Journal of the American College of Nutrition, Vol. 17, No. 6, 601-608 (1998)
Published by the American College of Nutrition
Cookies Enriched with Psyllium or Oat Bran Lower Plasma LDL Cholesterol in Normal and Hypercholesterolemic Men from Northern Mexico
Ana Lourdes Romero, MS,
Jesus Enrique Romero, MD,
Samuel Galaviz, PhD and
Maria Luz Fernandez, PhD
Centro de Investigacion y Postgrado (A.L.R., J.E.R., S.G.), Universidad de Sonora, Hermosillo, Sonora, Mexico
Department of Nutritional Sciences (M.L.F.), University of Connecticut, Storrs
Address reprint requests to: Maria Luz Fernandez, PhD, University of Connecticut, Department of Nutritional Sciences, 3624 Horsebarn Road Extension, U-17, Storrs, CT 06269
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ABSTRACT
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Background: Psyllium and oat bran have been shown to lower plasma LDL cholesterol levels in different populations. Hypercholesterolemia is prevalent in the Northern part of Mexico and might be associated to dietary habits and sedentary lifestyle.
Methods: Sedentary normal (cholesterol<200 mg/dL) (n=36) and hypercholesterolemic (cholesterol>220 mg/dL) (n=30) men from the Northern part of Mexico aged 20 to 45 years of age participated in an 8-week study to determine the effects of dietary soluble fiber, either psyllium or oat bran, in lowering plasma LDL cholesterol in this population. Fiber was administered by feeding the subjects an amount of cookies (100 g) equivalent to 1.3 or 2.6 g/day of soluble fiber from psyllium or oat bran, respectively. Subjects were randomly allocated to three groups: a control group consuming cookies with wheat bran, a known source of fiber with no cholesterol lowering effects, psyllium, or oat bran.
Results: Food frequency questionnaires indicated that subjects from the three groups had similar intakes of foods classified as hypercholesterolemic (p>0.05). Plasma LDL cholesterol concentrations were reduced by an average of 22.6 and 26% in the psyllium and oat bran groups (p<0.001) while a non-significant reduction of 8.4% was observed in the hypercholesterolemic individuals from the control group. No effects on plasma HDL or triglycerides levels were observed among the three dietary treatments except for hypercholesterolemic individuals supplemented with oat bran where a 28% reduction in plasma triglycerides was observed after 8 weeks (p<0.01).
Conclusion: These results indicate that psyllium and oat bran are efficacious in lowering plasma LDL cholesterol in both normal and hypercholesterolemic individuals from this population.
Key words: psyllium, oat bran, LDL cholesterol, hypercholesterolemia, Northern Mexico
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INTRODUCTION
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High intake of dietary fiber has been associated with favorable effects on human health [1,2]. Several sources of dietary soluble fiber including psyllium and oat bran have been shown to decrease plasma LDL cholesterol concentrations in normal and hyperlipidemic subjects [3–6]. Since there is a positive association with plasma LDL cholesterol levels and coronary heart disease risk [7], intake of nutrients known to lower the concentration of LDL in plasma is considered to be highly beneficial.
Based on the potential use as hypercholesterolemic agents, numerous clinical studies have been conducted to test different sources of soluble fiber in different populations varying in age [8] dietary intakes [9] or plasma lipid levels [10]. From these studies, psyllium intake has consistently shown significant reductions in plasma LDL cholesterol levels ranging from 10 to 24% [3,4,8,10]. Other sources of fiber such as oat bran have been more controversial [11–14] apparently due to the lack of consistency between studies, the diet consumed by subjects [12] or variations in the preparation or the source of the oat bran [14].
The secondary mechanisms by which psyllium lowers plasma LDL cholesterol concentrations have been tested in several animal models [15–23]. Studies in male and female guinea pigs have demonstrated that psyllium lowers plasma LDL cholesterol and hepatic cholesterol concentrations resulting in an up-regulation of cholesterol 7
-hydroxylase activity which suggests an interruption of the enterohepatic circulation of bile acids [15–18]. Increases in LDL fractional catabolic rate and hepatic apo B/E receptor number have also been observed by psyllium intake [15–18]. Up-regulation of cholesterol 7hydroxylase activity and mRNA abundance [19] and decreases in LDL production rate and accelerated LDL catabolism have been shown in hamsters consuming psyllium diets [20,21]. In African green monkeys, decreases in LDL apo B flux was postulated as the major mechanism of plasma LDL lowering induced by psyllium intake [22]. Oat bran has been shown to reduce plasma cholesterol and hepatic cholesterol concentrations in the cholesterol-fed rat [23,24].
Based on these numerous reports for clinical [3–6,8–14] and animal studies [15–24], we decided to test the effects of psyllium and oat bran on individuals characterized by high consumption of dietary fat and total calories [25]. For our studies we recruited sedentary males aged 20 to 45 years from a population living in the Northern part of Mexico which has been identified as having higher plasma cholesterol concentrations compared to the rest of the country [26].
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MATERIALS AND METHODS
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Materials
Enzymatic cholesterol assay kits, cholesterol standard and triglyceride kits were purchased from Boehringer Mannheim (Indianapolis, IN). Plastic bags were obtained from Reynolds company, (Richmond, VA). Psyllium (PSY) husks (Plantago ovata) with 87.3% total fiber and 11.2% soluble fiber were obtained from Laboratories Hormona (Mexico City, Mexico). Oat bran (OB) containing 14.3% total dietary fiber and 4.3% soluble fiber was purchased from a local natural store. Wheat flour and other baking ingredients were purchased in the local market.
Subjects
Male subjects were recruited to participate in the study. They were randomly assigned to one of three fiber groups: control, PSY or OB. A frequency questionnaire was developed to assess consumption of food items associated with hypercholesterolemia or hypertriglyceridemia. Individuals were advised to reduce the consumption of those food items during the time of the experiment. Two blood draws were performed to assess baseline values for plasma lipids at the beginning of the experiment within the first week and at end of the experiment after 8 weeks. An amount of cookies equivalent to 100 g/day containing the different fibers were given to subjects every Tuesday (for the next 3 days) and every Friday (for the following 4 days including the week end). Subjects were asked to return every week the portion of the cookies that was not consumed.
Subjects ranged in age from 20 to 45 years (mean 35–38 y), mean body weight ranged from 74 to 83 kg, body mass index values from 26.4 to 27.3 kg/m2 and mean systolic and diastolic pressure values ranged from 77 to 80 and from 116 to 123, respectively. Summarized details of subjects’ characteristics are given in Table 1.
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Table 1. Characteristics of subjects (normal and hypercholesterolemic) fed control, psyllium or oat bran cookies at baseline and after 8 weeks of dietary treatment1
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Patients treated with lipid-lowering drugs, diabetic individuals, cardiovascular or active gastrointestinal diseases were excluded from the study. All subjects selected were interviewed to inform them of the nature of the experiment and they were requested to provide a written informed consent. Subjects were followed on an ambulatory basis for 8 weeks. All subjects from the normal and hypercholesterolemic groups consumed 100 g of cookies daily which is equivalent to 0.6 g, 1.7 g or 2.8 g of soluble fiber derived from wheat bran, psyllium or oat bran, respectively. All human experiments were carried out according to the guidelines of the University of Sonora and protocols were approved by the Human Subject Committee.
Preparation of Cookies
Cookies were prepared according to the micro-method III [27]. Mixing was performed in a Hobart mixer (Model AS 200T, Hobart Company, Troy, OH) in a 1:1.25 proportion of solid: water for one min at low speed. After 10 minutes, mix was extended for a final 7 mm thick, 5 cm diameter cookie. Baking was conducted in a convection oven (model Z-X-4, Hornos Carcamo S.A., Mexico, D.F.) After 60 minutes cooling, the daily cookie portion (10 cookies corresponding to 100 g) was packed in individual plastic bags. Chemical composition of cookies is shown in Table 2.
Additional Measurements
Informed consent, a medical history, a physical examination, the food frequency questionnaire and the discomfort questionnaire were provided to subjects during the grouping time/baseline period. Subjects were advised to restrict consumption of certain dietary items listed in the food frequency questionnaire which are part of their normal diet. Frequency of consumption (0 to 7 times a week) of each or these food items was recorded by each subject every week. The discomfort questionnaire addressed the following symptoms that could be present due to fiber intake: nausea, stomach acidity, vomit, abdominal distention, diarrhea, increased evacuation number and flatulence. Personnel from the study visited with each patient twice a week to distribute the corresponding packages of cookies and the weekly discomfort questionnaire. To reduce possible gastrointestinal effects of increased fiber intake, subjects were advised to consume one-third of the cookies with every meal for a total of three meals per day. Body weight was recorded weekly.
Plasma Lipids
Plasma lipids were measured during baseline and after 8 weeks. Standardization and quality control for plasma cholesterol and triglyceride assays have been maintained in our laboratory by participation in the Centers for Disease Control-National Lung and Blood Institute (CDC-NHLBI) Lipid Standardization Program since 1989. Two blood draws at baseline and two blood draws after 8 weeks were obtained for all subjects to measure total plasma cholesterol, triglycerides and HDL-cholesterol. Total cholesterol was determined by enzymatic methods [28] using Boehringer-Mannheim cholesterol standards. HDL cholesterol was measured in the supernatant after precipitation of apo B containing lipoproteins [29], and LDL-cholesterol was calculated as described by Friedewald et al [30]. Triglycerides were determined adjusting for free glycerol according to Carr et al [31].
Statistics
Differences in the frequency of consumption of the different food items provided in the list was evaluated by the Kruskal-Wallis non-parametric test with a statistics software program (SAS, 1988). One-way ANOVA and the Newman-Keuls post-hoc test were used to evaluate significant differences in changes between baseline and 8 weeks among dietary treatments. Paired t-test was used to evaluate differences in plasma total, LDL and HDL cholesterol, triglycerides and LDL/HDL ratios at the beginning of the experiment and after 8 weeks of treatment using the same statistics software program. Within-group analyses were averages of measurements obtained during the establishment of baseline, compared with average measurements obtained during the final week of the treatment period. p<0.05 was considered significant.
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RESULTS
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At the beginning of the experiment 70 subjects were recruited and randomly distributed to the three dietary treatments and four of them did not complete the study for several reasons. The final distribution of the 66 individuals who completed the study was 24 for the control, 22 for the oat bran and 20 for the psyllium group. There were no significant differences in body weight, body mass index between baseline and after 8 weeks of treatment for all groups of subjects. Normal and hypercholesterolemic subjects in control, PSY or OB groups did not have a significant change in any of those characteristics (Table 1) indicating that fluctuations in body weight were not related to the observed changes in plasma lipids discussed below. However, normal individuals from the control group had lower plasma cholesterol levels at baseline than subjects from the other two groups and higher HDL cholesterol concentrations than the OB group (Table 3). In addition, individuals from the control group had higher plasma HDL cholesterol concentrations than the psyllium and oat bran groups for the hypercholesterolemic individuals (p<0.05). No differences were observed in plasma cholesterol at baseline among hypercholesterolemic subjects from the three groups or in plasma triglycerides for all subjects (Table 3).
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Table 3. Plasma lipids at baseline for normal and hypercholesterolemic individuals fed control, psyllium or oat bran cookies
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As described above, subjects from this population normally consume diets high in dietary fat and calories [25]. The average consumption of saturated fat is 18% of total calories (Fernandez, unpublished observations). Individuals from the three dietary groups were advised to reduce the intake of certain food items associated with increases in plasma cholesterol. Subjects participating in the study were highly motivated and made a conscientious effort to change their dietary habits and they all (n=66) reduced their usual intake of animal products during the 8 weeks of the study. The questionnaire to determine frequency of consumption was distributed weekly and the mode for each item in each dietary group was used for the summary of the 8 weeks as presented in Table 4. There were no differences in the food frequency intake mode for the food items under study for the three dietary groups as analyzed by the Kruskall-Wallis non-parametric test (Table 4). These data indicate that differences in the frequency of consumption of those food items was not a factor affecting plasma lipid levels in the subjects participating in this study. In addition, none of the subjects for any of the dietary groups complained of symptoms indicated in the discomfort questionnaire (data not shown) thus all subjects consumed the allotted amount of cookies and completed the 8 weeks of the study.
Plasma Lipids
Changes of plasma total, LDL and HDL cholesterol, plasma triglycerides and LDL/HDL ratio between baseline and after 8 weeks of dietary treatment were calculated for all subjects participating in the study (Table 5). Reductions in total cholesterol were 33.5 to 45.5 mg/dL for subjects in the psyllium and oat bran groups while reductions in total cholesterol for the control group were an average of only 2.1 mg/dL. The reductions in plasma total cholesterol were significantly greater in the psyllium and oat bran groups compared to the control group (p<0.001). Similar results were obtained for LDL cholesterol (Table 5). The psyllium and oat bran groups had 44 and 43 mg/dL reduction in LDL cholesterol which was significantly higher than the 6.0 mg/dL reduction observed in control subjects. Similarly, reductions in the LDL/HDL ratio in the PSY and OB groups were significantly more pronounced than those observed for the control group (p<0.01) as indicated in Table 5. Psyllium and oat bran intake had similar reductions of plasma total and LDL cholesterol. Changes in HDL cholesterol and triglycerides were not different among the three dietary groups.
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Table 5. Difference between baseline and 8 weeks of treatment in plasma total cholesterol, LDL cholesterol, HDL cholesterol, triglycerides and LDL/HDL ratio for all subjects in the wheat bran (control), psyllium or oat bran groups
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After analyzing changes in plasma lipids among groups, the efficiency of each dietary treatment compared to baseline was evaluated. Plasma total cholesterol concentrations were significantly reduced after 8 weeks of PSY or OB consumption for the normal and the hypercholesterolemic population (Table 6). The plasma cholesterol reduction ranged from 10 to 19% for the PSY group and 10 to 14% for the OB. No significant differences in plasma cholesterol were observed for subjects consuming the wheat bran cookies (control diet).
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Table 6. Changes between baseline and 8 weeks in total cholesterol of normal (cholesterol<220 mg/dL) or hypercholesterolemic (cholesterol>220 mg/dL) subjects fed control, psyllium or oat bran cookies1
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The observed reductions in plasma cholesterol concentrations were mostly associated with decreases in plasma LDL cholesterol as indicated in Table 7. Subjects consuming PSY or OB cookies had a 20 to 27% reduction in plasma LDL cholesterol after 8 weeks of consumption of these sources of dietary soluble fiber which was highly significant (p<0.0001). Although subjects consuming the wheat bran cookies had a small reduction in plasma LDL cholesterol in the order of 0.5 to 8%, it was not significantly different from baseline values (p>0.05).
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Table 7. Changes between baseline and 8 weeks in LDL cholesterol of normal (cholesterol<220 mg/dL) or hypercholesterolemic (cholesterol>220 mg/dL) subjects fed control, psyllium or oat bran cookies1
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No significant changes were observed in plasma HDL cholesterol for any of the dietary treatments for the normal or hypercholesterolemic subjects (p>0.05) (Table 8). Plasma triglycerides did not change for the majority of the tested groups except for the oat bran group in the hypercholesterolemic individuals where a 27% reduction in plasma triglycerides was observed after 8 weeks of treatment (Table 8). From the observed values in these variables, it is clear that the control group had normal HDL levels while the two groups assigned to the soluble fiber treatments were characterized by low plasma HDL cholesterol concentrations. In addition, all hypercholesterolemic individuals were characterized by having high baseline plasma triglycerides in addition to the high cholesterol values which probably classify these individuals as having mixed hyperlipidemia (Table 8). Further, individuals from the OB and characterized as normal (plasma cholesterol<220 mg/dL) also had elevated plasma triglyceride values at baseline.
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Table 8. Changes between baseline and 8 weeks in plasma HDL cholesterol and triglyceride of normal (cholesterol<220 mg/dL) or hypercholesterolemic (cholesterol>220 mg/dL) subjects fed control, psyllium or oat bran cookies1
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The overall LDL/HDL ratio, a reliable predictor for coronary heart disease risk was significantly improved after 8 weeks of PSY or OB intake (p<0.001) (Table 9). Although the control group presented a reduction in the LDL/HDL ratio after 8 weeks, this value was not significantly different from the baseline in the normal or the hypercholesterolemic individuals.
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Table 9. Changes between baseline and 8 weeks in LDL/HDL ratio of normal (cholesterol<220 mg/dL) or hypercholesterolemic (cholesterol>220 mg/dL) subjects fed control, psyllium or oat bran cookies1
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DISCUSSION
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In this study, we demonstrated that enriching the diet with a fiber supplement derived from psyllium or oat bran reduced plasma LDL cholesterol concentrations and improved the LDL/HDL ratio in a population characterized by having significant lipid disorders including high plasma cholesterol and triglycerides and low levels of HDL cholesterol.
In these studies, recommendations were made to subjects to decrease the consumption of dietary items high in fat and dietary cholesterol characteristic in this part of Mexico. Subjects obviously complied since intake of meat, organs, bacon, chorizo and other high fat foods typical of the daily intake of this population were reduced as assessed by the food frequency questionnaire. Moderate intakes of alcohol have been associated with higher plasma HDL levels [32,33]. However, alcohol intake was monitored in this study due to the association between hypertriglyceridemia and high alcohol consumption [34,35] since most of the subjects participating in this study had elevated plasma triglyceride levels.
Although eggs, a known source of dietary cholesterol were included in the dietary frequency questionnaire, a recently published meta-analysis including 224 studies with 8,143 individuals, either free-living subjects or metabolic ward patients, reported that decreasing dietary cholesterol from the average 385 mg/day to 300 mg/day would reduce plasma total cholesterol only by 1.9 mg/dL [36]. According to that same study, reducing fat content from 37 to 30% and saturated fat from 13 to 10% would decrease plasma cholesterol by 5.8 mg/dL, a more significant response [36]. However, studies by Schaefer et al [37] have demonstrated that there is a genetic component to the response to dietary cholesterol possibly associated with different apo E phenotypes [37]. Since the subjects participating in this study, especially the hypercholesterolemic group appear to have substantial lipid disorders, it is possible that they can be classified in one of those phenotypes where subjects are more responsive to dietary cholesterol [37]. Thus, typical foods high in dietary fat and cholesterol were included in this questionnaire.
The results from this study are in agreement with several reports on the hypocholesterolemic effects of psyllium [8–10] and with some of the reports on the plasma cholesterol lowering effects of oat bran [4,13,14]. Psyllium apparently lowers plasma cholesterol even in the cases where individuals consume high fat diets [38]. In contrast, oat bran apparently is not as effective in the cases of individuals consuming high amounts of fat [11]. In the present study, individuals decreased their normal fat consumption which agrees with oat bran being effective with lower intakes of dietary fat. In this study, we observed a substantial decrease in plasma triglycerides for the hypercholesterolemic individuals. Similar to our results, Anderson et al [4] reported a 19% significant reduction in plasma triglycerides in hypertriglyceridemic individuals consuming oat bran while no significant changes in this parameter were observed for the normotriglyceridemic subjects.
The direct action of psyllium in the intestinal lumen appears to be related to interruption of the enterohepatic circulation of bile acids which will alter hepatic cholesterol homeostasis and reduce plasma LDL cholesterol concentrations [39]. Studies by Everson et al [9] have demonstrated that psyllium does not reduce cholesterol absorption but rather binds to the bile acids emphasizing that this action could be the major primary mechanism by which psyllium reduces plasma cholesterol.
Studies conducted in animal models are in agreement with the human studies. In guinea pigs, psyllium intake is not related to decreases in cholesterol absorption but rather to interruption of entero-hepatic circulation of bile acids associated with the observed up-regulation of cholesterol 7-hydroxylase activity [17]. Similarly in hamsters, psyllium increases both the activity and mRNA abundance of this enzyme [19]. In addition, and similar to the human studies, reductions in plasma LDL cholesterol concentrations have been observed in guinea pigs and hamsters with both normal and hypercholesterolemic diets [15–19] indicating that psyllium is effective independent of the amount of dietary lipids. There are several metabolic responses associated with this primary action of psyllium in the small intestine which have been studied in detail in hamsters and guinea pigs.
The increases in cholesterol catabolism via bile acid synthesis results in a substantial reduction in hepatic cholesterol concentrations [15]. This reduction in hepatic cholesterol pools has been shown to alter hepatic cholesterol homeostasis in guinea pigs by up-regulating HMG-CoA reductase and down-regulating ACAT activities, the regulatory enzymes of cholesterol synthesis and esterification, respectively [15,16]. As a result of these alterations, secretion rates of apo B VLDL are reduced [18]. LDL apo B flux is decreased [18,21,22] and there are increases in LDL catabolism due to the up-regulation of hepatic apo B/E receptors [15,17,21]. It is possible that similar mechanisms are taking place in humans as a response to the increases in bile acid excretion [9,39] and that mobilization of hepatic cholesterol for the synthesis of bile acids also occurs resulting in the up-regulation of LDL receptors and increased LDL removal from plasma.
The active ingredient in oat bran is ß-glucan and carefully controlled studies in ileostomic patients have shown that bile acid excretion is increased during oat bran consumption compared to wheat bran or oat bran containing hydrolyzed ß-glucan [13]. These results suggest that both oat bran and psyllium have similar primary mechanisms in the intestinal lumen which result in plasma LDL cholesterol lowering. The observed decreases in plasma triglycerides due to oat bran intake in our present report and in the findings of other investigators [4,40] suggest that oat bran might decrease VLDL synthesis rates or accelerate VLDL removal in hyperlipidemic individuals as has been observed by other dietary interventions that lower plasma triglycerides [41,42]. Although other studies have shown a lack of effect of oat bran in decreasing plasma cholesterol [11,12], several reports [4,13,14], including our present study have shown that this source of soluble fiber is effective in lowering plasma cholesterol.
In summary we can conclude from this study that psyllium and oat bran were equally potent in reducing plasma LDL cholesterol concentrations and improving LDL/HDL ratio in normal subjects and in those with lipid disorders when an effort was made to reduce the amount of dietary fat. Further, oat bran had an additional beneficial effect in hypercholesterolemic individuals by reducing plasma triglycerides. This study is relevant to the individuals living in the Northern region in Mexico characterized by having the highest plasma cholesterol levels compared to the rest of the country [26] in addition to elevated plasma triglycerides and low HDL levels. Inclusion of a source of dietary soluble fiber supplement in addition to controlling fat intake appears to be quite effective for this population.
Received January 1, 1998.
Accepted May 1, 1998.
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ABSTRACT
INTRODUCTION
