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Article

A Buckwheat Protein Product Suppresses Gallstone Formation and Plasma Cholesterol More Strongly than Soy Protein Isolate in Hamsters

Development, Health Care, Kissei Pharmaceutical Company, Ltd., Matsumoto 399-8710, Japan and ^* Department of Applied Biochemistry, Faculty of Applied Biological Science, Hiroshima University, Higashi-Hiroshima 739-8528, Japan

¹To whom correspondence should be addressed.

	ABSTRACT

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This study was conducted to investigate the effects of a buckwheat protein product (BWP) on plasma cholesterol, gallbladder bile composition and fecal steroid excretion in hamsters fed diets with 5 g/kg cholesterol. Diets also contained 200 g/kg of casein, soy protein isolate (SPI) or BWP as protein sources. After 2 wk, plasma and liver concentrations of cholesterol in the hamsters fed BWP were significantly lower than those in the hamsters fed casein and SPI. The molar proportion of cholesterol in gallbladder bile was significantly lower in the BWP group than in the other groups, whereas that of bile acids was slightly higher in the BWP group (P 0.05), resulting in the lowest lithogenic index in the BWP group. None of the hamsters fed BWP had gallstones, whereas they were present in some of the hamsters fed other proteins. Compared with casein intake, BWP intake resulted in significantly higher ratios of cholic acid to chenodeoxycholic acid and of cholic acid to lithocholic acid in the gallbladder bile. The excretions of fecal neutral and acidic steroids were markedly higher in the BWP group compared with the other groups (P 0.05). SPI intake also significantly lowered cholesterol level in gallbladder bile and caused higher fecal bile acids compared with casein intake, but the effects were significantly less than those of BWP (P 0.05). The results suggest that BWP suppresses gallstone formation and cholesterol level more strongly than SPI by enhancing bile acid synthesis and fecal excretion of both neutral and acidic steroids.

KEY WORDS: • buckwheat protein • soy protein • cholesterol • gallstone • hamsters

	INTRODUCTION

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Buckwheat protein has received increased attention because of the high nutritional value that results from its favorable amino acid composition (Eggum et al. 1981 , Fornal et al. 1981 , Pomeranz 1983 ). Previously, we prepared a buckwheat protein product (BWP)² from buckwheat flour (Kayashita et al. 1995 ). We found that BWP has a potent hypocholesterolemic activity in rats (Kayashita et al. 1995 ). This activity is far stronger than that of soy protein isolate (SPI). Our study further suggested that the cholesterol-lowering effect of BWP is mediated by a greater fecal excretion of neutral sterols and that the lower digestibility of BWP is at least partially responsible for the effect (Kayashita et al. 1997 ). To obtain further information on the effect of BWP on cholesterol metabolism, this study was conducted with male Golden Syrian hamsters to investigate its effects on cholesterol and bile acid metabolisms and on gallstone formation. Hamsters were selected because they exhibit several similarities with the cholesterol and bile acid metabolisms of humans (Suckling et al. 1991 , Woolett et al. 1989 ).

Gallbladder cholesterol is normally dissolved in bile by the solubilization properties of bile acids and phospholipids. Biliary solubility of cholesterol depends on its concentrations relative to the molar concentrations of bile acids and phospholipids. Cholesterol supersaturation is necessary for gallstone formation. The mechanisms of gallstone formation seem to be associated with an elevation in biliary cholesterol (Robins et al. 1973 , Wheeler 1973 ). Diets occasionally affect bile composition and the proportion of bile acids (Khallow et al. 1991 ). Kritchevsky and Klurfeld (1979) reported that soy protein reduced gallstone formation in hamsters. Some dietary fibers also suppress gallstone formation by modulating cholesterol metabolism (Kritchvsky et al. 1984 , Rotstein et al. 1981 , Zhang et al. 1994 ). Although the mechanisms of these gallstone-preventive effects are not fully understood, these compounds had distinctive effects on bile acid and cholesterol metabolism. We compared the effects of BWP and SPI on the formation of cholesterol gallstones and the biliary composition in hamsters fed cholesterol-enriched diets.

	MATERIALS AND METHODS

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Materials.

A buckwheat protein product (BWP) was prepared from buckwheat flour according to the process described elsewhere (Kayashita et al. 1995 ). The composition of BWP was as follows (g/kg): water, 101; protein, 619; lipids, 113; and nonfiber carbohydrate, 113. Compositions of amino acids and lipids in BWP were described in our recent report (Kayashita et al. 1997 ). Compositions of amino acid in SPI and casein were also described elsewhere (Kayashita et al. 1995 ). Soybean protein isolate (SPI) and casein were purchased from Nissin Oil Manufacture (Tokyo, Japan) and oriental Yeast (Tokyo, Japan), respectively.

Animals and diets.

Male Golden Syrian hamsters weighing 63–83 g were purchased from Japan SLC (Shizuoka, Japan). Hamsters were cared for in accordance with guidelines established by the Japanese Society of Nutrition and Food Science. The hamsters were housed individually in an air-conditioned room (22–24°C with a 12-h light cycle); they had free access to the experimental diets and deionized water. The hamsters were divided into three groups of eight. The diets (Table 1 ) were prepared according to the recommendations of the AIN (1977) . The dietary fat level was adjusted to 100 g/kg by adding corn oil. Cholesterol was added to the experimental diets at 5 g/kg (Fornal et al. 1981 ). The hamsters were fed these diets for 2 wk. After the experimental period, food was removed from the cages at 0800 h. Blood samples were collected from the abdominal vena cava in hamsters under anesthesia with diethyl ether (1300–1500 h). Plasma was isolated by centrifugation at low speed (3000 x g for 10 min). The bile was collected rapidly from gallbladder, and the liver was then excised and weighed. Feces were collected for the final 3 d of the experimental period.

Plasma concentrations of total cholesterol, HDL cholesterol, triglyceride and phospholipids were measured using enzymatic kits (Total cholesterol C-Test Wako, Triglyceride G-Test Wako and Phospholipid-B Test Wako, respectively; Wako Pure Chemical, Osaka, Japan) as described elsewhere (Kayashita et al. 1997 ). Hepatic lipids were extracted as described by Folch et al. (1957) . Total cholesterol, triglyceride and phospholipids in liver lipid were measured using the kits described above.

Analysis of biliary lipid.

Biliary cholesterol and phospholipids were measured by commercial kits described above. Total bile acids were assayed using enzymatic kits (Enzabile-2, Daiichi Pure Chemicals, Tokyo, Japan). Lithogenic index was calculated according to the method of Thomas and Hofmann (1973) . This index is determined by the ratio of the actual molar percentage of cholesterol in the sample to the molar percentage of cholesterol present at saturation. Briefly, the lithogenic index, a quantitative representation of cholesterol saturation, is defined as the ratio of the actual molar percentage of cholesterol in the bile sample to the molar percentage of cholesterol that is theoretically soluble, which is calculated as the ratio of phospholipids:phospholipids + bile acid (Thomas and Hofmann 1973 ).

Analysis of biliary bile acids.

The compositions of the biliary bile acids were measured by gas-liquid chromatography (GLC) according to the method of Kawamoto et al. (1978) . Three milliliters of 2.5 mol/L NaOH and 1.3 µmol of nor-deoxycholic acid (Steraloids, Wilton, NY) as the internal standard were added to 0.1 mL of bile sample. Hydrolysis of bile acids was carried out in an oven at 110°C for 18 h and then in an autoclave at 120°C for 1 h. After acidification of the solvent to ~pH 1, bile acids were extracted two times with 5 mL of diethyl ether. The extracted bile acids were methylated with trimethylsilyl-diazomethane (GL Sciences, Tokyo, Japan) for 18 h. This solution was then evaporated to dryness under nitrogen steam, and trimethylsilyl derivatives of bile acids were prepared by reaction with commercial derivatization reagents (GL Sciences). The GLC analyses were performed on a GL Sciences GC-380 instrument fitted with an autoinjector and a TC-1 column (30 m x 0.25 mm), which was first held at 250°C and then heated to 290°C.

Analysis of fecal steroid.

Fecal neutral steroids and bile acids were measured by GLC according to the method of Sugano et al. (1984) . Feces from individual hamsters of each group were dried and ground in a homogenizer. Neutral steroids were extracted with chloroform/methanol (2:1, v/v), and then analyzed as trimethylsilyl derivatives using an internal standard (5 -cholestan, Sigma Chemical, St. Louis, MO). The fecal bile acids were extracted two times with ethanol. Hydrolysis of bile acid was carried out as described above. Neutral steroids were extracted two times with 5 mL of diethyl ether before acidification of the solvent, and removed. Bile acids were then extracted and methylated in the same way, and analyzed as trimethylsilyl derivatives using the internal standard (nor-deoxycholic acid).

Statistical analysis.

Results were presented as means ± SEM. Statistical significance of the difference between values was analyzed by one-way ANOVA followed by Duncan’s multiple range test (Duncan 1957 ). Results were considered significant at P 0.05. Some data were subjected to regression analysis. The significance of differences in gallstone incidence was determined by Fisher’s exact test.

	RESULTS

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Body weight gain and food intake.

Gains in body weight in the SPI group (33 ± 2 g/2 wk) were significantly higher (P 0.05) than those in the casein (26 ± 1 g) and BWP groups (29 ± 1 g) (n = 8 for each group), but there was no difference between the casein and BWP groups. Food intake in the BWP group (146 ± 9 g/2 wk) was significantly higher than that in the casein (100 ± 6 g) and SPI groups (109 ± 9 g) (n = 8 for each group).

Concentrations of plasma and liver lipids.

Plasma total cholesterol concentration in the BWP group was significantly lower than those in the casein and SPI groups (Table 2 ). Compared with the casein group, the BWP and SPI groups had higher ratios of plasma HDL to total cholesterol (P 0.05). BWP intake reduced plasma concentration of phospholipids compared with the other groups (P 0.05). Plasma triglyceride concentration in the SPI and BWP groups was lower than that in the casein group (P 0.05). Liver cholesterol concentration in the BWP group was markedly lower than that in the casein group (P 0.05). There was no significant difference in plasma and liver cholesterol between the SPI and casein groups. Hepatic concentrations of triglyceride and phospholipids were unaffected by dietary manipulation.

Visible gallstones were clearly observed in all eight hamsters fed the casein diet, whereas two of seven hamsters fed the SPI diet (29%) had gallstones (compared with casein, P < 0.01). It was difficult to evaluate the gallstone formation in one of the eight hamsters fed SPI. None of the BWP-fed hamsters had gallstones (compared with casein, P < 0.01).

Biliary lipids.

The concentration and molar percentage of cholesterol in gallbladder bile were markedly lower in the BWP group than in the casein group (P 0.05). The molar percentage of bile acids was slightly elevated (27%) in the BWP group compared with the casein group (Table 3 , P 0.05). Compared with casein intake, SPI intake caused a lower concentration and molar percentage of cholesterol (P 0.05), but the effects were significantly less than those of BWP (P 0.05). The concentration and molar percentage of biliary phospholipids in the BWP group were significantly lower than in the casein group. The lithogenic index in the BWP group was significantly lower than in the casein group, and that in the SPI group was intermediate and different from the other two groups (P 0.05; Fig. 1 ).

View larger version (22K): [in this window] [in a new window]   Figure 1. Lithogenic index of hamsters fed casein, soy protein isolate (SPI) or a buckwheat protein product (BWP) for 2 wk. Values are means ± SEM (n = 8, except SPI, n = 7). Different superscript letters indicate different means, P 0.05. The lithogenic index was determined by the method of Thomas and Hofmann 1973 .

Concentrations of chenodeoxycholic acid (CDCA) and cholic acid (CA) in gallbladder bile were higher in the BWP group than in the casein group (P 0.05). There were no significant differences in the concentrations between the SPI and casein groups (Table 4 ). The proportion of biliary cholic acid relative to total bile acids (molar percentage) was markedly higher in the BWP and SPI groups than in the casein group (P 0.05). The ratio of CA to CDCA was significantly higher in the BWP and SPI groups than in the casein group.

Fecal dry weight was markedly higher in the BWP group than in the casein group (Table 5 , P 0.05). Although the SPI diet also elevated fecal weight compared with the casein diet (P 0.05), the effect was far less than that for the BWP diet. The BWP diet markedly enhanced fecal excretion of cholesterol and total neutral steroids compared with the casein diet (Table 5 , P 0.05). There were no differences in fecal cholesterol and total neutral steroids between the SPI and casein groups. Excretion of coprostanol and cholestanol (microbial metabolites of cholesterol) did not differ between the casein and BWP groups. Excretion of cholestanol in the SPI group was significantly higher than in the BWP and casein groups.

	DISCUSSION

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This study demonstrated for the first time that the BWP diet markedly suppressed gallstone formation and reduced the concentration of cholesterol in gallbladder, plasma and liver of hamsters compared with the casein diet. These effects of BWP were far stronger than those of SPI. The results for the cholesterol status in BWP-fed hamsters were similar to the findings with BWP-fed rats (Kayashita et al. 1995 ). We found that the molar percentage of biliary cholesterol in the BWP group was significantly lower than that in the casein group, whereas that of total bile acids was higher, resulting in a lower lithogenic index. These results indicate that the suppressive effect on the gallstone formation by BWP is due to the alterations in biliary cholesterol and bile acids. Our results further indicated that BWP diet markedly elevated the excretion of total neutral steroids and bile acids compared with the casein diet. These effects were also more remarkable than those of SPI. These results suggest that the strong suppression of plasma and gallbladder cholesterol by BWP could be accounted for by its effects on fecal steroids. This study further demonstrated that the effects of BWP on the excretion of fecal bile acids and total neutral steroids were far stronger than those of SPI. Actually, there was no difference in the excretion of fecal cholesterol and total neutral steroids between the SPI group and the casein group, whereas those in the BWP group were markedly higher than those in the casein group; this is in agreement with the results of a previous study of rats (Kayashita et al. 1997 ). Taken together, these data suggest that the differences in the effects of BWP and SPI on cholesterol status and gallstone formation are due to differences in the effects of these proteins on fecal excretion of bile acids and total neutral steroids. In this study, the growth of hamsters fed BWP was less than that of hamsters fed SPI. This difference in growth, however, may not relate to the differences in the effects on the cholesterol status and gallstone formation because the body weight gain was not correlated with the plasma or biliary cholesterol.

We observed previously that consumption of BWP markedly elevated fecal excretion of total neutral steroids, but did not affect fecal excretion of bile acids in cholesterol-fed rats (Kayashita et al. 1997 ). However, this study with hamsters showed higher fecal excretion of both total neutral steroids and bile acids due to BWP intake. The reason of this difference of the effects of BWP on fecal bile acids in rats and hamsters is unknown at present.

BWP contains 11.3 g/100 g lipids, which contain a small amount of ß-sitosterol (0.2 g/kg BWP lipid), as a minor component. To examine the influence of BWP lipids on plasma and liver cholesterol, BWP lipids were extracted from BWP and added to the diet in our previous study (Kayashita et al. 1997 ). There was no influence of the BWP lipids on plasma and liver cholesterol in rats compared with corn oil. Thus, it seems unlikely that the BWP lipids and the plant steroids in BWP are responsible for its hypocholesterolemic activity. BWP also contains a small amount of carbohydrate (for the most part, starch), 11.3 g/100 g. In our recent study, the influence of buckwheat starch, which was extracted from buckwheat flour, on plasma and liver cholesterol was also examined in rats (Tomotake, Kayashita and Kato, unpublished data). There was no hypocholesterolemic effect of the buckwheat starch in rats compared with cornstarch.

Hamsters have more similarities with human cholesterol and bile acid metabolism than rats (Balmir et al. 1996 , Suckling et al. 1991 , Woolett et al. 1989 ). In fact, soy protein intake suppresses plasma cholesterol in both hamsters (Tepstra et al. 1991 ) and humans (Meinertz et al. 1989 , Sirtori et al. 1977 ). Therefore, we speculate that the suppressive effects of BWP on gallstone formation and plasma cholesterol might be observed in humans as well as hamsters, and that these effects might also be stronger than those of SPI in humans.

De Schrijver (1990) reported that rats fed plant proteins excreted significantly more steroids than those fed a casein diet. Kritchevsky and Klurfeld (1983) found that both the percentage of hamsters with gallstones and the lithogenic index were reduced with the replacement of casein by soy protein. They suggested further that hamsters fed soy protein might have a higher turnover of endogenous cholesterol. However, the mechanism by which soy protein suppresses gallstone formation has not been elucidated fully. Our results suggest that higher fecal excretion of bile acids due to SPI is responsible for its lowering effects on gallstone formation and gallbladder cholesterol. Our results with hamsters were similar to those with rabbits and rats, indicating that soy protein impaired bile acid reabsorption, resulting in elevated bile acid excretion (Huff and Carroll 1980 , Nagata et al. 1982 ).

The gallstone-preventive effects of both soluble and insoluble fibers have been demonstrated in hamsters (Kritchevsky et al. 1984 , Rotstein et al. 1981 ). In general, dietary fibers inhibit intestinal absorption of bile acids and neutral steroid, leading to hypocholesterolemic action. In this respect, BWP seems to exert an effect similar to that of dietary fiber. Our recent study with rats demonstrated that the low digestibility of BWP was related to its cholesterol-lowering effect (Kayashita et al. 1997 ). From these data, we postulated that BWP possesses a dietary fiber–like property. It has been reported that hydrophobic bile acids such as CDCA and DCA caused greater inhibition of bile acid synthesis than hydrophilic bile acids in rats (Heuman et al. 1989 ). Trautwein et al. (1999) also showed that psyllium caused an alteration in the bile acid profile of gallbladder bile, particularly the reduction in CDCA and the elevation in CA, resulting in a high ratio of CA to CDCA. Further, it has been demonstrated that pectin- or psyllium-supplemented diets enhance individual and total bile acid pool sizes more than a cellulose-supplemented diet (Matheson and Story 1994 ). These findings suggest that the stimulation of hepatic bile acid synthesis is one of the mechanisms by which soluble fibers such as pectin and psyllium suppress gallstone formation. Our results further indicated that BWP and SPI elevated the ratio of CA to CDCA in bile and caused higher fecal excretion of total bile acids. We speculate that BWP and SPI suppress gallstone formation by the up-regulation of bile acid synthesis and higher fecal excretion of steroids.

Sugano et al. (1990) reported that the undigested insoluble peptide from SPI, having binding capacity with bile acids, enhanced fecal excretion of acidic steroids and had a hypocholesterolemic effect in rats fed cholesterol-enriched diets. Our recent study with rats suggested that lower digestibility of BWP is at least partially responsible for the suppressive effect on plasma cholesterol and the enhancing effect on fecal excretion of steroids (Kayashita et al. 1997 ). This study with hamsters also showed higher fecal dry weight due to BWP intake, possibly because of its lower digestibility. The alteration in fecal dry weight due to BWP was correlated inversely with that in plasma cholesterol and positively with that in fecal steroids (Table 5) . These results suggest that undigested BWP fraction or lower digestibility of BWP may relate to higher fecal steroids and to lower plasma cholesterol as reported in rats (Kayashita et al. 1997 ).

In conclusion, this study with hamsters demonstrated that BWP has strong gallstone-preventive and cholesterol-lowering activities in plasma and gallbladder. Our study further suggests that these effects of BWP are mediated by enhancing bile acid synthesis and fecal excretion of neutral and acidic steroids. BWP might be useful for the treatment of both hypercholesterolemia and gallstone formation. Because BWP contains higher amounts of amino acids such as arginine and glycine than do casein and SPI (Kayashita et al. 1995 and 1997 ), further study is required to examine whether these components relate to the effects of BWP.

	ACKNOWLEDGMENTS

 
We thank D. L. Topping for helpful comments and suggestions during the preparation of this manuscript.

	FOOTNOTES

 
² Abbreviations used: BWP, buckwheat protein product; CA, cholic acid; CDCA, chenodeoxycholic acid; DCA, deoxycholic acid; GLC, gas-liquid chromatography; SPI, soy protein isolate.

Manuscript received October 18, 1999. Initial review completed December 13, 1999. Revision accepted March 6, 2000.

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