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© 2004 The American Society for Nutritional Sciences J. Nutr. 134:2617-2622, October 2004

Nutrient Metabolism

Reduced and High Molecular Weight Barley ß-Glucans Decrease Plasma Total and Non-HDL-Cholesterol in Hypercholesterolemic Syrian Golden Hamsters1

Thomas A. Wilson, Robert J. Nicolosi2, Bryan Delaney*,3, Kim Chadwell, Vikas Moolchandani, Timothy Kotyla, Sridevi Ponduru, Guo-Hua Zheng*, Richard Hess*, Nathan Knutson*, Leslie Curry*, Lore Kolberg*, Melanie Goulson* and Karen Ostergren*

Center for Health and Disease Research, Department of Health and Clinical Sciences, University of Massachusetts—Lowell, Lowell, MA 01854 and * Cargill Health and Food Technologies, Wayzata, MN 55391

2To whom correspondence should be addressed. E-mail: Robert_Nicolosi{at}uml.edu.


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Consumption of concentrated barley ß-glucan lowers plasma cholesterol because of its soluble dietary fiber nature. The role of molecular weight (MW) in lowering serum cholesterol is not well established. Prior studies showed that enzymatic degradation of ß-glucan eliminates the cholesterol-lowering activity; however, these studies did not evaluate the MW of the ß-glucan. The current study was conducted to evaluate whether barley ß-glucan concentrates, partially hydrolyzed to reduce MW, possess cholesterol-lowering and antiatherogenic activities. The reduced MW fraction was compared with a high MW ß-glucan concentrate from the same barley flour. Concentrated ß-glucan preparations were evaluated in Syrian Golden F1B hamsters fed a hypercholesterolemic diet (HCD) with cholesterol, hydrogenated coconut oil, and cellulose. After 2 wk, hamsters were fed HCD or diets that contained high or reduced MW ß-glucan at a concentration of 8 g/100 g at the expense of cellulose. Decreases in plasma total cholesterol (TC) and non-HDL-cholesterol (non-HDL-C) concentrations occurred in the hamsters fed reduced MW and high MW ß-glucan diets. Plasma HDL-C concentrations did not differ. HCD-fed hamsters had higher plasma triglyceride concentrations. Liver TC, free cholesterol, and cholesterol ester concentrations did not differ. Aortic cholesterol ester concentrations were lower in the reduced MW ß-glucan-fed hamsters. Consumption of either high or reduced MW ß-glucan increased concentrations of fecal total neutral sterols and coprostanol, a cholesterol derivative. Fecal excretion of cholesterol was greater than in HCD-fed hamsters only in those fed the reduced MW ß-glucan. Study results demonstrate that the cholesterol-lowering activity of barley ß-glucan may occur at both lower and higher MW.

KEY WORDS: • barley glucans • plasma cholesterol • aortic cholesterol • fecal sterols

Clinical trials have demonstrated that consumption of oats or barley lowers serum cholesterol concentrations (1–7). Similar results have been reported in hamsters fed hypercholesterolemic diets (8–12). The substance present in the soluble fiber fraction of both cereal grains to which this effect has been attributed is (1->3)(1->4)-ß-D-glucan (ß-glucan).4 Clinical and animal studies that used concentrated ß-glucan preparations from oats and barley showed similar properties in humans (13,14) and hypercholesterolemic hamsters (8–11,15–17). Structural differences between oat and barley ß-glucan have been reported (18–20), as have differences between molecular weight (MW) (21) and solubility (22), but the cholesterol-lowering properties are approximately equivalent (23).

A distinguishing feature of native ß-glucan from either oats or barley is the high MW (≥1000 kDa) (21). Because the high MW of ß-glucan contributes to high viscosity in food applications and undesirable sensory properties, production of reduced MW ß-glucan preparations has been considered. It was shown that preparations of ß-glucan concentrates from barley cultivars with low viscosity do not possess cholesterol-lowering activity (24,25). In addition, reduced MW ß-glucan concentrates that are likely to possess more desirable sensory properties have been prepared either by addition of exogenous ß-glucanase enzymes or by manipulation of endogenous ß-glucanase activity during production. However, these studies reported that enzymatic hydrolysis of high MW ß-glucan either reduces or eliminates the cholesterol-lowering activity (24,26,27). The relation between the MW of ß-glucan and its cholesterol-lowering activity is difficult to establish from these previous studies because the MW was not determined either before or after enzymatic treatment. Recent studies suggest that ß-glucan concentrates with intermediate MW may, in fact, possess cholesterol-lowering activities similar to those of high MW ß-glucan (28). Therefore, while the evidence suggests that consumption of high MW ß-glucan can lower plasma cholesterol concentrations and that consumption of reduced MW ß-glucan does not, it cannot be determined from the available studies whether there is any cholesterol-lowering activity associated with consumption of a ß-glucan concentrate with a MW between that found in the grain and the enzymatically degraded ß-glucan.

The present study was conducted to evaluate the possibility that the hypocholesterolemic activity of ß-glucan exists at both high and low MW. Concentrated high MW ß-glucan (MW = 1000 kDa) was prepared from barley. A reduced MW ß-glucan concentrate (MW = 175 kDa) was produced from the same barley flour by enzymatic digestion with ß-glucanase. The effect of dietary consumption of these preparations on lipoprotein cholesterol, plasma lipids, fecal excretion of neutral sterols, and aortic cholesterol accumulation in hamsters fed a hypercholesterolemic diet (HCD) was evaluated.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
    Production and characterization of high MW and reduced MW barley ß-glucan concentrates. Concentrated high MW/viscosity ß-glucan was prepared from milled barley (waxy hulless) flour, using a modification of the extraction method of Aman and Hesselman (29) as described previously (23). A reduced MW/viscosity variant was prepared by extraction from the same barley flour with a ß-glucanase preparation from Bacillus amyloliquefaciens (Spezyme LT75, Genencor International) under conditions similar to those used for high MW ß-glucan extraction (23). Concentrations of ß-glucan in all preparations were determined using a Megazyme kit version (Megazyme International) of the McCleary method [AOAC Method 995.16; see (30,31)] (Table 1).


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  		TABLE 1 Characterization of ß-glucan concentrates

 
    Characterization of high MW and reduced MW barley ß-glucan concentrates. The MW distribution of ß-glucan was assessed using size-exclusion chromatography (HPSEC) coupled with multiangle laser-light scattering (MALLS) and refractive index (RI) detectors. The HPSEC system consisted of the Waters 2690 liquid chromatograph, a Wyatt DAWN EOS detector (Wyatt Technology), and a Waters R410 RI detector in series. HPSEC was performed using 3 columns (300 x 8.0 mm) in series (Shodex OHpak SB-805 HQ, SB-804 HQ, and SB-803 HQ) running at 50°C. The mobile phase was water with 200 mg/L sodium azide at a rate of 1 mL/min. Samples were prepared at 0.1% (w:v) ß-glucan concentration and filtered (0.45 µm) before being injected (100 µL). The Wyatt DAWN EOS MALLS detector calculates MW distribution using ASTRA 4.73.04 with auxiliary input from the RI detector. All necessary steps (calibration, normalization, etc.) suggested by Wyatt were performed prior to analysis. The calculation used 0.150 (refractive index increment) as the RI increment for ß-glucan (Fig. 1).



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  		FIGURE 1 Molar mass distribution of extracted ß-glucan concentrates used for the reduced MW and high MW barley diets fed to hamsters for 6 wk. Solid line = high MW, dashed line = reduced MW.

 
    Diets. All diets were formulated and dietary ingredients were supplied by Research Diets, except barley ß-glucan concentrates, which were prepared by Cargill Health and Food Technologies. Diet ingredients for all groups were identical except for the proportion of concentrated barley ß-glucan (Table 2). The control HCD contained 15 g cellulose/100 g, while the experimental diets were formulated to contain 8 g/100 g of ß-glucan from barley by addition of the ß-glucan concentrate from the respective source at the expense of cellulose. The control group was fed the basic HCD. The high MW ß-glucan group was fed the HCD containing 8 g ß-glucan/100 g (MW = 1000 kDa) from barley in place of cellulose. The reduced MW ß-glucan was fed the HCD containing 8 g ß-glucan/100 g (MW = 175 kDa) from barley in place of cellulose. Analytical characterization of ß-glucan was conducted on hamster feed to validate composition and homogeneity of dietary blending and stability under conditions of storage and use. Hamster feed was milled and ß-glucan was quantified by using a Megazyme kit version of the McCleary method [AOAC method 995.16; see (30,31)].


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  		TABLE 2 Composition of hamster feed1

 
    Animals. Thirty male Syrian Golden hamsters (F1B strain, BioBreeders) ~8–10 wk of age were acclimated to individual stainless-steel cages and were fed a HCD for 2 wk prior to initiation of the experimental diets. Hamsters were then bled to determine plasma concentrations of TC, HDL-C, and non-HDL-C; they were divided into 3 groups (n = 10/group) with similar starting plasma non-HDL-C levels, and were fed the specified diets. Hamsters were maintained in accordance with the guidelines of the Animal Care Committee at the University of Massachusetts-Lowell Research Foundation and the guidelines prepared by the Committee on the Care and Use of Laboratory Animals of the Institute of Laboratory Animal Resources, National Research Council (DHEW publication no. 85-23, revised 1985). Hamsters were housed in environmentally controlled conditions with an alternating 12-h light:dark cycle and were given food and water ad libitum, except when food was withheld for the experimental protocols described below.

    Plasma lipoprotein cholesterol and triglyceride (TG). Blood was collected via the retro-orbital sinus into heparinized tubes from hamsters deprived of food for 12 h at wk 0, 2, 4, and 6. Plasma TC, HDL-C, non-HDL-C, and TG concentrations were measured as described previously (23).

    Aortic cholesterol. At the end of the exposure period (wk 6), hamsters were killed with an intraperitoneal injection of sodium pentobarbital, and aortic tissue was obtained for determination of cholesterol concentration. The heart and the thoracic aorta were removed and were stored in PBS at 4°C for subsequent analysis. Cholesterol concentrations in the aortic arch were determined as described previously (23).

    Hepatic cholesterol. Hepatic cholesterol concentrations were measured using methods described previously (23,33). After the entire liver was removed, a small portion (100 mg) of the lower right lobe was used for all analyses of cholesterol composition in each hamster.

    Fecal neutral sterols. Fecal samples were collected over the final 3 d of the exposure period, freeze-dried (lyophilized), and ground prior to analysis. Concentrations of total fecal cholesterol, and total and individual neutral sterols (coprostanol, campesterol, ß-sitosterol, ß-sitostanol) were determined as described previously (23) and based on external standards available.

    Statistical analysis. Repeated-measures one-way ANOVA was used to examine the effect of treatment over time on plasma cholesterol concentrations and body weight, using SigmaStat software (Jandel Scientific). A one-way ANOVA was used to examine the effect of treatment on food consumption, liver and aortic cholesterol concentrations, and fecal neutral sterol concentrations. When there were differences between experimental groups by repeated-measures ANOVA or ANOVA, a Student-Newman-Keuls post-hoc test was performed as previously reported (34), using SigmaStat. Differences were considered significant at P < 0.05. Values in the text are means ± SEM.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
    Body weights and food consumption. The hamsters adapted well to all diets, and all survived the dietary treatments. Food consumption did not differ among the HCD, high MW ß-glucan, and reduced MW ß-glucan-fed groups during the 6-wk study (14.7 ± 2.20, 15.3 ± 1.40, and 14.9 ± 2.13 g/d, respectively). Body weights also did not differ among the groups at each time point. The body weights of the hamsters fed the HCD, high MW ß-glucan, and reduced MW ß-glucan diets at wk 0 (91.6 ± 1.66, 89.4 ± 2.22, and 91.2 ± 1.90 g, respectively) were increased (P < 0.05) by wk 6 (104.5 ± 2.43, 101.9 ± 4.14, and 101.2 ± 1.94 g, respectively).

    Plasma cholesterol concentrations. Plasma cholesterol (TC, non-HDL-C and HDL-C) concentrations in hamsters fed the HCD were approximately the same in all groups after the 2-wk lead-in period. After the lead-in period diets, hamsters were fed the indicated diets. Plasma lipid and lipoprotein cholesterol concentrations measured at wk 2, 4, and 6 of the treatment period did not differ from one another, so the mean of the 3 data points was used. Compared with hamsters fed the HCD, there was a decrease in plasma TC and non-HDL-C concentrations in the hamsters fed reduced MW ß-glucan (–36% and –50%, respectively) and hamsters fed high MW ß-glucan (–32% and –43%, respectively) (P < 0.05) (Table 3). The magnitude of the decrease in plasma TC and non-HDL-C concentrations was not distinguishable based on the MW of the barley ß-glucan. Plasma HDL-C concentrations did not differ among any of the dietary treatment groups at the end of 6 wk. Plasma TG concentrations were lower in the hamsters fed reduced MW ß-glucan (–58%) and hamsters fed high MW ß-glucan (–38%) (P < 0.05) compared with hamsters fed the HCD. Compared with hamsters fed the HCD, the plasma TC:HDL-C ratio decreased in the hamsters fed reduced MW ß-glucan (–35%) and high MW ß-glucan (–29%) (P < 0.05).


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  		TABLE 3 Plasma lipids and lipoprotein cholesterol concentrations in hypercholesterolemic hamsters fed the control (HCD) diet and either reduced or high MW barley ß-glucans for 6 wk1, 2

 
    Liver cholesterol concentrations. Following the 6-wk treatment, liver total cholesterol concentrations did not differ significantly among hamsters fed the HCD, those fed the high MW ß-glucan, or those fed the reduced MW ß-glucan (3.09 ± 0.46, 3.65 ± 0.60, and 3.01 ± 0.52 mmol/g, respectively). Liver free cholesterol concentrations did not differ significantly among hamsters fed the HCD, hamsters fed high MW ß-glucan, and hamsters fed reduced MW ß-glucan (1.51 ± 0.29, 1.82 ± 0.31, and 1.51 ± 0.26 mmol/g, respectively). Also, the liver esterified cholesterol concentrations did not differ significantly among hamsters fed the HCD, hamsters fed high MW ß-glucan, and those fed reduced MW ß-glucan (1.58 ± 0.34, 1.83 ± 0.35, and 1.50 ± 0.37 mmol/g, respectively).

    Aortic cholesterol concentrations. At the end of the 6-wk treatment, compared with the hamsters fed the HCD and the hamsters fed the high MW barley ß-glucans, aortic esterified cholesterol concentrations were significantly lower in the reduced MW barley ß-glucan group (–51% and –42%, respectively) (P < 0.05) (Table 4). Compared with the hamsters fed reduced MW ß-glucan, aortic free cholesterol concentrations were significantly lower in the hamsters fed the HCD (–69%) and the hamsters fed high MW ß-glucan (64%) (P < 0.05). Aortic total cholesterol concentrations did not differ among groups.


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  		TABLE 4 Aortic cholesterol concentrations in hypercholesterolemic hamsters fed the control (HCD) diet and either reduced or high MW barley ß-glucans for 6 wk1

 
    Fecal neutral sterol concentrations. Compared with the hamsters fed the HCD, total fecal neutral sterol concentrations increased significantly in the hamsters fed high (93% increase; P < 0.05) and reduced MW ß-glucan (107% increase; P < 0.05; Table 5). However, fecal excretion of cholesterol increased significantly only in the hamsters fed the reduced MW ß-glucan (331%; P < 0.05) compared with the hamsters fed the HCD. Compared with the hamsters fed the HCD, feeding of either high (85% increase) or reduced MW ß-glucan (96% increase) significantly increased fecal coprostanol concentrations (P < 0.05). Fecal excretion of ß-sitosterol increased significantly only in the reduced MW ß-glucan group (200%) compared with the HCD group (P < 0.05). There were no differences among dietary treatment groups for the excretion of other fecal neutral sterols.


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  		TABLE 5 Excretion of total fecal neutral sterols in hypercholesterolemic hamsters fed the control (HCD) diet and either reduced or high MW barley ß-glucans for 6 wks1

 

   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The high MW of ß-glucan is thought to be important for the cholesterol-lowering activity and other physiological activities associated with consumption of barley grain or ß-glucan concentrate prepared from this grain. However, the relation between the MW of barley ß-glucan and its cholesterol-lowering activity has not been well established. Wood et al. (35) reported a significant linear inverse relation between the glycemic response to a 50-g oral glucose load and the viscosity of oat ß-glucan solutions. In that study, the viscosity of the test oat ß-glucan was modified by the combination of partial hydrolysis of ß-glucan and changing the concentration of ß-glucan in the solution. Wood and Beer (36) showed that processing (e.g., extrusion) reduced the MW of oat ß-glucan but had little effect on its cholesterol-reducing properties. In rats, feeding an ethanol-water and wet-milled oat ß-glucan concentrate reduced serum TC by 30%, whereas a cold-water and wet-milled ß-glucan concentrate reduced cholesterol by 10% compared with rats fed a cellulose control diet, although the latter had higher MW and higher hydrodynamic volume (37). In addition, a recent study with hamsters demonstrated a similar cholesterol-lowering effect of oat ß-glucan with MW varying from 136 kDa to 1650 kDa (28).

The current study is the first to evaluate the cholesterol-lowering activity of a reduced MW ß-glucan concentrate prepared from barley in hamsters fed HCD. Barley ß-glucan concentrate was prepared from waxy hulless barley cultivars that have previously been shown to lower plasma cholesterol concentrations in hamsters fed the HCD (23). The ß-glucan in this preparation had a MW of 1000 kDa, as demonstrated by Size Exclusion Chromatography-MALLS-RI. A reduced MW ß-glucan concentrate (MW of 175 kDa) was prepared by limited enzymatic hydrolysis of the high MW barley ß-glucan. There were decreased plasma TC concentrations in hamsters fed the HCD supplemented with concentrated barley ß-glucan, regardless of the MW, in this study. The magnitude of the decrease was consistent with previous studies evaluating the effect of high MW ß-glucan concentrates from barley (9,23). However, for reasons yet to be determined, the results of the current study with a low MW (175 kDa) having cholesterol-lowering properties is contrary to other studies that reported that enzymatic hydrolysis of high MW ß-glucan either reduces or eliminates the cholesterol-lowering activity (24,26,27). One possibility is that the relation between the MW of ß-glucan and cholesterol-lowering activity is difficult to establish from these previous studies (24,26,27), because the MW was not determined either before or after enzymatic treatment. Thus, it is difficult to know whether the MW of ß-glucans in the earlier studies was lower or higher than the MW of ß-glucans in the current study. Another possible explanation is that only a partial enzymatic process was used to produce our ß-glucan preparation in the current study vs. a complete hydrolysis procedure that was used in the other studies.

The effect on plasma TC was primarily attributable to decreased plasma non-HDL-C concentrations. However, because there was a decrease in plasma TGs, and the non-HDL-C value includes VLDL-C as well as LDL-C, it is possible that the decreased effect on the plasma TC is partly due to the decrease in VLDL-C rather than just LDL-C. Also, there was no decrease in plasma HDL-C concentrations in hamsters fed either the reduced or high MW ß-glucan, which is contradictory to other studies (8,9,15,23) but similar to observations in humans (1–3,5,13,38–40). The differences between the current study and previous studies (8,9,15) are that different sources of dietary fiber or ß-glucans were used and the length of the studies differed. Also, in our earlier study with the high MW ß-glucan (23), there was a significant decrease in plasma HDL-C after 9 wk of dietary treatment, whereas in the current study, there was only a slight decrease (P = 0.47) in plasma HDL-C after 6 wk of dietary treatment. Thus, the difference between the current study and our earlier one (23) with high MW ß-glucan may have been the length of the study. It is possible that if the current study had been 9 wk in duration, this decreasing trend in plasma HDL-C concentrations with the high MW ß-glucan may have become significant.

The ability of soluble fiber, and specific components therein, to lower serum cholesterol concentrations is thought to occur through a combination of mechanisms. Other studies have shown that consumption of ß-glucans inhibits the absorption of cholesterol from the gut, as demonstrated by significant increases in the excretion of fecal cholesterol and neutral sterols (2,41,42). In the current study, there was a large increase in the combined fecal excretion of cholesterol and coprostanol, a cholesterol metabolic derivative, in hamsters fed concentrated reduced or high MW ß-glucan compared with those fed the HCD. In addition, the hamsters fed reduced MW ß-glucan produced a significant increase in fecal cholesterol and ß-sitosterol excretion, though probably not biologically important for the latter, compared with the hamsters fed the HCD. However, the hamsters fed the high MW ß-glucan only significantly increased fecal excretion of coprostanol compared with those fed the HCD. These observations suggest that the reduced MW ß-glucan prevents the absorption of cholesterol and its derivatives (coprostanol) and other plant sterols (ß-sitosterol), to a slightly greater extent than the high MW ß-glucan. Together, these observations support the concept that the plasma cholesterol-lowering properties of ß-glucan are at least partly attributable to inhibition of cholesterol absorption and increased cholesterol metabolism in the gut.

The current study also demonstrated similar aortic TC concentrations in all groups. The high aortic TC concentrations in hamsters fed the HCD were primarily attributable to esterified cholesterol. In contrast, the aortic TC concentrations in hamsters fed reduced MW barley ß-glucan were almost entirely due to free cholesterol. This observation of significantly lower cholesterol ester accumulation in the hamsters fed the reduced MW barley ß-glucan compared with hamsters fed the HCD is particularly important because the tissue cholesterol ester concentration is viewed as the hallmark in fatty streak formation (43). There was no significant reduction in aortic cholesterol ester in hamsters fed the high MW ß-glucan diet compared with those fed the HCD; however, there was a slight decrease (P = 0.65). The reductions in aortic cholesterol ester and increase in free cholesterol accumulation in the hamsters fed the reduced MW ß-glucan compared with the controls are unexplainable at this time. However, one possibility may be that ACAT (acyl cholesterol acyl transferase) activity or synthesis may be decreased by lower MW ß-glucan; thus, although cholesterol accumulation is not different, esterification of cholesterol is effected. Future studies are needed to study this mechanism.

Although MW is a factor in the cholesterol-lowering activity of ß-glucan, the results of the current study demonstrate that both high MW and reduced MW ß-glucan concentrates from barley lower plasma cholesterol concentrations in hamsters with similar potency and through similar mechanisms of action. However, it appears that different mechanisms are working on the other indicators associated with atherogenic progression, i.e., aortic cholesterol accumulation, possibly through ACAT activity. The differences in structure and physical properties between reduced and high MW ß-glucan in barley do not appear to be absolute. Rather, partial reduction of the MW of ß-glucan still results in significant cholesterol lowering. Based on these results, it is likely that expanded use of ß-glucan concentrates from barley into new applications that were previously limited by high viscosity and undesirable sensory properties may be considered.


   ACKNOWLEDGMENTS
 
The authors would like to thank Subbiah Yoganathan and Garry Handelman for their technical assistance and Maureen Faul for her administrative assistance.


   FOOTNOTES
 
1 This study was sponsored by Cargill, Inc., Health and Food Technologies, Wayzata, MN. Back

3 Current address: DuPont Haskell Laboratory, Newark, DE 19714. Back

4 Abbreviations used: ACAT, acyl cholesterol acyl transferase; ß-glucan, large molecular weight water-soluble cell-wall polysaccharide consisting of (1->3,1->4)-ß-D-linked glucopyranosyl-monomer; HCD, hypercholesterolemic diet; HDL-C, HDL cholesterol; HPSEC, high-performance size-exclusion chromatography; MALLS, multiangle laser light scattering; MW, molecular weight (in this study, MW represents the weight average of the molecular weight distribution of the sample); non-HDL-C, VLDL + LDL cholesterol; RI, refractive index; TC, total cholesterol; TG, triglyceride. Back

Manuscript received 21 April 2004. Initial review completed 17 May 2004. Revision accepted 13 July 2004.


   LITERATURE CITED
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

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