Do Dry Roasting, Lightly Salting Nuts Affect Their Cardioprotective Properties and Acceptability?

Eur J Nutr DOI 10.1007/s00394-015-1150-4

ORIGINAL CONTRIBUTION

Do dry roasting, lightly salting nuts affect their cardioprotective properties and acceptability?

Siew Ling Tey1 · Terryn Robinson2 · Andrew R. Gray3 · Alexandra W. Chisholm2 · Rachel Clare Brown2

Received: 3 September 2015 / Accepted: 23 December 2015 © Springer-Verlag Berlin Heidelberg 2016

Abstract Compared with baseline, consuming both forms of hazel- Purpose Previous studies have reported improvements nuts significantly improved HDL-cholesterol and apolipo- in cardiovascular disease (CVD) risk factors with the con- protein A1 concentrations, total-C/HDL-C ratio, and sys- sumption of raw nuts. However, around one-third of nuts tolic blood pressure without significantly changing body consumed are roasted and salted. Thus, it is important to composition. Acceptance ratings did not differ between determine whether roasting and salting nuts affect the forms of hazelnuts and remained high throughout the study. health benefits observed with raw nuts. This study aimed Conclusion Dry roasting and lightly salting nuts do not to compare the effects of consuming two different forms of appear to negate the cardioprotective effects observed with hazelnuts on cardiovascular risk factors and acceptance. raw nut consumption, and both forms of nuts are resistant Methods Using a randomised crossover design, 72 partic- to monotony. Public health messages could be extended to ipants were asked to consume 30 g/day of either raw or dry include dry roasted and lightly salted nuts as part of a heart roasted, lightly salted hazelnuts for 28 days each. CVD risk healthy diet. factors were measured at the beginning and end of each treatment period. “Desire to consume” and “overall liking” Keywords Hazelnuts · Roasting · Salting · for both forms of hazelnuts were assessed daily using a Cardiovascular disease · Acceptance 150-mm visual analogue scale. Results Body composition, blood pressure, plasma total and low-density lipoprotein-cholesterol, apolipoprotein A1 Introduction and B100, glucose and α-tocopherol concentrations did not differ between forms of hazelnuts (all P 0.054). High- Cardiovascular disease (CVD) is one of the leading causes ≥ density lipoprotein (HDL)-cholesterol (P 0.037) and tria- of mortality worldwide, with one-third of all global deaths = cylglycerol (P < 0.001) concentrations were significantly [1] and 30 % of all deaths in New Zealand attributed to lower following the consumption of dry roasted, lightly CVD [2]. Nuts are naturally low in sodium and high in salted hazelnuts when compared to the raw hazelnuts. unsaturated fatty acids, dietary fibre, plant protein, phytochemicals, vitamins and minerals, some of which may act synergistically to produce a wide range of health benefits * Rachel Clare Brown [3–5]. However, around a third of whole nuts consumed [email protected] are roasted and salted [6]. Thus, it is important to determine whether processing nuts affects their health benefits. 1 Clinical Nutrition Research Centre, Singapore Institute for Clinical Sciences, A*STAR, 14 Medical Drive, #07-02, Presently, the National Heart Foundation of New Zea- Singapore 117599, Singapore land recommends the regular consumption of 30 g of raw 2 Department of Human Nutrition, University of Otago, PO nuts on the basis of their cardioprotective effect [7]. Two Box 56, Dunedin 9054, New Zealand studies reported that the palatability of roasted and salted 3 Department of Preventive and Social Medicine, University nuts was significantly higher than raw nuts when meas- of Otago, PO Box 913, Dunedin, New Zealand ured in a single session [8, 9]. If health outcomes are not

1 3 Eur J Nutr compromised, recommending consuming nuts in these examining the health effects of consuming hazelnuts are more preferred forms may provide an effective approach to relatively sparse despite the fact that hazelnuts are the sec- improving cardiovascular health among the general popula- ond most common nut produced worldwide [23]. In addition. This is important given the results of several studies tion, no studies have examined the effects of dry roasted which have reported the prevalence of whole nut consump- nuts, which are only lightly salted. Lightly salted nuts are tion on any given day to be only 6.9 % in New Zealand (of now commercially available and provide an alternative which approximately half were roasted forms) [6], 6.9 % in to more heavily salted varieties. We hypothesise that this Europe [10] and 6.0 % in the USA [11]. form of nut may be acceptable to consumers and will con- To our knowledge, only three clinical trials have com- fer similar health benefits to raw nuts. Therefore, the objec- pared the effects of consuming processed nuts on car- tive of this randomised crossover study was to compare the diovascular risk factors [12–14]. All three studies were effects of consuming a daily 30 g portion of each of whole conducted using a randomised, parallel design with inter- raw hazelnuts and dry roasted, lightly salted hazelnuts for vention periods ranging from 4 weeks [13, 14] to 12 weeks 28 days on CVD risk factors and acceptance. [12]. Spiller et al. [14] used 100 g/day of raw almonds, roasted almond butter or roasted salted almonds (209 mg of sodium per 100 g), while the other studies used 42 g/ Methods day (salted, unsalted, honey roasted, spicy) [12] or 56 g/ day (raw unsalted, roasted unsalted, roasted salted, honey Study design roasted or butter) [13] of peanuts. These studies showed no significant differences in blood lipid profiles [12–14], blood This study was conducted using a randomised, crossover pressure [12, 14], blood glucose and insulin [12] between design with two treatment periods: raw hazelnuts and dry different forms of nuts. It is important to highlight that the roasted, lightly salted hazelnuts. During the 2-week run-in authors did not report the methods used for roasting nuts period, participants were asked to consume their habitual and these studies had relatively small sample sizes (n < 27 diet excluding nuts and nut products. Following this, par- per single flavour treatment) and so might not have been ticipants were randomly allocated to receive one of the adequately powered to detect small but clinically important two treatments with the orders balanced. Each treatment effects. In addition, McKiernan et al. [13] did not report period was 4-week duration separated with a 2-week wash- the between-groups analysis on blood pressure. Thus, it out period. Participants were asked to continue to consume remains unclear whether roasting and salting nuts influence their habitual diet during the treatment and washout peri- different health outcomes. ods. However, they were asked to continue not consuming In addition to investigating the cardioprotective effects any nuts or nut products beyond the hazelnuts supplied for of nuts, it is also important to examine the acceptability and the study. Both forms of hazelnuts were packaged into indi- sustainability of the recommendation to consume nuts on vidually portioned, 30-g serving-sized bags. The amount of a daily basis. To date, only four clinical trials have investi- nuts chosen in this study was based on the National Heart gated the effects of regular consumption of raw hazelnuts Foundation of New Zealand recommendations [7]. on participants’ “desire” and “liking” [15–18]. These studies showed that daily consumption of between 30 and 42 g Participants of raw hazelnuts for periods between 5 days and 12 weeks did not appear to result in monotony, i.e. a decline in Seventy-two participants were recruited from the general acceptance over time. One recent study examined the “lik- public of Dunedin, New Zealand. Recruitment was through ing” for peanuts consumed as either a single flavour or a advertisements in the community paper, local newspa- variety of flavours daily for 12 weeks [19]. This study per, the University of Otago Staff Bulletin, and the distri- reported a significant decline in liking for peanuts over bution of flyers around the University of Otago campus, 12 weeks, with no difference between the single and mixed Otago Polytechnic campus and local supermarkets. Par- flavours. However, the authors did not report the actual lik- ticipants from previous studies within the Human Nutri- ing values for the different peanut flavours, which makes tion Department, who had provided permission to be con- the interpretation difficult [19]. With the limited evidence tacted for participation in future research projects, were to date, it is of interest to determine whether the sustained also contacted. The inclusion criteria for participation in acceptance observed with raw nut consumption can be gen- the intervention were free-living individuals aged 18 years eralised to other forms of nuts, e.g. roasted and salted nuts. and above. The exclusion criteria were people who: have The cardiovascular health benefits associated with con- asthma, allergies or intolerances to nuts, familial or second- suming almonds [20], pistachio nuts [21] and walnuts ary hyperlipidaemia, major chronic disease, or pacemak- [22] have been extensively investigated. However, studies ers or implanted defibrillators; or were current smokers,

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Table 1 Energy and nutrient composition of hazelnuts used in the to 160 °C. Therefore, our roasting process is comparable study to those seen with commercial roasting and is unlikely to Raw hazelnuts Dry roasted, lightly substantially change the nutrient composition of the nuts. (30 g) salted hazelnuts (30 g) To assess the quantity of sodium added to the processed hazelnuts, the nutritional composition of both forms of Energy (kJ) 846 846 hazelnuts were analysed on two occasions in four samples Protein (g) 4.7 4.6 (AssureQuality, Auckland, New Zealand). Both hazel- Fat (g) 18.5 18.4 nuts had very similar nutrient composition, except for Saturated fat (g) 1.3 1.3 sodium content (Table 1). Raw hazelnuts contained 3.9 mg Monounsaturated fat (g) 14.6 14.3 of sodium per 30 g (13 mg per 100 g), while dry roasted, Polyunsaturated fat (g) 2.6 2.9 lightly salted hazelnuts contained 39.9 mg of sodium per Carbohydrate (g) 4.7 5.2 30 g (133 mg per 100 g). Sodium (mg) 3.9 39.9 The dry roasted, lightly salted treatment was designed to α-Tocopherol (mg) 5 4.3 provide a similar quantity of sodium as commercially available lightly salted nuts, i.e. 145 mg of sodium per 100 g (Mother Earth, Hamilton, New Zealand), and sodium lev- pregnant or lactating women, or taking cholesterol-lower- els below that of commercially salted nuts. On average, ing medication or medication known to affect blood lipid commercially available salted nuts (cashew, mixed, pea- concentrations. nuts, beer nuts) contain 568 mg of sodium per 100 g (Eta, The present study was conducted according to the guide- Manukau City, New Zealand; Homebrand, Auckland, New lines laid down in the Declaration of Helsinki, and all Zealand; Mother Earth, Hamilton, New Zealand; Signature procedures involving human subjects were approved by Range, Auckland, New Zealand). the Human Ethics Committee of the University of Otago, New Zealand. Written informed consent was obtained Compliance from all subjects. The trial was registered for inclusion in the Australia New Zealand Clinical Trials Registry Compliance was measured in two ways: by weighing the (ANZCTR) (http://www.anzctr.org.au/), registration code bags returned at the end of each treatment and by measur- ACTRN12611000838910. ing plasma α-tocopherol concentrations. However, it should be noted that plasma α-tocopherol concentrations reflect Nut preparation relatively short-term changes in dietary α-tocopherol [28, 29]. Whole raw, unsalted, Whiteheart hazelnuts were purchased from a nut grower (Uncle Joe’s Walnuts and Hazelnuts, Dietary assessment Blenheim, New Zealand). Hazelnuts were shelled and delivered to the researcher 4 weeks before the intervention All participants completed a 3-day diet record (3-DDR), began for processing and packaging. All nuts used in the including two weekdays and one weekend day, during the study were stored at room temperature in darkness before baseline period and during each treatment period (three opening. 3-DDRs in total). Diet records were used to assess par- To obtain dry roasted, lightly salted hazelnuts, a known ticipants’ reported nutrient and energy intakes, with food quantity of raw hazelnuts were first soaked in a salt–water intake recorded at the time of consumption. Participants solution for 30 s and then drained for a further 30 s. One were provided with electronic scales (Salter Electronic, part iodised table salt (Pams, Auckland, New Zealand) to Salter Housewares Ltd., Kent, UK) to weigh food and five parts warm, filtered tap water was used to prepare the attended a 30-min training session by a dietitian outlin- salt–water solution. The hazelnuts were then spread evenly ing how to complete the diet record. The diet records were over oven trays and roasted in a standard preheated oven entered into a computer programme, Diet Cruncher [30], (Fisher & Paykel, Auckland, New Zealand) at 100 °C for which uses food composition data from the New Zealand 15 min. Each tray was shaken at 5-min intervals during the Plant and Food Research [31]. roasting process. Upon conclusion of the roasting process, the hazelnuts were removed from the oven and left to cool. Physical activity Previous research has reported that the nutrient composition of nuts remains largely unchanged when the roasting Physical activity was monitored using New-Lifestyles temperature is below 140 °C [24–27]. The temperatures NL-1000 accelerometers (New-Lifestyles Inc., Lee’s Sum- used for commercial dry roasting of nuts range from 100 mit, MO, USA) for seven consecutive days at baseline and

1 3 Eur J Nutr during each treatment period (three sets of measurements pressure monitor (Model HEM-907, Kyoto, Japan). Par- in total). The daily and 7-day average number of steps and ticipants were seated for approximately 5 min before blood distance were recorded from the accelerometers after they pressure was measured. were returned by each participant. Anthropometric measurements Biochemical analysis Height was measured at baseline using standard procedures Two fasting blood samples were collected from each par- to the nearest millimetre using a stadiometer. Participants ticipant, following a 12-h overnight fast, during the clinic stood on the stadiometer, with heels against the backboard. visits before and after each treatment period (eight samples The head block was lowered to rest on the top of the head. in total). An experienced nurse collected two blood samples Participants were asked to take a deep breath before the on non-consecutive days in one 10 mL Vacutainer contain- height measurement was taken. Body weight and body ing dipotassium EDTA for analysis of plasma lipids, apoli- composition were assessed before and after each treatment poproteins and α-tocopherol, and one 5 mL Vacutainer period, in the same visit in which blood samples were col- containing fluoride and oxalate for the analysis of plasma lected. Participants were barefoot and wore light clothing glucose (Belton Dickinson Diagnostics, Franklin Lakes, for these measurements. Body weight and body composi- NJ, USA). Vacutainers were inverted and stored in a chilly tion were measured using a bioelectrical impedance ana- bin containing frozen ice-pads after blood samples were lyser (Tanita, Model TFB-310, Tokyo, Japan). drawn. All blood samples were separated by centrifugation at 3000g, for 15 min at 4 °C within 3 h of being drawn. Acceptance for nuts Plasma aliquots were stored in Eppendorf tubes at 80 °C − until analysis. “Overall liking” at the pre- and post-exposure tasting Plasma total cholesterol, high-density lipoprotein session (HDL)-cholesterol and triacylglycerol (TAG) concentrations were measured in all blood samples by enzymatic The pre- and post-exposure tasting sessions were held in methods using kits and calibrators supplied by Roche Diag- the sensory laboratory, Department of Food Science, Uni- nostics (Mannheim, Germany) on a Cobas Mira Plus Ana- versity of Otago. The pre-exposure tasting session was lyser. HDL-cholesterol was measured using the supernatant held at the end of the 2-week baseline period, while the following the precipitation of apolipoprotein B containing post-exposure session was held immediately upon the con- lipoproteins with phosphotungstate–magnesium chloride clusion of the study. At the pre-exposure tasting session, solution [32]. Plasma low-density lipoprotein (LDL)-cho- participants were given a detailed briefing on the nature lesterol concentrations were calculated using the Friedwald of the study and the importance of complying with the formula [33]. Plasma apolipoprotein A1, B100, and glu- instructions. Both taste testing sessions involved a 20-min cose concentrations were determined by using commercial product assessment acceptability test. Participants were kits from Roche Diagnostics (Mannhein, Germany) on a seated in individual sensory booths and presented with Cobas Mira Plus Analyser. Plasma glucose was measured eight food items, water at room temperature and a record- using the hexokinase method as described by Neeley [34]. ing ballot. The food items were selected based on their Plasma α-tocopherol was measured using the Agilent high- fat, sodium and sugar contents. The food items included performance liquid chromatography system (1100 series, the raw hazelnuts and the dry roasted, lightly salted hazel- Agilent Technologies Inc., Santa Clara, CA, USA) based nuts used in the intervention, short bread (high-fat, sweet), on methods described by Thurnham et al. [35]. peanuts (high-fat, salty), chocolate (medium-fat, sweet), Calibration and quality control were maintained by par- potato crisps (medium-fat, salty), raisins (low-fat, sweet) ticipation in the Royal Australasian College of Pathologists and rice crackers (low-fat, salty). Before starting the Quality Assurance Programme. The inter-assay coefficient taste testing and between each sample, participants were of variation for each outcome measurement was total cho- asked to rinse their mouths with water. Participants were lesterol: 3.31 %, HDL-cholesterol: 5.82 %, TAG: 4.31 %, instructed both visually and verbally how to rate their apolipoprotein A1: 3.35 %, apolipoprotein B100: 2.71 %, “overall liking” on a 150-mm visual analogue scale (VAS) glucose: 3.22 % and α-tocopherol: 2.81 %. anchored with “Dislike extremely” on the left-hand side (0 mm), “Neither like nor dislike” in the middle (75 mm) Blood pressure and “Like extremely” on the right-hand side of the scale (150 mm). Participants were asked to wait for at least At each clinic visit, blood pressure was measured in trip- 1 min between each sample and asked not to converse dur- licate and the mean was recorded, using an Omron blood ing testing.

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“Desire to consume” and “overall liking” during the normality and/or homoscedasticity. Paired t tests were then intervention used to explore within-group changes for nutrient intakes, physical activity, biochemical indices, blood pressure, body Throughout each 4-week treatment phase, participants composition and acceptance before and after each 4-week were asked to complete the exposure ballots at the time intervention to assist interpretation of between-groups of consuming the daily 30 g allowance of hazelnuts. Par- effects and as within-group effects of interest in themselves. ticipants were able to consume the daily portion of hazel- Similarly, linear mixed models were used to compare rat- nuts, as and when desired, providing the daily allowance ings of “desire to consume” and “overall liking” between was not shared with others. Nuts were available for family the two forms of hazelnuts with random participant and par- and friends upon the conclusion of the study. At the time of ticipant-nut form effects. The association between ratings of consuming the hazelnuts, participants were asked to record “desire to consume” and “overall liking” was assessed using the time of day when and the location where the nuts were the Pearson’s correlation coefficient. consumed. They were then asked to eat one hazelnut and All analyses were based on modified intention to treat rate their “Desire to consume” on a 150-mm VAS anchored principles (using all available data for each analysis) and with “Strong desire not to consume” on the left-hand side were conducted using Stata 11.1 (StataCorp, College Sta- (0 mm) and “Strong desire to consume” on the right-hand tion, TX, USA). All tests were two-sided with the level of side of the scale (150 mm). Next, participants were asked statistical significance set at 5 %. In some cases, non-signif- to consume the rest of their daily allowance of hazelnuts icant tendencies (0.05 P < 0.10) are highlighted. ≤ and rate their “overall liking” using the same 150-mm VAS that was used in the laboratory-based tasting sessions. Results Statistical analysis Participant characteristics In order to have 80 % power to detect at the 2-sided 0.05 level, a difference of 0.25 mmol/L in LDL-choles- Seventy-eight subjects were initially recruited and screened terol between groups, assuming a standard deviation of to participate in the study. Five participants withdrew prior 0.65 mmol/L and a correlation between baseline and fol- to the collection of baseline measurements and randomisa- low-up values of 0.5 or higher but without making any tion due to commitments unrelated to the study, and one assumptions about the correlations between treatment participant was later discovered to have diabetes and was effects for the same participant, 80 participants would be retrospectively excluded as not meeting the inclusion cri- required to provide full data. teria. The remaining 72 participants completed the study, The primary analyses were to compare the effect of con- which consisted of 48 females and 24 males. The mean suming two different forms of hazelnuts on biochemical (SD) age was 45.5 (14.8) years, and the mean (SD) BMI indices (plasma total, LDL- and HDL-cholesterol, TAG, was 26.7 (4.69) kg/m2. apolipoprotein A1 and B100, and α-tocopherol), dietary data (energy, total fat, saturated fat, monounsaturated fat, Compliance polyunsaturated fat, protein, carbohydrate, alcohol, cholesterol, dietary fibre and vitamin E), physical activity (steps Compliance by weighing the returned bags was high and and distance), blood pressure, body weight and composition similar for both forms of hazelnut: 98.4 % of raw hazel- (body weight, BMI, fat mass, fat-free mass, percentage body nuts and 98.1 % of dry roasted, lightly salted hazelnuts fat) and acceptability data (“desire to consume” and “overall were consumed using this method. An objective measure of liking” ratings). Linear mixed models, with a random partic- compliance through the assessment of plasma α-tocopherol ipant effect to account for the repeated measures, were used concentrations was also used. Plasma α-tocopherol con- to examine the between-groups effects of the two different centrations increased significantly following the raw hazel- forms of hazelnuts on the continuous outcomes. These mod- nut-enriched diet (P 0.008), with a tendency for the dry = els included terms for baseline values so that comparisons roasted, lightly salted hazelnut-enriched diet (P 0.099), = between the forms of hazelnuts were in terms of differences supporting the high compliance rate observed by the afore- in changes and the intervention period (first or second) to mentioned methods. adjust for any influence of this on outcomes. Interactions between nut type and the intervention period were investi- Dietary data gated to ensure there was no evidence for carryover effects. Log transformations were used for both final and baseline Seventy-one of the 72 study participants completed a values of dependent variables where this improved residual 3-DDR at baseline and during the two treatment phases.

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Table 2 Energy and nutrient intakes during each dietary phase (n 71) = Baseline Raw hazelnuts† Dry roasted, lightly salted hazelnuts† Adjusted between-groups Change End Baseline Change End Baseline P value‡ = − = − Total energy (kJ) 9166 (8500, 9832) 81.5 ( 431, 594) 239 ( 791, 312) 0.079 − − − Protein (g) 89.8 (80.8, 98.7) 1.6 ( 9.6, 6.4) 3.7 ( 10.6, 3.3) 0.422 − − − − % of total energy 16.3 (15.3, 17.3) 0.3 ( 1.3, 0.8) 0.2 ( 1.1, 0.8) 0.736 − − − − Total fat (g) 81.4 (74.8, 88.0) 10.4 (4.1, 16.6)** 6.7 (0.4, 13.0)* 0.177 % of total energy 33.4 (31.8, 35.1) 4.1 (2.3, 5.9)*** 4.0 (2.4, 5.6)*** 0.889 SFA (g) 31.6 (28.8, 34.4) 1.4 ( 4.2, 1.4) 1.8 ( 4.7, 1.1) 0.756 − − − − % of total energy 13.0 (12.2, 13.8) 0.7 ( 1.6, 0.2) 0.4 ( 1.3, 0.5) 0.442 − − − − MUFA (g) 28.1 (25.5, 30.8) 10.2 (7.6, 12.7)*** 7.9 (5.3, 10.4)*** 0.056 % of total energy 11.5 (10.7, 12.4) 4.2 (3.3, 5.1)*** 3.9 (3.1, 4.7)*** 0.323 PUFA (g) 12.4 (11.0, 13.8) 2.0 (0.7, 3.2)** 0.8 ( 0.6, 2.3) 0.027 − % of total energy 5.11 (4.63, 5.60) 0.7 (0.2, 1.1)** 0.4 ( 0.1, 0.9) 0.123 − Carbohydrates (g) 261 (238, 284) 16.5 ( 34.1, 1.1) 27.9 ( 46.6, 9.2)** 0.066 − − − − − % of total energy 47.2 (45.4, 49.0) 3.6 ( 5.5, 1.8)*** 4.3 ( 6.1, 2.5)*** 0.397 − − − − − − Sugars (g) 113 (100, 126) 7.7 ( 17.3, 1.8) 11.9 ( 21.5, 2.3)* 0.279 − − − − − Alcohol (g) 9.68 (5.92, 13.4) 0.7 ( 3.7, 2.3) 0.7 ( 2.1, 3.4) 0.338 − − − % of total energy 3.22 (1.97, 4.47) 0.4 ( 1.4, 0.6) 0.3 ( 0.8, 1.3) 0.168 − − − Cholesterol (mg) 269 (235, 303) 6.6 ( 45.9, 32.6) 3.7 ( 34.5, 42.0) 0.607 − − − Dietary ﬁbre (g) 26.5 (23.6, 29.4) 0.5 ( 1.2, 2.2) 1.3 ( 3.2, 0.6) 0.036 − − − Sodium (mg) 3025 (2701, 3349) 261 ( 526, 4) 491 ( 777, 205)** 0.032 − − − − − Vitamin E (mg) 10.9 (9.7, 12.1) 4.4 (3.4, 5.3)*** 4.0 (2.9, 5.0)*** 0.344

Data are presented as mean (95 % CI) MUFA monounsaturated fatty acids, PUFA polyunsaturated fatty acids, SFA saturated fatty acids † Results were derived from paired t tests. Signiﬁcantly different from baseline: * P < 0.05; ** P < 0.01; *** P < 0.001 ‡ Follow-up values between treatments were determined by using linear mixed models controlling for baseline value and intervention period

Nutrient intakes at baseline and at the end of each treat- concentrations, systolic blood pressure, body composition, ment phase are summarised in Table 2. The only signifi- and physical activity level between the two forms of hazel- cant differences between the two treatments were polyun- nuts (all P 0.125). However, HDL-cholesterol (1.45 vs. ≥ saturated fat (P 0.027), dietary fibre (P 0.036) and 1.41 mmol/L; P 0.037) and TAG (1.12 vs. 1.03 mmol/L; = = = sodium (P 0.032) intakes. The reported grams of poly- P < 0.001) concentrations were significantly higher follow- = unsaturated fat and dietary fibre consumed were signifi- ing the raw hazelnuts compared to the dry roasted, lightly cantly higher when consuming raw hazelnuts compared to salted treatment. In addition, there was a non-significant dry roasted, lightly salted hazelnuts. On the other hand, tendency for higher diastolic blood pressure following the the sodium intake when consuming raw hazelnuts was consumption of raw hazelnuts compared with dry roasted significantly higher compared to the dry roasted, lightly lightly salted hazelnuts (72.6 vs. 71.5 mmHg; P 0.054). = salted hazelnuts (2764 vs. 2534 mg, respectively). When Compared with baseline, the values at the end of both compared to baseline, energy derived from total fat and hazelnut interventions were significantly reduced for total- monounsaturated fat, as well as vitamin E intake was sig- C/HDL-C ratio (both P < 0.001) and systolic blood pres- nificantly higher, while energy from carbohydrate was sig- sure (both P 0.034). On the other hand, HDL-cholesterol ≤ nificantly lower when the diets were supplemented with (both P < 0.001) and apolipoprotein A1 (both P 0.005) ≤ hazelnuts (all P < 0.001). concentrations increased significantly from baseline as a result of hazelnut consumption. In addition, compared to Clinical outcomes baseline, plasma α-tocopherol concentration was higher when the diet was supplemented with raw hazelnuts The clinical outcomes at baseline and at the end of each (P 0.008) with a tendency for higher concentrations for = treatment phase are summarised in Table 3. There was the dry roasted, light salted hazelnuts (P 0.099). The = no evidence of a difference in total cholesterol, LDL- change in body weight from baseline to the end of hazel- cholesterol, apolipoproteins, glucose and α-tocopherol nut interventions was close to zero ( 0.03 to 0.13 kg). − − 1 3 Eur J Nutr

Table 3 Effects on clinical outcomes following each dietary phase (n 72) = Baseline Raw hazelnuts† Dry roasted, lightly salted hazelnuts† Adjusted between-groups Change End Baseline Change End Baseline P value‡ = − = − Biochemical indices Total-C (mmol/L) 5.11 (4.84, 5.38) 0.02 ( 0.10, 0.14) 0.05 ( 0.16, 0.06) 0.125 − − − LDL-C (mmol/L) 3.25 (3.01, 3.49) 0.11 ( 0.20, 0.01)* 0.08 ( 0.17, 0.02) 0.447 − − − − − HDL-C (mmol/L) 1.35 (1.27, 1.43) 0.10 (0.06, 0.13)*** 0.06 (0.03, 0.08)*** 0.037 Triacylglycerol (mmol/L) 1.10 (1.00, 1.20) 0.02 ( 0.03, 0.12) 0.07 ( 0.12, 0.01)* <0.001 − − − − Total-C/HDL-C ratio 3.97 (3.69, 4.24) 0.21 ( 0.32, 0.10)*** 0.18 ( 0.28, 0.08)*** 0.557 − − − − − − apoA1 (g/L) 1.59 (1.53, 1.66) 0.06 (0.03, 0.10)** 0.04 (0.01, 0.07)** 0.249 apoB100 (g/L) 0.87 (0.82, 0.93) 0.01 ( 0.04, 0.01) 0.01 ( 0.03, 0.01) 0.848 − − − − Glucose (mmol/L) 4.82 (4.72, 4.92) 0.02 ( 0.11, 0.07) 0.01 ( 0.07, 0.06) 0.751 − − − − α-Tocopherol (µmol/L) 30.2 (28.5, 32.0) 1.22 (0.34, 2.10)** 1.06 ( 0.20, 2.32) 0.743 − Blood pressure Systolic (mmHg) 124 (120, 128) 2.0 ( 3.8, 0.2)* 2.9 ( 4.6, 1.1)** 0.316 − − − − − − Diastolic (mmHg) 73.5 (71.1, 75.9) 0.8 ( 1.9, 0.3) 2.0 ( 3.3, 0.7)** 0.054 − − − − − Pulse (bpm) 64.9 (63.0, 66.9) 0.04 ( 1.19, 1.11) 0.82 ( 2.28, 0.64) 0.257 − − − − Body composition Body weight (kg) 76.7 (73.3, 80.2) 0.13 ( 0.45, 0.19) 0.03 ( 0.31, 0.25) 0.569 − − − − BMI (kg/m2) 26.7 (25.6, 27.8) 0.05 ( 0.16, 0.06) 0.02 ( 0.11, 0.08) 0.610 − − − − Fat mass (kg) 25.1 (22.5, 27.7) 0.27 ( 0.76, 0.21) 0.14 ( 0.55, 0.28) 0.558 − − − − Fat-free mass (kg) 51.6 (49.2, 54.1) 0.11 ( 0.39, 0.61) 0.09 ( 0.31, 0.50) 0.989 − − Total body water (kg) 37.8 (36.0, 39.6) 0.07 ( 0.30, 0.44) 0.06 ( 0.24, 0.36) 0.957 − − Body fat (%) 32.0 (29.5, 34.5) 0.17 ( 0.71, 0.37) 0.14 ( 0.58, 0.30) 0.908 − − − − Physical activity level Number of steps per day 8519 (7604, 9433) 71 ( 1106, 963) 234 ( 1059, 592) 0.790 − − − − Distance per day (km) 4.56 (4.17, 4.95) 0.17 ( 0.59, 0.25) 0.25 ( 0.62, 0.11) 0.768 − − − − Data are presented as mean (95 % CI) Apo apolipoprotein, HDL-C high-density lipoprotein-cholesterol, LDL-C low-density lipoprotein-cholesterol, Total-C total cholesterol † Results were derived from paired t tests. Signiﬁcantly different from baseline: * P < 0.05; ** P < 0.01; *** P < 0.001 ‡ Follow-up values between treatments were determined by using linear mixed models controlling for baseline value and intervention period

Hazelnut consumption also had no significant effect on fat correlated (both P < 0.001; data not shown). In addition, mass, fat-free mass and total body water. consuming hazelnuts for 28 days each had no significant effect on “overall liking” ratings from pre (raw 105 mm; Acceptability for nuts dry roasted, lightly salted 107 mm)- to post-exposure (raw 108 mm; dry roasted, lightly salted 111 mm) taste testing The “desire to consume” (Fig. 1a) and “overall liking” sessions. (Fig. 1b) ratings for both forms of hazelnuts were high, i.e. 105 mm on the 150-mm VAS. Mean “desire to consume” ≥ ratings for the dry roasted, lightly salted hazelnuts were not Discussion statistically significantly different from the ratings for raw hazelnuts (P 0.418). Mean “overall liking” ratings for the The present study is to the best of our knowledge the first to = raw and dry roasted lightly salted hazelnuts over the 28-day compare the effects of consuming processed hazelnuts (dry exposure period followed the same pattern as the “desire roasted, lightly salted) and raw hazelnuts on cardiovascu- to consume” ratings, in which no significant difference in lar risk factors and acceptance. Our results showed minimal “overall liking” ratings was found between the two forms differences in clinical outcomes between the two forms of of hazelnuts (P 0.205). Ratings for “desire to consume” hazelnuts. The incorporation of raw or dry roasted, lightly = and “overall liking” remained unchanged throughout the salted hazelnuts into the usual diet was associated with 28-day exposure period. “Desire to consume” and “overall lower total-C/HDL-cholesterol ratio and systolic blood liking” ratings for both forms of hazelnuts were positively pressure and increased HDL-cholesterol and apolipoprotein

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Fig. 1 Mean “desire to consume” (a) and “overall liking” (b) for raw hazelnuts and dry roasted, lightly salted hazelnuts during the 28-day exposure period. Solid horizontal line raw hazelnuts, dashed line dry roasted, lightly salted hazelnuts

A1 concentration, without adverse changes in body weight of these dietary components were not significantly different or acceptance. between the two hazelnut interventions, with only polyun- Three previous studies have investigated the effect of saturated fat intakes being slightly higher during the period consuming processed almonds (raw, roasted salted, roasted where raw hazelnuts were consumed. Exercise levels as butter) and peanuts (raw, roasted unsalted, roasted salted, measured by accelerometer were also similar between the honey roasted, butter or spiced), on blood lipids and lipo- two groups. Thus, it is unclear why this difference has proteins at intakes greater than this study (42–100 g) occurred. [12–14]. All studies showed no significant differences in The present study found no significant differences in change in blood lipid profiles between different forms of the changes in apolipoprotein A1 and apolipoprotein B100 nuts. However, unlike previous work, the change in HDL- concentrations between raw and dry roasted, lightly salted cholesterol and TAG concentrations was statistically sig- hazelnuts. No previous research investigating the effect of nificantly different between forms of hazelnuts in the pre- consuming processed nuts on apolipoprotein concentra- sent study. HDL-cholesterol and TAG concentrations were tions was identified. The present study would suggest that significantly higher following the consumption of the raw consuming raw nuts or dry roasted, lightly salted nuts has hazelnuts, when compared to the dry roasted, lightly salted a similar influence on plasma apolipoprotein concentra- hazelnuts. Dietary components and physical activity level tions. In addition, the current study found that compared have the potential to affect HDL-cholesterol and TAG con- with baseline, the apolipoprotein A1 concentration at the centrations. For instance, high intakes of free sugar may end of both hazelnut interventions was significantly higher. be associated with elevated TAG concentrations [36]. In The increase in apolipoprotein A1 seen in the present study addition, high alcohol and saturated fat consumption may reflects the increase in HDL-cholesterol. It is encour- increase HDL-cholesterol, whereas polyunsaturated fat aging to see both these indices increase with hazelnut may reduce HDL-cholesterol concentrations [37]. Intakes consumption.

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Several recent studies have compared the effects of the plasma α-tocopherol concentrations between ground, sliced digestibility of raw and roasted nuts [38–41]. Overall, these and whole hazelnuts, and the consumption of all forms of studies suggest that although roasting results in a higher hazelnuts significantly increased plasma α-tocopherol [44]. proportion of small particles following mastication, this has Thus, hazelnuts appear to be a rich source of vitamin E. a negligible effect on digestion kinetics, lipid release and This is of particular importance, given that epidemiological the bioaccessibility of bioactives. This may in part explain research has shown an inverse association between vitamin the lack of difference between the raw and roasted hazelnut E intake from nuts and seeds and overall risk of CHD [45]. treatments for the majority of lipoprotein parameters meas- Previous research with weaker study designs (e.g. sin- ured in this study, as well as body weight. gle or sequential arms) and conducted using small (n 30) ≤ Spiller et al. [14] and Jones et al. [12] reported no statis- samples (and so at risk of being underpowered for small tically significant difference in systolic and diastolic blood but still clinically important differences) found no evidence pressure between different forms of nuts. The present study for changes in plasma glucose concentrations following found that although compared with baseline both forms hazelnut consumption [46–48]. One recent randomised of hazelnuts significantly reduced systolic blood pres- parallel study reported no significant difference in blood sure, only the dry roasted, lightly salted hazelnut treatment glucose between four different flavoured forms of peanuts showed a significant reduction in diastolic blood pressure. in 151 participants [12]. The current study, which has used The dry roasted, lightly salted hazelnuts showed a tendency a randomised crossover design with a larger sample size for a greater reduction in diastolic blood pressure when (n 72), provides more convincing evidence that hazelnut = compared to the raw hazelnuts. This suggestive finding consumption has no influence on glycaemic control in non- was also reported in a recent meta-analysis [42]. It should diabetic individuals. These findings are in agreement with be noted that the nuts commercially available in New Zea- results from two recent reviews which reported no benefi- land contained around 570 mg of sodium per 100 g. The cial relationship between nut consumption and glycaemic sodium content of the salted nut variety used in the current control [49, 50]. study, Spiller et al.’s [14] and Jones et al.’s [12] contained Nuts are high in energy and fat and thus have the poten- 133, 210 and 679 mg per 100 g of nuts, respectively. In the tial to contribute to a positive energy balance [51]. As aforementioned studies, participants were provided with the rates of overweight and obesity have increased both 30, 100 and 42 g of nuts, respectively, equating to 40, 210 in New Zealand and internationally [52], questions sur- and 285 mg of sodium per day. This is equivalent to 1.7, rounding recommendations to increase nut consumption 9.1 and 12.4 % of the recommended upper limit for sodium have subsequently arisen. The predicted weight gain over of 2300 mg/day [43]. It appears that when the contribution 4 weeks based only on the additional energy provided by of sodium from nuts is 285 mg/day, there is no adverse hazelnuts and assuming no dietary compensation would ≤ effect on blood pressure. Future studies should investigate be 0.71 kg [53]. This predicted weight gain is likely to be whether long-term consumption of large quantities of com- overestimated even without dietary compensation because mercially available nuts, with a sodium content of more the dynamic nature of metabolism as a result of weight than four times that used in the present study, would have a change was not considered [54]. However, no evidence negative impact on blood pressure. for weight gain was observed with the consumption of Previous work has shown that roasting hazelnuts reduces either raw or dry roasted, lightly salted hazelnuts in the the vitamin E content by up to 10–38 % [25, 27]. Our present study, and in fact, small reductions in weight were analysis indicated that the roasting process reduced the observed. Results of the present study further add to pre- vitamin E content by around 15 %. However, this reduc- vious research, which suggests that regular nut consumption did not influence plasma α-tocopherol concentration results in either no weight gain or less weight gain than tions. The present study found no significant difference predicted [55–59]. This may be explained by dietary com- in plasma α-tocopherol concentrations between the raw pensation, inefficient energy absorption, and an increase in and dry roasted, lightly salted hazelnuts treatments. Con- metabolic rate [51, 60]. suming raw or dry roasted, lightly salted hazelnuts both The present study shows that although both forms of improved plasma α-tocopherol concentration, although hazelnuts increased polyunsaturated fat intake and low- the change from baseline was only statistically significant ered sodium intake, the magnitude of the change was sig- for the raw hazelnut treatment. Whether this result can be nificantly different between the treatments. The absolute extended to commercially batch roasted nuts is unknown, amount of polyunsaturated fat was significantly higher dur- particularly as the hazelnuts used in the current study ing the raw hazelnut period, while the sodium intake was were dry roasted at a low temperature for a short duration. significantly lower during the dry roasted lightly salted Results from the present study are in agreement with pre- hazelnut period. It is important to note that the sodium from vious research, which showed no significant difference in the dry roasted lightly salted hazelnuts only contributed

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<2 % (40/2534 mg) of the total sodium intake during the Conclusion intervention. There are several possible explanations for this. Firstly, participants may have reduced the intake of To conclude, both raw and dry roasted, lightly salted hazel- other savoury foods that are high in sodium from their diet nuts were highly acceptable and improved CVD risk factors when they consumed dry roasted, lightly salted hazelnuts. to a similar extent; thus, current recommendations to con- Secondly, accurate measurement of dietary sodium is chal- sume nuts regularly can be extended to include dry roasted, lenging. Therefore, this could be a spurious finding and lightly salted hazelnuts. This would provide consumers should be interpreted with caution. Overall, the addition with increased choice, which may enhance the likelihood of 30 g of either form of hazelnuts to the diet significantly of consuming sufficient nuts as part of the cardioprotec- increased the percentage of energy derived from monoun- tive diet, especially in populations such as New Zealand saturated fat, while the percentage of energy derived from adults where nut consumption levels are much lower than carbohydrate and sugar intake were significantly lowered recommendations. during the hazelnut-enriched diets. Furthermore, one 30 g serving of hazelnuts provided approximately 50 % of the Acknowledgments We would like to thank the participants for their adequate intake of vitamin E for males and approximately commitment and enthusiasm in participating in this study. 65 % of the adequate intake for females [43]. Thus, incor- Authors’ contribution The authors’ responsibilities were as fol- porating nuts into the usual diet could be an effective way lows—S.L.T., T.R., A.R.G., A.W.C. and R.C.B. designed the study; to meet the recommended intake for vitamin E [61]. When T.R. conducted the research; S.L.T., A.W.C. and R.C.B. supervised the dietary data are taken together, it appears that the addi- the data collection; S.L.T. and A.R.G. analysed the data; S.L.T. and tion of a 30-g portion of either raw or dry roasted, lightly R.C.B. wrote the manuscript. All authors read and approved the final manuscript. salted hazelnuts to a typical New Zealand diet significantly improves overall diet quality and should therefore be Compliance with ethical standards encouraged as part of a cardioprotective diet. Two relatively small studies (n < 40) reported that honey Conflict of interest None of the authors had any personal or finan- cial conflict of interest. roasted and roasted, salted nuts have higher palatability ratings compared to raw nuts when tested on a single session [8, 9]. To exert health effects, nuts must be consumed regularly, and in sufficient quantity. Prolonged exposure to References a food may influence palatability ratings. Therefore, these one-off ratings provide limited information. Seven clinical 1. Browne JL, Grobbee DE (2011) Cardiovascular prevention and international health: time for action. Eur J Cardiovasc Prev studies have investigated the effects of regular nut consump- Rehabil 18:547–549 tion on acceptance. Two relatively small studies (n < 24 per 2. New Zealand Ministry of Health (2015) Mortality and demo- treatment) assessed acceptability at pre- and post-exposure graphic data 2012. 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