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Diet and Human Performance Laboratory, Beltsville Human Nutrition Research Center, Agricultural Research Service, U.S. Department of Agriculture, Beltsville, MD 20705;
* Department of Nutrition, The Pennsylvania State University, State College, PA 16802; and
Food Quality And Safety Research, National Center for Agricultural Utilization Research, Agricultural Research Service, U.S. Department of Agriculture, Peoria, IL 61604
2To whom correspondence should be addressed. E-mail: baer{at}bhnrc.arsusda.gov.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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15% of energy (en%) from protein, 46 en% from carbohydrate and 39 en% from fat with 8 en% substitution across diets of the following: trans monoenes, oleic acid, saturated fatty acids (lauric + myristic + palmitic) or stearic acid fed as triacylglycerides. Fats were incorporated into mixed diets comprised of foods typically consumed in the United States. After a 14-d adaptation period, volunteers collected all feces for 7 d. Across diets, absorption of stearic acid (94.1 ± 0.2%) was lower (P < 0.0002) than that of palmitic acid (97.3 ± 0.2%) and higher than generally reported. Absorption of lauric, myristic, oleic, linoleic and trans 18:1 monoenes did not differ from each other (>99%) but was higher than that of stearic and palmitic acids (P < 0.001). Metabolizable energy values were similar for all fatty acids. Although absorption of palmitic and stearic acids was affected by diet treatment, the magnitudes of the differences were small and do not appear to be biologically important, at least in terms of lipoprotein metabolism. On the basis of these results, reduced stearic acid absorption does not appear to be responsible for the differences in plasma lipoprotein responses to stearic acid relative to other saturated or unsaturated fatty acids.
KEY WORDS: • absorption • metabolizable energy • fatty acids • stearic acid • trans fatty acids
Stearic acid is a saturated fatty acid that, in contrast to other long-chain saturated fatty acids, does not raise plasma LDL cholesterol. We recently demonstrated in a controlled feeding study designed to evaluate the effects of individual fatty acids, that compared with a carbohydrate-control diet, a diet containing 8% of energy (en%)2 of saturated fatty acids (lauric + myristic + palmitic) increased LDL cholesterol 5%, whereas an equivalent amount of stearic acid in the diet did not alter plasma LDL cholesterol (1). Further, a diet enriched with 4 en% stearic acid and 4 en% trans monoenes did not raise LDL cholesterol as much as a diet containing 8 en% trans monoenes (1). One possible explanation for the disparity in effect of saturated fatty acids on plasma LDL cholesterol may be differences in their absorption. Differences in absorption could also affect the metabolizable energy content of specific fatty acids and thus may have implications for nutrition labeling.
Early studies conducted with rats fed tristearin suggested that stearic acid is undigestible (2–4). More recent studies conducted with humans have suggested that stearic acid is digestible but there is a wide range of absorption reported. The absorption [(intake - excreted)/intake] of most fatty acids is reported to be >95% in humans, but the absorption of crude fat from high stearic acid sources is reported to range from 68 to 98% (5–8). Others have fed individual meals of 13C-labeled fatty acids in an emulsion of fat, protein and carbohydrate to measure appearance and metabolic conversion of fatty acids (9,10). The wide range of stearic acid absorption reported may be a consequence of differences in the amount of stearic acid consumed, the dietary source of the stearic acid and the length of adaptation to the diet before absorption measurements. The physiologic and biochemical mechanisms and nutrient interactions responsible for the differential absorption of fatty acids from triacylglycerides are likely numerous.
In conjunction with a large, well-controlled dietary intervention to determine the effects of individual fatty acids on plasma cholesterol concentrations, we conducted an absorption study to determine whether the effects of fatty acids on plasma cholesterol and lipoproteins could be attributable to differences in fatty acid absorption. In this study, mixed diets were used to replicate typical meals consumed by humans and to avoid issues related to the feeding of large amounts of atypical fat sources. Subjects consumed these diets for 14 d before sample collection to overcome limitations of inadequate gastrointestinal adaptation to the diet.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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This study was conducted with men (n = 11) who were participants in a larger study with a primary objective to investigate the effects of specific fatty acids on lipid and lipoprotein metabolism (1). A randomized crossover design was used to account for period effects associated with the sequence of diets and to account for interindividual variability. Subjects were selected on the basis of their willingness to collect food and fecal samples, and on the frequency of bowel movements. The selected subjects self-reported that they had at least one daily bowel movement. The mean (±SEM) age of the subjects was 44.1 ± 3.5 y old, body weight was 79.6 ± 2.7 kg and BMI was 25.6 ± 1.0 kg/m2.
Medical history, blood chemistry, urine analyses, complete blood count and a physical examination conducted by a physician were used to determine that the subjects were healthy and had no apparent signs or symptoms of disease (e.g., hypertension, hyperlipidemia, diabetes, peripheral vascular disease, gout, liver or kidney disease or endocrine disorders). Before acceptance as a subject, all participants were fully informed of study requirements and before entry into the study were required to read and sign a consent form detailing the study objectives, risks and benefits. All procedures were approved by the Johns Hopkins University Bloomberg School of Public Health’s Committee on Human Research. Subjects were compensated for their participation in this study.
Diet composition.
During the main study, subjects consumed six diets. Fatty acid absorption was determined for four of the six diets. These diets were formulated to contain 15 en% from protein, 46 en% from carbohydrate and 39 en% from fat. The macronutrient composition of the diets was designed to include the mean fat intake for men in the United States at the time when the study was planned (11). The diets were formulated with an 8 en% substitution across diets of the following: trans monoenoic fatty acids (TFA), oleic acid (OL), saturated fatty acids (lauric + myristic + palmitic) (LMP) or stearic acid (STE), and these fatty acid substitutions were accomplished by providing the fatty acids as triacylglycerides (and a small amount of naturally occurring mono- and diacylglycerides) from a variety of fat sources (Table 1). Other fatty acid concentrations (as triacylglycerides) were similar among diets, and the diets contained similar concentrations of dietary fiber, calcium and magnesium. A 7-d menu rotation was designed to enhance diet acceptance. Within each diet, the day-to-day composition was similar. The study was conducted in two 15-wk phases with three treatment periods per phase and an 8-wk break between phases. There was no break or washout period between treatments within each of the phases.
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Each morning, Monday through Friday, subjects were weighed before breakfast. Maintenance energy intake was determined by feeding to weight maintenance for 2 wk before the start of collections. During this time, energy intake was adjusted in 0.84-MJ or 1.6-MJ increments, to maintain body weight. No adjustments of energy intake were made immediately before or during the collection period. Subjects were fed the same items and the same proportions of each item relative to total daily dietary energy intake. Therefore, the ratio of all nutrients was constant for all subjects. Each day, subjects completed a questionnaire detailing beverage intake, factors related to dietary compliance, exercise, medications and illnesses. The questionnaires were routinely reviewed by a study investigator, and all problems identified were discussed with the subject during the next meal. Exercise was not controlled but subjects were encouraged to maintain their normal exercise patterns (type of exercise, duration and frequency) throughout the study and record their exercise on their daily questionnaire.
Monday through Friday, all subjects were served and consumed their breakfast and dinner at the Beltsville (Maryland) Human Nutrition Research Center’s Human Study Facility under the supervision of a dietitian. At breakfast, each subject was provided with a carry-out lunch to be consumed that day. Snack items were included in the daily menu, and subjects were provided the option of consuming the snacks at dinner or later in the evening. Meals for the weekend were packaged for home consumption and provided to the subjects, with written instructions, after dinner on Friday. Coffee, tea and diet sodas were consumed ad libitum but all additives (sugar and milk) for coffee and tea were provided with the meals. Only foods provided by the Human Study Facility were allowed to be consumed during the study. The subjects had no knowledge of the type of fat in the diets.
Food was collected for chemical analyses during the weeks of fecal collections. Each subject was asked to prepare two trays of food, one tray for consumption by the subject and a duplicate tray for chemical analysis. After the subject gathered the appropriate items for the meal, a trained dietitian reviewed both trays to ensure the appropriate foods and amounts were selected. The subjects then prepared the foods on both trays as though they were to be consumed. For example, foods that were normally heated or cooked (e.g., eggs) were heated in microwave ovens, bread was toasted, margarine or butter was put on potatoes and warmed. When the subject finished food preparation, one of the two trays was selected at random by the dietitian and prepared for chemical analysis. For each subject, one day’s food was blended with ice and water in a Waring blender, and poured into a preweighed plastic container. After freeze-drying, the containers were immediately reweighed, and the homogenized samples were crushed by hand to form a powder. For each diet treatment, a pooled weekly sample for each subject was produced by taking a subsample (15 g/100 g of the total daily weight) of each day’s food.
Fecal collections.
After consuming a diet for 2 wk, subjects were given a gelatin capsule containing brilliant blue (20 mg) at the end of the evening meal. The 2-wk adaptation period before the start of fecal collection provided sufficient time for dietary associated changes in microbial flora and intestinal function to occur (12). Each subject was given a Styrofoam container containing dry ice (replenished at least every other day) and instructed to start collecting all feces. Feces were collected into plastic bags and the date and time was written on each bag. Immediately after collection, the feces were placed into the Styrofoam container and brought to the Center (usually within 12 h after collection, except on the weekend when the maximum time would be 36 h), where they were placed in a freezer. At the end of 7 d, the subject was given another capsule containing brilliant blue and instructed to continue collecting feces until at least one bowel movement was green.
Each bag of feces was freeze-dried and immediately reweighed (the mean weight of a plastic bag was subtracted). For each diet, a subject’s samples were pooled by including the first marked sample, and all of the subsequent samples until the marker reappeared in the feces. The freeze-dried pooled samples were crushed into a homogeneous powder in the plastic bags.
Analytical methods.
Subsamples of food were pooled within diet treatment and were analyzed for protein, ash, total dietary fiber, magnesium and calcium (Covance Laboratories, Madison, WI). The weekly composites for each subject’s samples of food and feces were analyzed for crude fat (methylene chloride extraction, CEM, Matthews, NC) and gross energy (adiabatic bomb calorimetry, Parr Instruments, Peoria, IL).
Fatty acid composition of the food and feces was determined by GC separation of FAME after Folch extraction. Fecal samples were acidified before extraction. Total lipids were extracted (13) and measured gravimetrically after the extraction of a 200–250 mg sample of the lyophilized materials. The fatty acids in the lipid extract were methylated using boron triflouride-methanol (14,15) and quantified using a Hewlett-Packard 5890 gas chromatograph (Analytical Instrument Recycle, Golden, CO). The FAME were separated on a SP-2330 capillary column (Supelco, Bellefonte, PA) with helium as a carrier gas at a flow rate of 30 mL/min. Flow rates for hydrogen and air were 30 and 300 mL/min, respectively. The temperature was set at 150°C for 8 min, then increased to 190 C at 2°C/min, and maintained at 190°C for 20 min. Both injector and detector temperature were 250°C. The mass of each fatty acid was quantified with the addition of an internal standard, heptadecanoic acid (17:0), to each sample before extraction. Fecal samples were acidified before extraction. The composition of triacylglyceride molecular structures in the stearate test fat was determined by atmospheric pressure chemical ionization MS (16).
Calculations and statistical analyses.
The apparent absorption of lauric, myristic, palmitic, stearic, cis 18:1, trans 18:1, and linoleic fatty acids was calculated for those fatty acids whose daily intake was at least 1 g. Apparent absorption (no correction for endogenous excretion) was calculated as:
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Least-square means (LS means) and diet differences were determined using a mixed ANOVA model which included terms for diet, period, diet-by-period interaction, and a repeated term for subject, and the p-values were adjusted using the Tukey procedure for multiple mean comparisons. Values in the Results are presented as LS means ± SEE. Statistical analyses were performed using SAS (Cary, NC) for Windows (version 6.11).
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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10.9 to 14.2 MJ, and mean daily fat intake was 110.5 ± 1.6 g (providing 4.16 ± 0.06 MJ/d). No subject reported any digestive upset, disturbance or diarrhea associated with consumption of any of the four diets, and all subjects completed the feeding protocol. Total protein (mean of four diets = 15 en%), fat (39 en%), carbohydrate (46 en% with dietary fiber as 4.4 g/100 g of dry weight), calcium (0.16 g/100 g of dry weight) and magnesium (0.06 g/100 g of dry weight) intake did not differ when the subjects consumed the four diets.
The desired fatty acid profile of the diets was achieved with combinations of "hidden fat" in foods (20 g/100 g of total fat) and use of 5–12 "visible fat" sources that were incorporated into foods prepared in the Facility specifically for this study (Table 1). These visible sources of fat represented the remaining 80 g/100 g of the total fat.
The STE diet contained the highest percentage of the stearate test fat (43.9 g/100 g of total fat); the other diets contained 0.4 to 0.8 g/100 g of total fat from this fat source. For the STE diet, the stearate test fat contributed 1.7 en% of the diet from tristearine, 6.0 en% from distearines and 7.0 en% from monostearines (Table 2).
Mean stearic acid absorption of all four dietary treatments was 94.1% and was lower than that of other fatty acids (P < 0.001) (Table 3). Palmitic acid absorption was 97.3% and was higher (P < 0.001) than that of stearic acid but lower than that of other fatty acids (P < 0.001). Absorption of lauric, myristic, oleic, trans 18:1 and linoleic was 
99% and was not different among these fatty acids. Crude fat absorption was 98.4 ± 0.1% across all four diets.
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In some studies, crude fat absorption is measured as a response to diets containing different sources of fat, as opposed to measuring the absorption of specific fatty acids. When cocoa butter was compared with corn oil in diets fed to humans (129 g/d), crude fat absorption was lower (96.5% for corn oil compared with 89.3% for cocoa butter) (20). When more modest amounts (30.7 g/d) of cocoa butter were fed to humans, there was no difference in absorption of fat between cocoa butter and corn oil (21). In the present study, crude fat absorption was significantly lower when subjects consumed the STE diet compared with the TFA and OLE diets but the magnitude of the difference was very small (98.8 compared with 97.9%). It is unlikely that these small differences in crude fat absorption are biologically meaningful, at least with respect to their effect on lipoprotein metabolism.
Because biological responses to different fatty acids may be more meaningful than those to crude fat, the measurement of specific fatty acid absorption may provide greater understanding of the effect of fat metabolism and risk for disease. When olive oil, butter fat, cocoa butter and beef fat were incorporated into diets and fatty acid absorption was measured, stearic acid absorption from each of these four fats (68, 90, 92, and 94%, respectively) was less than that of palmitic (96–97%) and oleic acids (99%) (6). The low stearic acid absorption measured when volunteers consumed the olive oil diet (68%) may have been a consequence of a relatively low intake (<4 g/d) of stearic acid and possibly a high contribution of stearic acid from endogenous sources (e.g., intestinal cells) (5). When two diets with different palmitic and stearic acid concentrations (altered using palm oil, shea nut oil and butter) were fed to 10 men, palmitic acid absorption was higher (95–99%) than that of stearic acid (86–98%) (7). High absorption of palmitic, oleic and stearic fatty acids from liquid-based diets (97–99%) (5) was consistently observed in studies that used limited fat sources, and in this study with mixed diets. Whether volunteers were fed a few fat sources, liquid-based diets or mixed diets, the absorption of stearic acid and palmitic acid was lower than that of other fatty acids measured, and palmitic acid absorption was always greater than that of stearic acid. However, in most studies, the magnitude of the difference was consistently small.
Although significant decreases in stearic acid absorption may be achieved, these decreases are achieved with novel triacylglycerols such as Salatrim (22); although the interesterified test fat used in the STE diet is atypical of the structure of most triacylglycerols consumed from foods (stearic acid is usually found in the sn-1 and sn-3 position in foods and was randomized in the test fat), there is little evidence that position of the stearic on the triacylglycerol affects biologic function (e.g., lipid or lipoprotein response) (23). Brink et al. (24) found a difference in stearic acid absorption from a structured triacylglycerol in a small study of nine rats. In their study, stearic acid absorption was higher when it was at the sn-1 and sn-2 position rather than at the more typical sn-1 and sn-3 position. However, in this study there was a significant interaction with dietary calcium, which makes interpretation of these data more difficult.
Data from this absorption study are consistent with data from stable isotope absorption studies (10,25). Further, isotope studies suggest that there is little hydrogenation of other fatty acids (e.g., oleic acid) to stearic acid in the gastrointestinal tract but there may be some conversion of stearic acid to palmitic acid with subsequent excretion in the feces (10). This conversion would lead to an overestimation of the absorption of stearic acid although the magnitude of the conversion of isotopically labeled fatty acids appears small (10). In vivo, it appears that this conversion is <10% in humans (9).
Calculation of energy content of foods is of interest to consumers, and an important consideration in complying with food labeling requirements in the United States. General factors for calculating energy values of foods were derived from specific factors of individual food groups (26). As advances in food technology and development of designer foods increase, application of these specific or general factors is more likely to create discrepancies between food labels and the measured energy content of the products (27). As data on absorption of specific nutrients becomes available, the premise for calculation of energy for individual foods can be extrapolated to specific nutrients, such as fatty acids. The metabolizable energy (or physiologic fuel value) content of different fatty acids fed in this study can be calculated using the absorption of specific fatty acids measured in this study, and the assumption that no fatty acid energy is lost in urine. Based on the heats of combustion of lauric (37.0 kJ/g), myristic (38.2 kJ/g), palmitic (39.2 kJ/g), stearic (39.9 kJ/g) and oleic (39.9 kJ/g) acids and their absorption, the resulting metabolizable energy values of these fatty acids are 37.0, 37.8, 38.1, 37.5 and 39.3 kJ/g, respectively. Thus, although the gross energy of stearic acid is greater than that of other saturated fatty acids, its metabolizable energy value is similar to other saturated fatty acids due to its lower absorption. In contrast, unsaturated fatty acids have a slightly higher absorption coefficient than stearic acid and a metabolizable energy value 4.8% higher than that of stearic acid. Some discrepancies in the energy content of fat may be a consequence of lower absorption coefficients for crude fat (90–95%) that were used by Atwater (26) to develop the specific factors, compared with the crude fat digestibilities that typically exceed 98% in more recent studies, including the current study. Data on energy value of fats and fatty acids are particularly important as new approaches to improve the estimates of food energy are developed (28).
In mixed diets fed to humans, stearic and palmitic acids have a lower absorption coefficient than other fatty acids, and the absorption of most fatty acids is >99%. Differences in gross energy and absorption affect the metabolizable energy content of fatty acids. Therefore, if the fatty acid profiles of a food are atypical and not representative of typical foods, then the calculated energy content may be incorrect. With current food and fecal collection techniques and analytic methodologies, it is possible to measure small differences in the absorption of fatty acids. However, the biological importance of these differences may also be minor. Although digestibilities of palmitic and stearic acids differed significantly among the diets, the magnitudes of the differences were small, and cannot reasonably account for major differences in plasma lipoprotein responses after consumption of stearic acid compared with other saturated or unsaturated fatty acids.
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FOOTNOTES |
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3 Abbreviations used: en%, percentage of energy; LMP, saturated fatty acids (lauric + myristic + palmitic)-enriched diet; OL, oleic acid–enriched diet; STE, stearic acid–enriched diet; TFA, trans monoenoic fatty acid–enriched diet.
Manuscript received 25 June 2003. Initial review completed 15 September 2003. Revision accepted 1 October 2003.
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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