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A diet rich in oat bran improves blood lipids and hemostatic factors, and reduces apparent energy digestibility in young healthy volunteers

Subjects

Abstract

Background/Objectives:

Oat bran shows cholesterol-lowering properties, but its effects on other cardiovascular risk markers are less frequently investigated. This study examined the effects of oat bran on blood lipids, hemostatic factors and energy utilization.

Subjects/Methods:

A double-blind, randomized crossover study in 24 adults (age 25.2±2.7 years; body mass index: 24.9±2.9 kg/m2), who completed two 2-week dietary intervention periods: low-fiber diet (control) or an oat bran (control +102 g oat bran/day) diet. Fasting blood samples were drawn before and after each period, and 3-day fecal samples were collected during the last week of each period.

Results:

Total cholesterol decreased by 14% during the oat bran period compared with 4% during the control period (P<0.001). Non-high-density lipoprotein (HDL) cholesterol decreased by 16% in the oat bran period compared with 3% in the control period (P<0.01), as did total triacylglycerol (21 vs 10%, P<0.05) and very-low-density lipoprotein triacylglycerol 33 vs 9%, P<0.01). Plasminogen activator inhibitor-1 (PAI-1) and factor VII (fVII) levels decreased more during consumption of oat bran compared with the control period (PAI-1: 30 vs 2.3%, P<0.01; fVII: 15 vs 7.6%, <0.001). Fecal volume and dry matter were greater when consuming the oat bran diet compared with the control (P<0.001), and energy excretion was increased by 37% (1014 vs 638 kJ/day, P<0.001); however, changes in body weight did not differ (oat bran:−0.3±0.5 kg; control: 0.0±0.7 kg).

Conclusions:

Addition of oat bran (6 g soluble fiber/day) to a low-fiber diet lowered total and non-HDL cholesterol, as well as hemostatic factors, and may affect energy balance through reduced energy utilization.

Introduction

Prospective cohort studies suggest that consumption of dietary fibers protects against coronary heart disease (Pereira et al., 2004), although all mechanisms are not fully elucidated. The cholesterol-lowering effect of oats, rich in soluble mixed-linkage (1 → 3), (1 → 4)-β-D-glucans, has been known for decades (de Groot et al., 1963), and a large number of studies have demonstrated that oat products lower total and low-density lipoprotein (LDL) cholesterol significantly (Pick et al., 1996; Saltzman et al., 2001; Berg et al., 2003; Reyna-Villasmil et al., 2007). The US Food and Drug Administration allows a claim that food products containing oats that deliver 3 g of β-glucan daily can reduce the risk of heart disease (US Food and Drug Administration, 1997). Recently, the European Food Safety Authority issued an opinion that a cause and effect relationship between intake of oat β-glucans and reduction in blood cholesterol has been established (EFSA Panel on Dietetic Products, 2009).

In addition to a well-established lowering of total and LDL cholesterol (Brown et al., 1999), indications that blood pressure and insulin sensitivity are affected have been presented, and intake of soluble dietary fiber has also been negatively correlated with plasminogen activator inhibitor-1 (PAI-1), the major regulator of fibrinolysis under normal conditions (Djousse et al., 1998). Increased PAI-1 has been associated with increased cardiovascular risk (Gorog, 2010). Relatively small changes in PAI-1 levels can have significant effects overall (Lefevre et al., 2004), and both PAI-1 and factor VII (fVII) have been found to relate to postprandial increments in triacylglycerol (Lefevre et al., 2004). Dietary fat is known to affect PAI-1 and fVII (Lefevre et al., 2004), whereas effects of dietary fibers have been less studied. In addition, PAI-1 is involved in adipogenesis and high levels have been observed in obese individuals (Van Gaal et al., 2006); thus, dysfunction of the fibrinolytic and hemostatic systems in obesity may represent one of the links between obesity and cardiovascular disease (CVD).

The main aim of the present study was to examine the effect of oat bran consumption on zinc absorption; these results have been published previously (Sandstrom et al., 2000). Here, we present the effects of a diet rich in oat bran on lipid metabolism, hemostatic and fibrinolytic factors, as well as energy digestibility in young healthy adults on a strictly controlled diet.

Materials and methods

Study design

Two studies with similar designs were conducted in two consecutive years. The studies were designed as randomized crossover studies with 2 × 2 weeks dietary intervention periods separated by a washout period of 4 weeks. A total of 12 participants were enrolled in each of the two studies. The diets were based on ordinary food items and were similar in the two dietary periods apart from the incorporation of 102 g of oat bran/10 MJ in one period. Fasted blood samples were drawn on two consecutive days before and after each dietary period after an overnight fast of at least 10 h. The participants were instructed to refrain from physical exercise and any use of drugs for 48 h and from alcohol for 24 h. For this paper, feces samples collected during the last 3 days of each dietary intervention period were used to determine apparent energy digestibility.

Participants

The 24 participants enrolled in the two studies were 22–30 years of age, with a mean body weight of 24.9±2.9 kg/m2, all apparently healthy and non-smokers. One of the females used oral contraceptives, whereas none of the participants used other medications or dietary supplements. The participants were all given oral and written information about the study before signing a consent form before enrolment. The study was conducted in accordance with the Declaration of Helsinki Principles and approved by the local ethics committee of Frederiksberg and Copenhagen (KF.V.V.200.2016/90).

Diets

A standardized diet was provided for the participants, consisting of breakfast, lunch and evening meals, together with fruits and snacks; examples of the daily menus were presented previously (Sandstrom et al., 2000). The oat bran (Kungsörnen AB, Järna, Sweden) was incorporated into breads and served with each of the main meals. The participants were allowed to consume bottled mineral water ad libitum, and coffee/tea prepared from bottled mineral water. All foods were prepared in advance in the metabolic kitchen at the department. The lunch meals were served at the Department of Human Nutrition, whereas the breakfast and evening meals were provided for home consumption. On Fridays, the participants were provided all foods for Saturday and Sunday for consumption at home. The participants were instructed not to leave any foods, but if they did they were to bring the leftovers back for registration and analyses. The energy distribution of the standardized diets was similar apart from the content of dietary fiber with an intended macronutrient composition of 35 E% from fat, 15 E% from protein and 50 E% from carbohydrates (Table 1). The diet was adjusted to the energy requirements (ER) of the individual study participants. ER was assessed at a screening visit to the nearest megajoule, based on sex, weight and physical activity (PAL) level as follows (World Health Organization, 1985):

Table 1 Analyzed dietary composition of the experimental diets (per 10 MJ)

If they were not weight stable or experienced hunger after 2 days on the experimental diet, ER was adjusted and extra foods provided, such as bread rolls each providing 0.5 MJ with the same macronutrient composition as the whole diet. No measures were taken to lower energy intake if participants felt overly satiated or if they gained weight, as the diets had been prepared in advance.

Blood sample analyses

Serum triacylglycerol and total cholesterol (TC) levels were measured using enzymatic colorimetric test kits (Roche CHOL and TG, Roche Diagnostics GmbH, Mannheim, Germany). The intra-assay precisions were 0.6% and 0.9%, respectively. LDL cholesterol (LDL-C) and high-density lipoprotein cholesterol (HDL-C) levels were measured in serum using a homogeneous enzymatic colorimetric test kits (Roche HDL-C plus 2nd generation, Roche Diagnostics); intra-assay precision: 1.8%. The very-low-density lipoprotein fraction was isolated by ultracentrifugation as described elsewhere (Chapman et al., 1981), and triacylglycerol and cholesterol content was measured as described above. All lipid analyses were performed on a COBAS MIRA Plus (Roche Diagnostics). PAI-1 was determined by enzyme-linked immunosorbent assay, and intra-assay precision was 6% (TintElize PAI-1; Biopool, Umeå, Sweden). Percentage of plasma fVII was assessed using a one-step clotting assay, in which clotting time is recorded on a coagulometer and expressed relative to an internal standard (Schnittger-gross, Amelung, Germany) after incubation with human fVII-deficient plasma (Biopool), and initiation of the clotting process by addition of calcium chloride and human thromboplastin; intra-assay precision was measured to be 5%. All blood samples were analyzed within 2 years after completion of the study.

Diet sample analyses

Duplicate portions of the diets were analyzed for protein, fat, carbohydrates, non-starch polysaccharide, soluble and insoluble dietary fiber as previously described (Sandstrom et al., 2000).

Fecal sample analyses

Before analysis, the fecal samples were weighed, freeze-dried and homogenized. For each participant, 3-day fecal collections from the same dietary intervention period were pooled. Fecal energy was measured by bomb calorimetry within 2 years after completion of the study (Ika-calorimeter system C4000; Heitersheim, Germany).

Calculations and statistical analyses

All statistical analyses and calculations were performed using the Statistical Analysis System software package, version 9.1 (SAS Institute Inc., Cary, NC, USA). Apparent energy digestibility was calculated as the difference between intake and fecal loss, and expressed as a percentage of energy intakes. For all blood sample parameters, the mean of the two measurements obtained on two consecutive days before and after each dietary intervention period was calculated and used for the reporting of data. All dependent variables were controlled for homogeneity of variance and normal distribution by investigation of residual plots, normal probability plots and histograms. In a mixed linear analysis of covariance model, end point values of biochemical markers were modeled as the dependent variable to evaluate the effect of diet. Participants were modeled as a random variable, and body weight, sex and the corresponding baseline values were modeled as covariates, and period, as well as period × diet interaction, was included as fixed variables. A similar model was applied to investigate the effect of diet on fecal parameters; however, in this study, a corresponding baseline value was not available. For all analyses, only the period × diet interaction was omitted from the model when P>0.10. Results are presented as means±s.d., unless otherwise stated, and the statistical significance is defined as P<0.05.

Results

All participants completed the two dietary intervention periods. Body weight of the participants did not change significantly during the two dietary intervention periods (Table 2). Compliance with the diets was good, as assessed via daily contact with the study participants, and as also indicated by complete urine collections and 95% recovery of fecal transit markers (Sandstrom et al., 2000).

Table 2 Fasting concentrations of biochemical markers before and after each dietary intervention period (n=24) (mean±s.d.)

Blood lipids and hemostatic factors

Results on blood lipids and hemostatic factors are presented in Table 2. In the oat bran period, TC decreased by 14%, which was significantly different from the 4% decrease observed in the control (P<0.001). Decreases in LDL, HDL and very-low-density lipoprotein cholesterol of 13%, 11% and 33%, respectively, were observed during the oat bran period; however, they were not significantly different from changes seen during the control period, in which decreases of comparable magnitude were observed. With regard to changes in non-HDL cholesterol (total—HDL cholesterol), a 16% decrease was observed in the oat bran period, which differed significantly from the 3% decrease observed in the control period (P<0.01). In addition, total triacylglycerol concentrations decreased more during the oat bran period compared with the control period (21 vs 10%, P<0.05) as did very-low-density lipoprotein triglyceride (33 vs 9%, P<0.01), whereas no changes were observed for LDL+HDL triglyceride. Furthermore, both PAI-1 and fVII decreased significantly more during the oat bran period compared with the control period (PAI-1: 30 vs 2.3%, P<0.01; fVII: 15 vs 7.6%, <0.001).

Fecal parameters

Fecal volume was 45% larger during the oat bran period compared with the control period (197 vs 136 g/day, P<0.001) (Table 3), which was accompanied by a 37% increase in energy excretion (1014 vs 638 kJ/day, P<0.001); thus, apparent energy digestibility was reduced (92.6 vs 95.3%, P<0.001).

Table 3 Fecal volume, energy excretion and apparent energy digestibility during each dietary intervention period (n=22)

Fecal dry matter excretion was 70% higher with the oat bran diet compared with the control (P<0.001), whereas no difference was seen for % dry matter.

Discussion

Elevated plasma concentrations of LDL cholesterol and triacylglycerol, as well as low concentrations of HDL cholesterol, are well-established risk factors for CVD, and an improvement of the lipid profile is associated with reduced CVD morbidity and mortality. Non-HDL cholesterol is emerging as a CVD risk factor and is calculated by subtracting HDL cholesterol concentration from TC concentration (Cui et al., 2001; Robinson et al., 2009). In view of this, we focused on determining the changes in total, LDL, HDL and non-HDL cholesterol. We found that TC decreased significantly, as well as both HDL and LDL cholesterol, although these differences did not differ between diets. Non-HDL cholesterol level decreased in the oat bran period, which suggests a beneficial effect on CVD risk. In a meta-analysis by Brown et al. (1999), 1 g of soluble dietary fiber from oat was found to lower total and LDL cholesterol by 0.037 and 0.032 mmol/l, respectively, (Brown et al., 1999). In the present study, oat bran provided 6 g of soluble fiber daily (per 10 MJ), which means that total and LDL cholesterol levels were lowered by 0.098 and 0.058 mmol/l per 1 g of soluble fiber, respectively. This is a more pronounced effect than would be estimated based on the meta-analysis.

In recent years, β-glucans have been extracted from oats (and barley) in order to incorporate them into foods, as it can be difficult to consume sufficient amounts of oat bran or rolled oats to obtain a daily intake of 3 g β-glucans. However, some studies using β-glucan extracts fail to report cholesterol-lowering effects, which has been ascribed to degradation and depolymerization of the fiber through processing of both the extract and foods, which risk loss of viscosity (Wolever et al., 2010). Oat bran and rolled oats contain mixed-linkage (1 → 3), (1 → 4)-β-D-glucans high in molecular weight (>2000 kDa) (Aman et al., 2004), which is believed to be one of the major determinants of viscosity, and thought to, at least, in part, produce the cholesterol-lowering effects of soluble fibers (Brown et al., 1999; Theuwissen and Mensink, 2008). Thus, it is crucial to ensure that the β-glucans are not degraded during processing and, thus, rendered ineffective. This is in line with the opinions from the US Food and Drug Administration and the European Food Safety Authority who specify that products should be non- or minimally processed, such as rolled oats, in order to qualify for a health claim (US Food and Drug Administration, 1997; EFSA Panel on Dietetic Products, 2009). Furthermore, this supports the current shift in the paradigm from years of investigation of health-improving effects of biologically active compounds rather than whole foods, in which the benefits of food structures and synergies may be obtained.

In the present study, we found that consumption of oat bran lowered both PAI-1 activity and fVII concentrations. Similarly, 10 g of oat husk for 2 weeks has been shown to decrease PAI-1 activity without any changes in fVII (Sundell and Ranby, 1993), and Landin et al. (1992) found that 10 g of guar gum administered daily for 2 weeks decreased PAI-1 activity significantly (Landin et al., 1992). Increased postprandial fVII concentrations have been linked to lipid metabolism as it increases after intake of high-fat meals (Liu et al., 2008), and it is likely that the observed reduction in fVII and PAI-1 are linked, at least in part, to the decreased triacylglycerol concentrations observed in the present study. Previous studies have shown that oat bran can reduce postprandial plasma triacylglycerol responses (Cara et al., 1992; Dubois et al., 1995), and it is likely that a decreased postprandial lipemia, if occurring repeatedly over a 2-week period, may reduce not only fasting triacylglycerol concentrations but also PAI-1 activity and fVII concentrations. Mixed-linkage (1 → 3), (1 → 4)-β-D-glucans are fermentable, resulting in increased microbial production of short-chain fatty acids in the colon such as acetate, propionate and butyrate. It has been suggested that these may inhibit hepatic synthesis of coagulation factors through inhibition of fatty acid release (Venter and Vorster, 1989). Thus, the most likely mechanisms to explain an effect of soluble fiber on PAI-1 are its reducing effects on lipid absorption and on the flow of triacylglycerol-rich lipoproteins to the liver. Interestingly, abnormalities in hemostasis and lipid metabolism are often present in the same individual and are commonly associated with (central) obesity. PAI-1 has been found to be involved in adipogenesis, and elevated concentrations have been seen in obese subjects (Van Gaal et al., 2006). Thus, dysfunction of the fibrinolytic and hemostatic systems in obesity may represent one of the links between obesity and CVD.

Apart from cardioprotective effects of dietary fiber, a diet rich in wholegrain foods (Koh-Banerjee et al., 2004; Bazzano et al., 2005) and dietary fiber (Liu et al., 2003) has been associated with a smaller weight gain in prospective observational studies. This is thought to be mediated via a suppression of hunger and food intake, as well as a reduction in apparent nutrient digestibility (Astrup et al., 2010). In our study, we observed an 3% reduction in apparent energy digestibility with the addition of 102 g/10 MJ oat bran to a low-fiber diet, which has been observed before using similar doses of oat bran (Calloway and Kretsch, 1978; Chen et al., 1998), as well as other types of soluble dietary fibers, such as wholegrain rye (Wisker et al., 1996), a fiber mixture from grains, cereals and citrus (Rigaud et al., 1987), and a diet with mixed cereal fibers (Miles et al., 1988). It has been estimated that the gradual weight gain of 0.5–1 kg/year in American adults can be explained by a positive energy balance of <200 kJ/day in most people (Hill, 2006), implying a potential for increased consumption of oat products in body weight management as part of a ‘small changes strategy’ aimed at reducing positive energy balance. However, this needs to be addressed in a longer-term study, preferably in overweight participants.

The strengths of our study include the strictly controlled diet used, which, however, limited the duration of the study. Cholesterol concentrations have often found to decrease within 1–2 weeks, but we cannot rule out the fact that the effects would have been different if the study had lasted longer, which could be either a more pronounced effect or that the effect would level off and set at a new equilibrium. The effect of dietary fiber on energy utilization are directly linked to a limited absorption and thus appear rapidly; the short duration, however, does limit our ability to detect any body weight changes that may occur as a result of decreased energy utilization. However, we cannot rule out the fact that excess oat bran consumption could lead to changes in adaptation to a higher fiber intake, for example, a different fermentation pattern, which in time may affect energy utilization to some extent. Finally, molecular weight and viscosity of the oat bran used was not measured, and thus the link between the effects observed and the mechanisms involved remains unconfirmed, although in line with the current evidence.

In conclusion, the results of the present study suggest that a diet high in oat bran significantly improves multiple cardiovascular risk factors in healthy young adults.

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Acknowledgements

We gratefully acknowledge dietitian Hanne Mary Jensen, lab technician Hanne Lysdal Petersen, Kitchen assistants Karina Graft Rossen and Ingelise Lundgaard for their dedicated assistance with the practical work, and the volunteers for participating in the studies. The study was supported by a grant from the Faculty of Life Sciences, University of Copenhagen.

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Correspondence to M Kristensen.

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Kristensen, M., Bügel, S. A diet rich in oat bran improves blood lipids and hemostatic factors, and reduces apparent energy digestibility in young healthy volunteers. Eur J Clin Nutr 65, 1053–1058 (2011). https://doi.org/10.1038/ejcn.2011.102

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Keywords

  • oat bran
  • β-glucan
  • blood lipids
  • obesity
  • apparent digestibility
  • hemostasis

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