Sarah K.
Gebauer
a,
Janet A.
Novotny
a,
Gail M.
Bornhorst
b and
David J.
Baer
*a
aUS Department of Agriculture, Agricultural Research Service, Beltsville Human Nutrition Research Center, Building 307B, Room 213, BARC-East, Beltsville, MD 20705, USA. E-mail: David.Baer@ars.usda.gov; Fax: +1-301-504-9098; Tel: +1-301-504-8719
bBiological and Agricultural Engineering, University of California, Davis, 3056 Bainer Hall, 1 Shields Avenue, Davis, CA 95616, USA
First published on 28th September 2016
The measured metabolizable energy (ME) of whole almonds has been shown to be less than predicted by Atwater factors. However, data are lacking on the effects of processing (roasting, chopping or grinding) on the ME of almonds. A 5-period randomized, crossover study in healthy individuals (n = 18) was conducted to measure the ME of different forms of almonds (42 g per day), as part of a controlled diet: whole, natural almonds; whole, roasted almonds; chopped almonds; almond butter; and control (0 g per day). After 9 days of adaptation to each diet, participants collected all urine and fecal samples for 9 days. Diets, urine, and feces were analyzed to determine ME. Fracture force and fracture properties of whole and chopped almonds were measured. Measured ME (kcal g−1) of whole natural almonds (4.42), whole roasted almonds (4.86), and chopped almonds (5.04) was significantly lower than predicted with Atwater factors (P < 0.001); ME of almond butter (6.53 kcal g−1) was similar to predicted (P = 0.08). The ME of whole roasted and chopped almonds was lower than almond butter (P < 0.0001). ME of whole natural almonds was lower than whole roasted almonds (P < 0.05). This may be due to lower hardness of whole roasted (298 ± 1.3 N) compared to whole natural almonds (345 ± 1.6 N) (P < 0.05), and to whole natural almonds fracturing into fewer, larger particles, thus inhibiting the release of lipids. Atwater factors overestimate the ME of whole (natural and roasted) and chopped almonds. The amount of calories absorbed from almonds is dependent on the form in which they are consumed.
Previous studies with nuts have demonstrated that food form impacts macronutrient absorption. Absorption of fat from whole nuts and peanuts is less than that for other forms of nuts, including butter, oil, and flour,10,11 suggesting that the food matrix impacts metabolizable energy (ME) of food. Recent research has focused on several aspects of the physiochemical nature of the almond seed matrix in order to understand the dynamics of food digestion and release of energy. Using in vitro digestion models, Grundy et al. have demonstrated that intact almond cell walls encapsulate lipid which prevents diffusion of lipase into the intracellular space and thus inhibits lipolysis.12 Unless these cell walls are disrupted, lipid digestion is limited. From in vitro duodenal digestion models, Grundy also has shown that particle size has an impact on lipid bioaccessibility.13 Despite the fact that roasting almonds results in smaller particles when masticated,14,15in vitro digestion models (gastric and duodenal) do not show differences in lipid bioaccessibility.15 Nonetheless, the observed in vivo differences in lipemic response of different forms of almonds11,16 suggest that the ME of almonds processed by different methods may be different, which may impact the accurate labeling of food.
The Atwater general factors and Atwater specific factors, developed in the late 1800s and 1950s, respectively, are still the predominantly used methods to calculate the energy content of foods in nutrient databases and on food labels. We have previously shown that Atwater factors overestimate the measured ME of whole nuts (pistachios, almonds), and walnuts pieces, due to incomplete absorption of macronutrients.17–19 However, the measured ME of other forms of nuts is unknown. The objective of the present study was to determine the impact of food structure and processing (roasting, chopping or grinding) on the measured ME of almonds, within the context of a completely controlled diet.
Study participants were randomized to a treatment sequence consisting of each of the 5 diet periods. The randomization scheme was created using a permutation calculator and random number generator. There were 18 sequences that were selected and checked for balance of treatment by period.
Diets were designed by a study dietitian using a 7-day menu rotation. The control diet consisted of the base diet, designed as a typical American diet (31% fat, 16% protein, 53% carbohydrate), and 0 g d−1 of almonds. All foods were identical between the control and almond diets, except for the almonds. This was achieved by proportionately reducing the amount of every food on the base diet to allow for the isocaloric inclusion of 42 g d−1 almonds.
All of the almonds (nonpareil variety) fed in the study were provided by the Almond Board of California and originated from the same lot (purchased from Hughson Nut, Inc.). The only difference in the almonds across treatments was whether they remained as whole natural almonds or whether they were dry roasted (154–157° C, 9 min roasting time), and either packaged as whole roasted almonds, chopped (particle sizes of 8.7 & 3.2 mm corresponding to industry standard of medium 22/8), or ground into almond butter (ground to smooth consistency by a commercial processor, Maisie Jane's California Products, Inc., with no additives). The dose of 42 g (1.5 oz) was selected based on the U.S. Food & Drug Administration qualified health claim for nuts. Half of the daily dose of almonds was included at breakfast and half of the dose was included at dinner, so that nuts were consumed while participants were at the facility.
Participants were assigned to an individual calorie level using the Harris Benedict equation, based on an age, height, weight, and activity level. Body weight was measured daily, Monday through Friday, and was closely monitored throughout the intervention. Adjustments in calorie level were made in 200 kcal increments if participants exhibited changes in body weight. Adherence to the diets was assessed by daily interaction with participants, monitoring of body weight, and review of daily questionnaires. Daily questionnaires collected information regarding general health, medications, and exercise; amounts of approved beverages consumed (diet soda, calorie free lemonade, coffee, and tea); documentation of any non-study foods; and verification that all study foods were consumed.
Urine was collected in 24 h cycles for 7 days of each diet period during which participants were instructed to collect all urine samples. Participants were provided daily collection supplies, including a 4 L container with boric acid (10 g), an overflow container if needed, and a collection form to record dates/times of collection, any missed samples, and use of medication.
Participants were administered a capsule containing Brilliant Blue to mark the start of the fecal collections. Supplies for fecal collections included a large Styrofoam cooler with dry ice, plastic collection bags, a collection apparatus, and a gym bag to transport samples. Participants were instructed to collect all fecal samples and store them on dry ice until their next visit to the BHNRC. A second capsule of Brilliant Blue was given after 7 days of collection and participants continued collecting until instructed by the study staff to stop. Appearance of the second marker in the feces indicated the end of the collection phase. All samples collected between the appearance of the first and second marker were included for analysis. Daily collection forms were completed with date and time of sample and whether any samples were missed.
Details of chemical analysis have been previously published.18 Briefly, adiabatic bomb calorimetry (Parr Instrument Company; Moline, IL) was used to measure energy of diet, feces, and urine. Samples were analyzed in duplicate. ME was determined by the methods of Novotny et al.,18 using the following equation:
Carea = 1 − e−(X/X50)b·ln2 |
Base diet | Whole, natural almonds | Whole, roasted almonds | Chopped, roasted almonds | Almond butter (from roasted almonds) | |
---|---|---|---|---|---|
a Values are shown as mean ± standard deviation (n = 2 to 6 samples). b Protein was determined as N × 5.18 for the almonds and as N × 6.25 for the base diet. c Carbohydrate was calculated by difference. | |||||
Proteinb | 20.4 ± 0.2 | 20.7 ± 0.1 | 21.8 ± 0.1 | 20.8 ± 0.1 | 19.6 ± 0.1 |
Lipid | 14.4 ± 0.2 | 57.2 ± 0.7 | 55.6 ± 0.3 | 54.5 ± 0.7 | 56.1 ± 0.5 |
Ash | 3.68 ± 0.10 | 3.12 ± 0.05 | 3.07 ± 0.09 | 2.91 ± 0.13 | 2.92 ± 0.11 |
Carbohydratec | 61.5 | 19.0 | 19.5 | 21.8 | 21.4 |
Fracture force of almonds was significantly influenced by almond type (P < 0.0001). The average fracture force was significantly greater for natural almonds (70.0 ± 2.9 N) compared to roasted almonds (52.0 ± 2.2 N) (P < 0.05, Table 2). Hardness of whole natural, whole roasted and roasted chopped almonds was significantly influenced by almond type (P < 0.01). Whole natural almonds had a greater hardness (345 ± 1.6 N) compared to whole roasted almonds (298 ± 1.3 N) (Table 2). Chopped roasted almonds had an intermediate hardness (310 ± 1.4 N), which was not different from either whole natural or whole roasted almonds (Table 2).
Almond type | Fracture force (N) | Hardness (N) |
---|---|---|
a Fracture force was quantified by the three-point bending test on a whole almond kernel, and could not be completed on chopped samples. Hardness was quantified by uniaxial compression of one almond kernel or 1 g of chopped almonds. One-way ANOVA using the Tukey Studentized Range (HSD) test was used to analyze differences between treatment almonds. Values are shown as mean ± standard error (n = 25). Values within each column with different letters are significantly different (P < 0.05). | ||
Whole, natural almonds | 70.0 ± 2.9a | 345 ± 1.6a |
Whole, roasted almonds | 52.0 ± 2.2b | 298 ± 1.3b |
Chopped, roasted almonds | — | 310 ± 1.4ab |
The fracture properties of whole natural, whole roasted, and chopped roasted almonds are shown in Table 3, and example images of one almond (or 1 g chopped almonds) after compression are shown in Fig. 1. The Rosin–Rammler model provided a good fit to the experimental data (R2 = 0.99–1.00). The x50, b, and number of particles per image were all influenced by almond type (P < 0.001). Whole natural almonds had a greater x50 and b value, but a lower number of particles per image compared to whole roasted almonds (P < 0.05). This indicates that as the whole natural almonds were fractured, they broke into fewer, larger pieces compared to whole roasted almonds. The chopped roasted almonds had a larger median particle area (x50) but a fewer number of particles per image compared to the whole roasted almonds (P < 0.05). The particle size distribution of almond butter (as consumed) is shown in Fig. 2. The median particle diameter (d50) was 11.0 ± 0.4 μm. The 90th percentile particle diameter (d90) was 170.4 ± 24.1 μm.
Fig. 1 Example binary images from the fracture of (A) one whole natural almond, (B) one whole roasted almond, or (C) 1 g chopped roasted almonds, after compression at 30 mm s−1 to 71% strain. |
Almond type | x 50 (mm2) | b (dimensionless) | Number of particles/image | R 2 |
---|---|---|---|---|
a Values represent mean ± standard error (n = 25). The R2 value represents the average goodness of fit of the Rosin–Rammler distribution to the experimental data sets. One-way ANOVA using the Tukey Studentized Range (HSD) test was used to analyze differences between treatment almonds. Values within each column with different letters are statistically different (P < 0.05). | ||||
Whole, natural almonds | 27.6 ± 1.7a | 1.1 ± 0.10a | 137 ± 11c | 0.99 |
Whole, roasted almonds | 13.7 ± 0.4c | 0.9 ± 0.05a | 339 ± 10a | 1.00 |
Chopped, roasted almonds | 17.5 ± 0.5b | 1.1 ± 0.08a | 185 ± 8b | 1.00 |
The measured ME of whole natural almonds was lower than whole roasted almonds (P < 0.05) (Table 4). When comparing the different forms of roasted almonds, the ME of whole and chopped almonds was lower than that of almond butter (P < 0.0001). The ME of whole roasted almonds was not statistically different from chopped roasted almonds (P > 0.05).
Almond type | Measured MEa | Estimated ME using atwater general factorsb | Estimated ME using atwater specific factorsb |
---|---|---|---|
Metabolizable energy, ME.a Values presented are mean ± standard error (n = 18). Values within each column with different letters are statistically different (P < 0.05). Mixed model analysis was used to compare ME of different forms of almonds, using contrast statements for the following a priori defined comparisons: whole natural almonds versus whole roasted almonds; whole roasted almonds versus chopped almonds (roasted); whole roasted almonds versus almond butter (roasted); and chopped almonds (roasted) versus almond butter (roasted).b Differences in measured metabolizable energy and estimated metabolizable energy were determined by paired t-tests. Estimated metabolizable energy using Atwater General Factors represents the calculated metabolizable energy based on Atwater general factors and the measured macronutrient composition of each almond form. Estimated metabolizable energy using Atwater specific factors represents the calculated metabolizable energy based on Atwater specific factors and the measured macronutrient composition of each almond form.c Statistically different compared with measured metabolizable energy (P < 0.05). | |||
Whole, natural almonds | 4.42 ± 0.24a | 6.34c | 5.91c |
Whole, roasted almonds | 4.86 ± 0.24b | 6.44c | 6.01c |
Chopped, roasted almonds | 5.04 ± 0.20b | 6.47c | 6.04c |
Almond butter | 6.53 ± 0.19c | 6.62 | 6.18 |
Based on the chemical analysis of each almond treatment (Table 1), the estimated ME (kcal g−1), calculated with Atwater general factors, values of the energy content of macronutrients based on general values for heats of combustion and digestibility, of whole natural almonds, whole roasted almonds, chopped almonds, and almond butter was 6.34, 6.44, 6.47, and 6.62, respectively. When using Atwater specific factors, values of the energy content of macronutrients based on heats of combustion and digestibility of different classes of foods, the estimated ME (kcal g−1) was 5.91, 6.01, 6.04, and 6.18, respectively. The measured ME (kcal g−1) for whole natural almonds (4.42), whole roasted almonds (4.86), and chopped almonds (5.04), was significantly lower than that estimated by Atwater general or specific factors (P < 0.001; Table 4). The Atwater general factors overestimated ME by a greater extent than Atwater specific factors. The percent difference between the measured ME and the estimated ME value using the Atwater specific factors was −25%, −19%, and −17%, respectively for the whole natural almonds, whole roasted almonds, and chopped roasted almonds. The measured ME of almond butter (6.53 kcal g−1) was similar to that predicted when using Atwater general or specific factors (P > 0.05 for both).
As is common with all plant cells, the energy containing macronutrients contained in each almond cell is surrounded by a cell wall. Disruption of the cell wall can occur by mechanical means, either during mastication, processing, chopping or grinding, or by bacterial fermentation in the colon (after the site of absorption). Previous studies with almonds have shown that incomplete rupturing of cell walls during mastication of almond seed tissue results in a large proportion of intact cells.31 The energy containing macronutrients encapsulated in these intact cells remain inaccessible to digestive enzymes, and are excreted in the feces, such that they are not absorbed. Studies have demonstrated that particle size, an indicator of the proportion of unruptured cells, is related to the bioaccessibility of the macronutrients contained in almonds.14,16 Particle size of almonds decreases as the degree of mastication increases (due to greater cell wall disruption), resulting in less fecal fat excretion and higher energy absorption.
Processing of nuts, such as roasting, chopping, and grinding, impacts mastication, particle size, and lipid bioaccessibility;11,14,32 however, the ME of different forms of almonds has not been previously determined. In the present study, the dry roasting of whole almonds resulted in a higher ME compared with natural almonds. Dehydration during the roasting process causes almond tissue to be more brittle, leading to a higher proportion of smaller particles (and lower proportion of large particles) and increases in energy absorption.14
In the present study, whole natural almonds had a greater fracture force and greater hardness compared to whole roasted almonds. Although the fracture force (52 to 70 N) for either type of almonds is much less than the average bite force exerted by the teeth in adult humans (630 N for males and 424 N for females),33 it may play a role in the fracture properties and resulting particle size distribution during chewing.
Fracture properties of whole natural and roasted almonds were determined after compression of a single almond kernel, as this method has been shown to provide similar results to the particle size after in vivo mastication of almonds.21 After fracture, whole roasted almonds had a greater number of particles with a smaller median particle area (Table 3, Fig. 1) compared to whole roasted almonds. This may indicate that during mastication, whole roasted almonds are broken down to a greater degree. As previously reported, smaller particles result in greater lipid release from the almond cell walls.16,34 Since the whole roasted almonds had smaller particles, a greater amount of lipids may have been released, resulting in greater ME compared to whole natural almonds.
The ME of whole roasted and chopped almonds was lower than almond butter, which is likely due to extensive cell wall disruption during the grinding of almonds into butter. The median particle size of the almond butter was 11 μm. Since the almond butter already had a large particle size reduction during grinding, there was little additional breakdown required during mastication and digestion. This extensive cell wall disruption and small particle size may have allowed more energy to be released from the cells and absorbed by the body compared to the chopped and whole almonds, resulting in the higher observed ME value. The ME of almond butter was similar to what is predicted by the Atwater factors.
The ME of whole, roasted almonds was not statistically different than chopped almonds. The median particle area after fracture was in a similar range for whole and chopped roasted almonds, although the values were significantly different (13.7 vs. 17.5 mm2). However, both of these values were significantly lower than the median particle area for whole natural almonds (27.6 mm2). This may indicate that during roasting, regardless of whether the almonds are whole or chopped, particles break down to a similar degree, which results in a similar ME value.
Variability of ME ranged from 2.84 kcal g−1 to 7.66 kcal g−1 across the almond forms. Individual differences in mastication patterns likely contribute to the variability in ME. Instruction was not provided with regards to chewing so that the mastication of the different almond forms was representative of typical consumption. Variability in individual responses differed based on almond form (data not shown), suggesting that differences in mastication patterns have less of an impact on ME when almonds are ground into butter than when they are consumed whole (i.e., cell walls are already ruptured during grinding and energy is more available regardless of differences in mastication). Individual differences in intestinal microbiota also may contribute to variability of ME. Future studies are warranted to determine whether differences in microbiota explain differences in ME across individuals, which could have broader implications with regards to energy intake and body weight of individuals.
Footnotes |
† Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture (USDA). |
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This journal is © The Royal Society of Chemistry 2016 |