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Effects of different forms of hazelnuts on blood lipids and α-tocopherol concentrations in mildly hypercholesterolemic individuals

Abstract

Background/Objectives:

Diets high in nuts reduce cholesterol, probably due to their favorable lipid profile and other bioactive substances. However, the physical form of the nut may be important as the cell wall of intact nuts may limit the hypocholesterolemic effect of nuts by reducing lipid bioavailability. Therefore, we investigated the effects on blood lipids of incorporating three different forms of hazelnuts (ground, sliced and whole) into the usual diet.

Subjects/Methods:

In a randomized crossover study with three phases, 48 mildly hypercholesterolemic participants were asked to consume 30 g of ground, sliced or whole hazelnuts for 4 weeks. Body weight, plasma total cholesterol (TC), low-density lipoprotein cholesterol (LDL-C), high-density lipoprotein cholesterol (HDL-C), triacylglycerol (TAG), apolipoprotein (apo) A1, apo B100 and α-tocopherol were measured at baseline and at the end of each dietary phase.

Results:

There were no significant differences in any outcome variable between the different forms of nuts (all P0.159). However, compared with baseline, mean values at the end of each hazelnut intervention were significantly higher for HDL-C (P=0.023) and α-tocopherol (P=0.005), and significantly lower for TC (P<0.001), LDL-C (P<0.001), TC:HDL-C ratio (P<0.001), apo B100 (P=0.002) and apo B100:apo A1 ratio (P<0.001), with no significant difference in body weight (P=0.813).

Conclusion

s: The ingestion of three different forms of hazelnuts equally improved the lipoprotein profile and α-tocopherol concentrations in mildly hypercholesterolemic individuals. Hazelnuts can therefore be incorporated into the usual diet as a means of reducing cardiovascular disease risk.

Introduction

The beneficial effects of regular nut consumption are well documented. Both epidemiological studies (Fraser et al., 1992; Kushi et al., 1996; Albert et al., 2002; Hu and Willett, 2002) and clinical trials (Kris-Etherton et al., 1999a; Rajaram et al., 2001; Sabate et al., 2003; Gebauer et al., 2008; Griel et al., 2008; Banel and Hu, 2009; Phung et al., 2009; Torabian et al., 2010) have consistently shown that nuts can have an important role in the management of plasma lipids, and reduce CVD morbidity and mortality. The American Heart Association recommends the consumption of nuts as a means of replacing saturated fat with unsaturated fats (Krauss et al., 2000). Similarly, the World Health Organization and National Heart Foundation of New Zealand recommend the consumption of 30 g of nuts as part of a cardio-protective diet (American Institute for Cancer Research and World Cancer Research Fund, 1997; New Zealand Guidelines Group, 2003).

The cis-unsaturated lipid content of nuts, as well as the presence of dietary fiber, plant protein, phytosterols, antioxidants, vitamins, minerals and other bioactive substances, is thought to be largely responsible for their cardio-protective properties (Kris-Etherton et al., 1999b; Segura et al., 2006; King et al., 2008; Sathe et al., 2009). However, recent research has questioned the proportion of nutrients that are readily released from nuts and are thus available for metabolism (Ellis et al., 2004; Berry et al., 2008; Mandalari et al., 2008; Traoret et al., 2008; Cassady et al., 2009). This term has been coined ‘bioaccessibility’. It has been suggested that the cell wall of intact nuts may limit the release of lipids and other nutrients available for digestion (Ellis et al., 2004).

Evidence of this concept is derived from in vitro digestion experiments in which lipid, protein and vitamin E from finely ground almonds were found to be more digestible than those from whole almonds (Mandalari et al., 2008). Further, short-term human trials report that whole nut consumption increases fecal fat losses, suggesting that some of the fat passes through the gastrointestinal tract undigested (Ellis et al., 2004; Hollis and Mattes, 2007; Traoret et al., 2008). This could potentially diminish the cholesterol-lowering properties of whole nuts. The release of these nutrients could theoretically be increased by breaking down the cell walls mechanically through slicing or grinding. To date no studies have examined the cholesterol-lowering properties of different forms of nuts, which potentially differ in nutrient bioaccessibility.

Although numerous clinical studies and reviews have consistently shown the hypocholesterolemic effects of several nuts, such as almonds (Sabate et al., 2003; Phung et al., 2009), macadamia nuts (Griel et al., 2008), peanuts (Kris-Etherton et al., 1999a), pecans (Rajaram et al., 2001), pistachio nuts (Gebauer et al., 2008) and walnuts (Banel and Hu, 2009; Torabian et al., 2010), few studies have investigated hazelnuts. To date, only three short-term intervention trials have assessed the effects of hazelnut supplementation on blood lipids (Alphan et al., 1997; Durak et al., 1999; Mercanligil et al., 2007). However, the sample size used in all three studies was relatively small and one of the studies was a poorly designed, non-randomized trial using a convenience sample (Durak et al., 1999). Whether the simple inclusion of hazelnuts into the usual diet can produce similar cholesterol-lowering effects to other tree nuts requires further investigation.

Therefore, the primary aim of this study was to compare the effects of consuming three different forms of hazelnuts (whole, sliced and ground) on blood cholesterol and α-tocopherol concentrations. Second, we assessed the effects of consuming hazelnuts for 4 weeks on these outcome variables.

Subjects and methods

Subjects

A total of 48 participants (20 males and 28 females) were recruited from the general public in Dunedin, New Zealand. To be eligible, participants were required to be healthy males or females aged between 18 and 65 years with plasma total cholesterol (TC) concentrations >4.8 mmol/l, but <8.0 mmol/l. Participants were excluded if they had asthma, food allergies, familial hyperlipidemia, a chronic disease, or were taking cholesterol-lowering medication or medication known to affect blood lipid concentrations. The study protocol was approved by the Human Ethics Committee of the University of Otago, New Zealand. All participants gave written informed consent. The trial was registered at the Australian New Zealand Clinical Trials Registry (http://www.anzctr.org.au/), registration number ACTRN012607000178448.

Nut variety and form

Ennis hazelnuts were purchased from a New Zealand producer (Uncle Joe's Walnuts, Blenheim, New Zealand). To obtain sliced hazelnuts, the whole hazelnuts were mechanically processed in a food processor (Robot Coupe CL50, Robot Coupe USA Inc., Jackson, MS, USA). To produce ground hazelnuts, the whole hazelnuts were initially ground in a food processor (Tasin 102, Ta Shing Food Machineries Co Ltd., Taichung, Taiwan) and then transferred to a Waring blender, in which the nuts were finely ground. A mechanical sieving process was carried out to ensure the hazelnuts were finely ground with a particle size <0.5 mm.

Study design

Our study was based on the National Heart Foundation of New Zealand recommendations, as per which people are recommended to consume 30 g of nuts, five times a week (New Zealand Guidelines Group, 2003). The participants were asked to consume 30 g of raw hazelnuts each day in place of a high-saturated-fat snack or ‘treat food’. A list of high-fat snacks, which contain similar energy and fat content to 30 g of hazelnuts, was obtained from ‘The Concise New Zealand Food Composition Tables’ (Athar et al., 2006). Participants were encouraged to replace these snacks with the study hazelnuts. A booklet containing hazelnut recipes and information about the study was given to all participants.

This study was conducted using a randomized, multiple crossover design with three dietary phases: ground, sliced and whole hazelnuts. All participants were randomly allocated to receive one of the three forms of hazelnuts for a period of 4 weeks, followed by a 2-week washout, during which they were instructed not to consume any hazelnuts, other nuts or nut products, and to consume snack foods prior to the study. This was repeated until all participants had consumed all forms of hazelnuts.

Compliance

Participants received a 4-week supply of hazelnuts, which were individually portioned into daily-serving-sized bags, at the beginning of each dietary phase. Compliance was assessed by measuring participants’ plasma α-tocopherol concentration, by weighing the bags returned at the end of each intervention phase, and by 3-day diet records completed during each experimental period. Participants were encouraged to continue their usual pattern of physical activity.

Dietary assessment

A 3-day (two weekdays and one weekend day) weighed diet record of all foods and beverages consumed was collected from participants at baseline and during each intervention phase using the same food scales (Salter Housewares Ltd., Kent, UK), accurate to within ±1 g. Detailed instructions on how to collect diet records were explained to each participant by a trained researcher.

All diet records were analyzed to provide an estimate of average daily energy and nutrient intake using the computer program Diet Cruncher (Marshall, 2003), which utilizes food composition data from the New Zealand Composition Database (New Zealand Institute for Crop and Food Research, 2006). All diet records were entered by the same person to ensure consistency in data-entry decisions.

Biochemical analysis

Fasting venous blood samples were taken at baseline, at the end of each dietary phase and at the end of each washout period. Two blood samples were taken during each testing period to account for intra-individual variation in blood cholesterol concentration. A total of 6 ml of venous blood was collected into Vacutainers (Becton Dickinson Diagnostics, Franklin Lakes, NJ, USA) containing dipotassium EDTA for analysis of plasma lipids, apolipoproteins (apo's) and α-tocopherol. Plasma aliquots were stored at −80 °C until analysis.

Plasma TC, high-density lipoprotein cholesterol (HDL-C) and triacylglycerol (TAG) concentrations were measured in all blood samples by enzymatic methods using kits and calibrators supplied by Roche Diagnostics (Mannheim, Germany) on a Cobas Mira Plus Analyser. HDL-C was measured in the supernatant following precipitation of apo B containing lipoproteins with phosphotungstate-magnesium chloride solution (Assmann et al., 1983). Plasma low-density lipoprotein cholesterol (LDL-C) concentration was calculated using the Friedewald formula (Friedewald et al., 1972). Apos A1 and B100 and α-tocopherol concentrations were measured in one of the two non-consecutive blood samples during each period. Apo A1 and apo B100 concentrations were determined by immunoturbidimetry using commercial kits from Roche Diagnostics. Plasma α-tocopherol was determined using the Agilent high-performance liquid chromatography system (1100 series, Agilent Technologies Inc., Santa Clara, CA, USA) based on the methods described by Thurnham et al. (1988).

Calibration and quality control was maintained by participation in the Royal Australasian College of Pathologists Quality Assurance Programme. The coefficients of variation for plasma TC, HDL-C and TAG during the study period were 1.08%, 3.10% and 1.77%, respectively. The coefficients of variation for measurements of apo A1 and apo B100 were 1.60% and 2.29%, respectively, and that for α-tocopherol was 5.63%.

Body weight and height

Height was measured at baseline to the nearest millimeter using a stadiometer. Body weight was measured at baseline, at the end of each dietary phase and at the end of each washout period on a calibrated electronic scale (Wedderburn Scales, Auckland, New Zealand) that measured to the nearest 0.01 kg.

Statistical analysis

A minimum of 40 participants would be required at the end of the study, in order to have 90% power to detect a clinically meaningful difference in plasma LDL-C concentration of 0.25 mmol/l between treatment diets (ground, sliced and whole hazelnuts), assuming a s.d. of 0.5 mmol/l and a correlation between repeated measurements of at least 0.55, using a two-sided test with the level of significance set to 5%. Allowing for an approximate 10% dropout rate, 44 participants were required at baseline.

The outcome variables included biochemical indices, energy and nutrient intake, and anthropometric measurements. Linear mixed models with a random participant effect to account for the underlying correlation between the repeated measures were used to examine the effect of different forms of hazelnuts on the continuous outcomes. The models included variables for assessing the influence of the intervention period and carryover effects into subsequent dietary periods.

The secondary measures of interest were the changes in mean response of the outcome variables from baseline to the end of the hazelnut interventions. The mean values for the end of ground, sliced and whole hazelnut interventions were used for this analysis. Paired t-tests were used to compare within-subject differences in outcome variables from baseline to the end of the interventions.

All statistical analyses were performed using Stata Intercooled version 9.0 (StataCorp, College Station, TX, USA). All tests were two-sided, with the level of statistical significance set at 5%.

Results

Of the 103 participants initially screened for the study, 45 participants did not meet the eligibility criteria due to the TC concentration being <4.8 mmol/l, and a further 10 participants declined to take part. The remaining 48 participants were randomized to receive ground, sliced and whole hazelnuts in a balanced order. Two participants (4%, one female and one male) dropped out from the study during the intervention. One participant withdrew after 2 weeks due to over-commitment, and one participant withdrew after 14 weeks due to a personal issue unrelated to the study. In total 46 of the 48 participants (27 females and 19 males) completed the 16-week intervention including washout periods. Participants ranged in age from 25 to 64 years with a mean (s.d.) age of 49.9 (9.4) years. The mean (s.d.) height at baseline was 169.2 (8.5) cm, mean (s.d.) weight was 74.4 (13.1) kg and mean (s.d.) BMI was 25.9 (3.5) kg/m2.

The degree of compliance as assessed by a recount of nut packages and 3-day diet records was reportedly 100% for ground hazelnuts, 100% for sliced hazelnuts and 99.4% for whole hazelnuts. There were no significant differences in compliance between treatments. Although these measures of compliance have limitations, the high rates of compliance are in agreement with the observed increase in plasma α-tocopherol concentration after each dietary phase.

The nutrient composition during each dietary phase is presented in Table 1. Energy intake, percentage of total energy from total fat, saturated fatty acids, monounsaturated fatty acids, protein and carbohydrate were not statistically significantly different across the three dietary treatments (all P0.073). Table 2 compares the difference in nutrient composition between the baseline diet and the dietary treatments. For this analysis the dietary records from the three dietary phases were combined and averaged. There were no statistically significant differences in the intake of total energy, saturated fatty acids, polyunsaturated fatty acids, protein and cholesterol between the baseline diet and hazelnut-enriched diets (all P0.357). Compared with baseline, there was an increase in vitamin E intake, and the percentage of total energy from total fat and monounsaturated fatty acid intake, whereas carbohydrate intake decreased significantly on the hazelnut-enriched diets (all P0.003).

Table 1 Nutrient composition during each dietary phase from the 3-day diet record
Table 2 Difference in nutrient composition between the baseline diet and the dietary treatments (n=42)

There were no statistically significant differences in plasma TC, LDL-C, HDL-C, total:HDL-C ratio, TAG, apo A1, apo B100 or α-tocopherol concentration between the dietary treatments (all P0.159, Table 3). There was no evidence of carryover effects for any of the biochemical variables except for HDL-C. HDL-C did not completely return to baseline levels after the interventions. However, compared with baseline, mean values at the end of the hazelnut interventions were significantly higher for HDL-C by 0.03 mmol/l (P=0.023) and for α-tocopherol by 1.32 μmol/l (P=0.005), while there was a significant reduction in TC by 0.19 mmol/l (P<0.001), LDL-C by 0.22 mmol/l (P<0.001), total:HDL-C ratio by 0.29 (P<0.001), apo B100 by 0.04 g/l (P=0.002) and apo B100:apo A1 ratio by 0.03 (P<0.001; Table 4). Plasma TAG (P=0.725) and apo A1 (P=0.749) concentrations were not statistically significantly different over the study period (Table 4).

Table 3 Effect of different forms of hazelnuts on biochemical indices and anthropometric measurements
Table 4 Effect of 3 months of hazelnut consumption on biochemical indices and anthropometric measurements (n=46)

The body weight of the participants did not statistically significantly differ between the dietary treatments (P=0.534; Table 3). Compared with baseline, body weight was not significantly different after consuming hazelnuts for 4 weeks (P=0.813; Table 4).

Discussion

The primary aim of this study was to assess the lipid-lowering properties of different forms of hazelnuts. It is hypothesized that the favorable effects of nuts on lipids and lipoproteins are due to their nutrient composition including unsaturated fatty acids and other bioactive substances (Kris-Etherton et al., 1999b; Segura et al., 2006; King et al., 2008; Sathe et al., 2009). However, recent studies have suggested that the cell wall of whole nuts may limit the bioaccessibility of these nutrients (Ellis et al., 2004; Mandalari et al., 2008; Traoret et al., 2008). Theoretically, the release of these nutrients may be increased by breaking down the cell walls of nuts through grinding or slicing, thereby allowing greater accessibility and imparting greater improvements in blood lipids and lipoproteins. Contrary to this hypothesis, our study failed to show a difference in the cholesterol-lowering properties of whole, sliced or ground nuts. All forms of hazelnuts improved biochemical indices to a similar extent.

Although a number of studies have reported increased amounts of lipid in the feces upon the consumption of whole nuts compared with ground nuts (Ellis et al., 2004) or nut oil (Traoret et al., 2008), our study suggests that the amount of fat potentially lost in the feces upon consumption of one serve of nuts (that is, 30 g) may be too small to significantly influence lipoprotein metabolism. This is further supported by our body weight data. One would expect that if substantial amounts of lipid, and thus energy, were lost in the stool, there would be differences in body weight upon consuming the different nut forms. However, body weight remained stable throughout the study. In addition, there was no difference in plasma α-tocopherol, a fat-soluble vitamin, between the three nut forms.

The postprandial work of Burton-Freeman et al. (2004) support our results. They compared the postprandial lipemic response to a meal containing whole almonds or almond oil. Although the almond oil meal produced an earlier peak in plasma TAG concentration (≈180 min) compared with the whole almond meal (≈300 min), area under the TAG response curve did not differ significantly among the test meals, indicating that there was no significant difference in total lipid uptake into the blood between the meals. In a similar study, Berry et al. (2008) found a significant difference in area under curve for TAG. These contrasting results are likely to be due to the threefold difference in fat provided by the nuts in these two studies. Berry et al. (2008) provided 96.5 g of whole almonds, whereas in the study by Burton-Freeman et al. (2004) 28 and 40 g of nuts were consumed by females and males, respectively. This suggests that when nuts are consumed in recommended amounts, that is, 30 g, there are no discernible differences in postprandial lipemia. The results of our study also indicate that this premise is true for cholesterol-lowering. It appears that any potential difference in the degree of the nutrient bioaccessibility from different forms of nuts is not of sufficient magnitude to influence their hypocholesterolemic effect when consumed in recommended amounts (American Institute for Cancer Research and World Cancer Research Fund, 1997; New Zealand Guidelines Group, 2003). Thus, metabolic changes resulting from differences in lipid bioaccessibility may only be apparent when a large amount of nuts are consumed. However, the vast majority of the general public in Western countries do not consume large quantities of nuts on a regular basis. The average intake of nuts among frequent nut consumers is 31 g/day in Europe and 21 g/day in America (King et al., 2008). Therefore, evaluating the bioaccessibility of larger quantities of nuts appears to be of little practical significance.

A secondary aim of this study was to investigate the lipid-lowering properties of hazelnuts. The results add to the growing body of evidence demonstrating the beneficial effects of nut consumption on blood lipid- and lipoprotein-mediated risk factors for CVD. Compared with baseline, mean values at the end of each hazelnut intervention were statistically significantly lower for TC, LDL-C, TC:HDL-C ratio and higher for HDL-C. Previous research on hazelnut supplementation has been limited to three studies. The results from this study strengthen the findings of previous smaller intervention trials that have shown similar improvements in blood lipid concentrations with the consumption of hazelnuts (Alphan et al., 1997; Durak et al., 1999; Mercanligil et al., 2007).

A remarkable finding of this study was that despite the baseline diets of participants being relatively healthy compared with the average Western diet, that is, they were relatively low in saturated fat (11% of total energy) and moderately high in fiber (29 g/day), the hazelnut-enriched diets still induced favorable changes in blood lipid profile. On the basis of previous meta-analyses (Gordon et al., 1989; Law and Wald, 2002; Baigent et al., 2005), it appears that as much as a 10–15% decrease in the risk of CVD would be expected given the plasma lipid and lipoprotein responses observed in the present study. It is equally encouraging that favorable effects on blood cholesterol were seen with the consumption of only 30 g of nuts per day. This seems to be a manageable amount for the general public to consume on a regular basis.

In addition to favorable changes in blood lipids, our study was the first to report that the addition of hazelnuts to the usual diet significantly increases plasma α-tocopherol concentration. Plasma α-tocopherol increased by 1.32 μmol/l, which is very similar to the increase of 1.31 μmol/l observed after consuming 27 g/day of almonds for 4 weeks (Jambazian et al., 2005). This indicates that, like almonds, hazelnuts are a rich, available source of vitamin E.

One limitation of the current study is that we did not include a control condition in which no nuts were consumed. However, we did provide a 2-week washout period between each condition, during which participants were provided with a break from consuming nuts. There was no evidence of a carryover effect for any of the biochemical indices except for HDL-C, suggesting that HDL-C may require a longer period to completely return to baseline.

One further limitation of this study is that mastication was not assessed. Previous research has suggested that the physical form of almonds may influence mastication and pre-swallowing particle size, which could affect the subsequent release of nutrients (Frecka et al., 2008). It is possible that mastication of the whole hazelnuts in the present study produced a pre-swallowing particle size similar to that of ground and sliced hazelnuts, thus eliminating any substantial differences in nutrient availability between nut forms.

In conclusion, this study shows that three different forms of hazelnuts, which differed in the degree to which they were mechanically processed, can equally improve plasma lipoprotein and α-tocopherol concentrations among mildly hypercholesterolemic individuals. Our data confirm the potential for hazelnuts to improve the blood lipid and lipoprotein concentrations in a way that would be expected to reduce the risk of CVD.

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Acknowledgements

We thank the participants for their commitment and enthusiasm in participating in this study. We thank Miss Michelle Harper and Mr Ashley Duncan for technical assistance in analyzing the blood samples. We also thank Mrs Margaret Waldron and Mrs Sue Vorgers for expert venipuncture and support of participants. This work was funded and supported by the National Heart Foundation of New Zealand Grant number 1234.

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Correspondence to R C Brown.

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Tey, S., Brown, R., Chisholm, A. et al. Effects of different forms of hazelnuts on blood lipids and α-tocopherol concentrations in mildly hypercholesterolemic individuals. Eur J Clin Nutr 65, 117–124 (2011). https://doi.org/10.1038/ejcn.2010.200

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Keywords

  • hazelnuts
  • form
  • bioaccessibility
  • lipids
  • α-tocopherol
  • cardiovascular disease

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