).

Table 3 Study 2: comparison of carbohydrate-containing foods consumed alone or with pistachios: palatability, iAUC and relative glycemic response (N ¼ 10)

Test Meal (Amounts) Code Palatability (mm) iAUC RGRa (bread scale)

White bread (g) WB 81.8±3.8a 188.1±22.4a 100a Rice Rice 79.9±5.1a 133.8±17.6b 72.5±6.0a Rice þ 56 g pistachios 56P þ rice 80.3±5.4a 109.9±15.7b 58.7±5.1b Pasta Pasta 76.7±4.6a 169.7±21.1a 94.8±11.4a Pasta þ 56 g pistachios 56P þ pasta 77.9±5.8a 112.2±22.0b 56.4±5.0b Instant mashed potatoes Potato 49.8±5.8b 203.8±27.5a 109.0±6.6a Instant mashed potatoes þ 56 g pistachios 56P þ potato 56.5±7.3b 161.6±23.1a 87.4±8.0a

Abbreviations: iAUC, incremental area under the glucose curve; RGR, relative glycemic response. Values not sharing a common alphabet are significantly different (Po0.05). aRGR is calculated based on bread scale; to convert to the glucose scale multiply by 0.71 (Atkinson et al., 2008).

140 for foods varying in composition and physical form (for example, beverages). 120

100 Palatability All test meals were well tolerated. Palatability scores of 80 * instant mashed potatoes with or without pistachios were * significantly lower when compared with all the other test 60 * meals (Tables 2 and 3). 40 Discussion

Relative Glycemic Response Relative 20 The present study is the first to assess the effect of pistachio 0 nuts on post-prandial glycemia. The findings confirm the

Rice very low glycemic responses to pistachios eaten alone would Pasta Potato be predicted on the basis of their low available carbohydrate Rice + P Pasta + P Pasta Potato + P Potato content (6 g per ounce) and on the results of other nuts White Bread (almonds) and oil seeds (peanuts), (Johnston and Buller,

White Bread + P 2005; Jenkins et al., 2006; Josse et al., 2007). Moreover, these Figure 2 Relative glycemic response to meals of white bread, data demonstrate that the addition of pistachios to foods rice, pasta or instant mashed potatoes containing 50 g of available with high available carbohydrate content reduces the overall carbohydrate consumed alone or with 56 g of pistachios. *The pistachio meal is significantly different from the respective non- glycemic impact of the foods studied (parboiled rice, pasta, pistachio control meal (Po0.01). white bread and mashed potatoes), despite increasing the overall available carbohydrate content. Of particular interest was the progressive reduction in bread glycemic response that food by 0.35 units on the glucose scale or 0.49 U on the with the increasing doses of pistachios. The graded glycemic bread scale. It must be pointed out that these results may response reduction of white bread has also been observed only apply to the foods tested and results may be different with almonds in a similar dose-response study conducted in

European Journal of Clinical Nutrition Pistachios improve post-prandial glycemia CWC Kendall et al 700 healthy individuals (Josse et al., 2007). Pistachios and other Sari et al., 2010), almonds (Griel and Kris-Etherton, 2006) nuts are energy-dense foods, and it has been recognized that and walnuts (Banel and Hu, 2009) can potentially reduce the gastric emptying is reduced by a high fat and energy load risk of CVD by improving serum lipid concentrations. such that the pylorus tends to regulate the flow of energy The low glycemic effect of nuts may provide a reason for into the duodenum (Hunt and Stubbs, 1975; Peracchi et al., the inclusion of nuts in diets aimed at reducing the risk of 2000). A study by Henry et al. (2008) found that the glycemic diabetes as the substitution of nuts for high GI carbohydrates response of bread can be lowered by the addition of any would reduce the glycemic load of the diet. Furthermore, it type of fat. Thus, increasing energy and fat load with an may be beneficial to advise people with Type 2 diabetes to increasing dose of pistachios would therefore tend to reduce consume nuts when they consume carbohydrates as part of the glycemic response in a dose-dependent manner as their daily diet to reduce the acute, post-prandial glycemic observed. It is also possible that the addition of pistachios impact of the meal. These recommendations are supported resulted in a reduction in carbohydrate absorption or altered by recent recommendations by both the American Diabetes the osmotic load and volume of the stomach, all of which Association and the International Diabetes Federation, would alter the post-prandial glycemic response. The acute which emphasize management of post-meal hyperglycemia benefits of pistachios on glycemia observed in the current as an important component in the management and preven- study may be indicative of long-term improvements in tion of Type 2 diabetes (American Diabetes Association glycemic control in light of recent evidence showing that (ADA), 2007; International Diabetes Federation, 2007). the addition of 60–100 g of pistachios to a Mediterranean Few studies have assessed the effect of nuts on diabetes risk diet for 4 weeks significantly reduced fasting glucose levels and control. Of the two cohort studies, only the results from in healthy adults in comparison with an unmodified the Nurses Health Study cohort (Jiang et al., 2002) but not Mediterranean diet (Sari et al., 2010). the Iowa Women’s Health Study (Parker et al., 2003) indicate The low post-meal glycemic response to pistachios is also that consumption of five or more servings per week of of particular interest in relation to recent studies, indicating nuts compared with rarely or no intake reduces the risk of that nut consumption was protective for CVD (Fraser et al., developing diabetes (relative risk ¼ 0.73, 95% confidence 1992; Hu et al., 1998; Ellsworth et al., 2001; Kris-Etherton interval, 0.60–0.89). Data from clinical studies indicate that et al., 2001; Albert et al., 2002). In each of these large nuts are beneficial in reducing CHD lipid risk factors in prospective studies, the Physicians’ Health Study (Albert patients with diabetes or the metabolic syndrome (Lovejoy et al., 2002), the Iowa Women’s Health Study (Ellsworth et al., 2002; Tapsell et al., 2004; Estruch et al., 2006; Li et al., et al., 2001), the Nurses’ Health Study (Hu et al., 1998) and 2009). In addition, some studies have found a significant the Adventist Health Study (Fraser et al., 1992), those who reduction in fasting insulin (Casas-Agustench et al., 2011; consumed the greatest amount of nuts versus those who Tapsell et al. 2009) or a significant improvement in insulin consumed the least had significant reductions in the risk of resistance (Casas-Agustench et al., 2011). However, none death from CVD, relative risk ¼ 0.53, 0.81, 0.65 and 0.52, have reported a significant reduction in glycated proteins as respectively. Clinically, post-meal hyperglycemia has been a marker of long-term glycemic control (Lovejoy et al., 2002; linked to endothelial dysfunction (Williams et al., 1998; Scott et al., 2003; Tapsell et al., 2004; Estruch et al., 2006; Kawano et al., 1999) and oxidative stress (Ceriello et al., Mukuddem-Petersen et al., 2007; Casas-Agustench et al., 2004); both of which are CVD risk factors. Post-prandial 2011; Tapsell et al., 2009; Ma et al., 2010). In light of recent lipemia has also been associated with an increased risk for evidence showing that the combination of the 2 h post-meal coronary heart disease (CHD). Although consumption of glucose levels and fasting blood glucose allow for better nuts would increase post-prandial lipemia, a study by Berry estimation of risk both for diabetes and CVD than the fasting et al. (2008) found that eating whole almonds resulted in a blood glucose alone (Sorkin et al., 2005; International lower post-prandial rise in plasma triglycerides compared Diabetes Federation, 2007); further studies that examine with almond oil or sunflower oil meals (74 and 58%, the effect of nuts on post-meal glycemia are warranted. respectively) that were balanced for macronutrients and We conclude that pistachios resulted in a minimal rise in fiber. In addition, nuts have a healthy fatty acid profile that blood glucose when fed alone over a wide range of is largely unsaturated and may provide other CHD benefits acceptable intake levels. Moreover, they also depress the beyond reducing the post-prandial glycemic impact of a blood glucose response to bread in a dose-dependent manner meal. Monounsaturated fat tends to raise high-density and the glycemic response of other carbohydrate rich meals, lipoprotein cholesterol when exchanged for carbohydrate, possibly related to their high fat, fiber and protein content. and the Mensink and Katan equation also attribute a small In view of their favorable fatty acid profile, their beneficial but important low-density lipoprotein cholesterol lowering effects on serum lipid levels and their low glycemic impact, it effect to monounsaturated fat (Mensink and Katan, 1992). seems now appropriate to assess their effects in longer-term This lowering of low-density lipoprotein cholesterol is studies of diabetes. These studies should aim at reducing the supported by a number of studies, which have shown that dietary glycemic load to assess whether nut consumption pistachios (Edwards et al., 1999; Kocyigit et al., 2006; results in reduced concentrations of long-term biomarkers of Sheridan et al., 2007; Gebauer et al., 2008; Kay et al., 2010; glycemic control, such as glycated proteins. However, it is

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