Pectins and Guar Gum: Effect on Plasma Lipoproteins and Tissue

7 Pectins and Guar Gum: Effect on Plasma Lipoproteins and Tissue Lipoprotein Lipase Activity in Rats N.-G ASP—University of Lund, Chemical Center, Department of Food Chemistry, S-220 07 Lund, Sweden H. G. BAUER—University of Lund, Department of Surgery, S-220 07 Lund, Sweden P. NILSSON-EHLE—University of Lund, Department of Clinical Chemistry, S-220 07 Lund, Sweden R.ÖSTE—Universityof Lund, Chemical Center, Department of Nutrition, S-220 07 Lund, Sweden Various dietary fiber supplementations were given to rats fed semisynthetic diets with 20% casein and 20% peanut o i l for 3-6 months. When added to cholesterol free diets, 5% guar gum slightly decreased total plasma and HDL cholesterol, whereas 5% low or high methoxylated pectin had no significant effect or a slightly elevating effect. When 0.5% cholesterol was included in the diets, 5% pectin decreased total cholesterol and increased HDL cholesterol, thus increasing substantially the relative HDL concentration. Wheat bran increased total and HDL cholesterol, and there seemed to be a dose-response relationship. Differences in plasma triglycerides were generally insignificant. Lipoprotein lipase activity was slightly elevated in heart tissue after feeding wheat bran and slightly lowered in adipose tissue after feeding high methoxylated pectin. Dietary fiber might be a factor protecting against atherosclerotic disease (1). This hypothesis is based on epidemiological data linking a large number of "Western" diseases with a low intake of dietary fiber (2). It has got experimental support, however in that certain types of dietary fiber might alter plasma lipoprotein concentrations. The relationship between the plasma lipoprotein profile and c l i n i c a l appearance of atherosclerotic heart disease is now well established. During the latest decade increased interest has focused on the differential effect of various lipoprotein classes; specifically the protective function of high-density lipoproteins 0097-6156/83/0214-0093$06.00/0 © 1983 American Chemical Society

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UNCONVENTIONAL SOURCES OF DIETARY FIBER

(HDL) against a t h e r o s c l e r o s i s has been f i r m l y e s t a b l i s h e d ( 3 ) , whereas increased l e v e l s of low-density l i p o p r o t e i n s (LDL) are regarded as a major r i s k f a c t o r f o r c a r d i o v a s c u l a r d i s e a s e . E f f e c t s of d i e t a r y f i b e r on plasma l i p i d s have been most pronounced and most c o n s i s t e n t i n studies using p u r i f i e d , viscous types of f i b e r , such as p e c t i n and guar gum. The decrease i n t o t a l and LDL c h o l e s t e r o l when feeding these f i b e r s i s accompanied by an increased f e c a l b i l e - a c i d e x c r e t i o n . Increased b i l e - a c i d l o s s with increased de novo synthesis from c h o l e s t e r o l i s u s u a l l y considered the main mechanism by which d i e t a r y f i b e r may a l t e r plasma c h o l e s t e r o l . However, decreased absorption of d i e t a r y c h o l e s t e r o l or a l t e r e d c h o l e s t e r o l and l i p o p r o t e i n metabolism by other mechanisms may a l s o be important (for review see f o r instance 4 ) . Wheat bran binds b i l e - a c i d s i n v i t r o (5) but i n v i v o e f f e c t s on plasma c h o l e s t e r o l have been almost uniformly negative (6). Some studies on small groups of humans ( 7 , 8 ) , however, i n d i c a t e that bran might increase HDL c h o l e s t e r o l , although unchanged (9) or even decreased (10) l e v e l s have a l s o been r e p o r t e d . Colon cancer i s the form of cancer most s t r o n g l y l i n k e d to d i e t a r y f a c t o r s , e s p e c i a l l y f a t and f i b e r . I t i s suggested that the b u l k i n g e f f e c t of d i e t a r y f i b e r would d i l u t e carcinogens and diminish the time during which the c o l o n i c mucosa i s exposed to carcinogens ( V [ ) . Fibers, such as p e c t i n and guar gum, however, increase the flow of b i l e s a l t s to the l a r g e bowel and have poor b u l k i n g e f f e c t as they are r e a d i l y degraded by the i n t e s t i n a l m i c r o f l o r a . Since b i l e s a l t s and/or t h e i r m i c r o b i a l degradation products are cocarcinogens, t h i s complicates the d i e t a r y f i b e r / colon cancer hypothesis. Experiments with chemically induced colon cancer i n the r a t have p a r t i a l l y , but not c o n s i s t e n t l y , supported the d i e t a r y f i b e r hypothesis (12). Thus, Bauer et a l . (13,14) r e c e n t l y reported that both h i g h - and low-methoxylated p e c t i n (6.5 or 5% i n a d i e t c o n t a i n i n g 20% c a s e i n , 20% f a t and no other d i e t a r y f i b e r ) given during i n d u c t i o n of colon cancer with subcutaneous 1.2-dimethyl-^ h y d r a z i n e , enhanced the y i e l d of tumors. Guar gum, 5%, a l s o tended to increase the tumor y i e l d , although not s i g n i f i c a n t l y compared with c o n t r o l s on a v i r t u a l l y f i b e r - f r e e d i e t . Others(15) however reported a p r o t e c t i v e e f f e c t of 15% p e c t i n . With t h i s background, the present i n v e s t i g a t i o n was undertaken. The e f f e c t on plasma t o t a l and HDL c h o l e s t e r o l , and t r i g l y c e r i d e s of two kinds of p e c t i n with d i f f e r e n t degrees of methoxylation, and of guar gum was studied i n 3-6 months feeding experiments with r a t s . Wheat bran and oat bran were a l s o studied for comparison. P e c t i n and wheat bran was fed both with and without d i e t a r y c h o l e s t e r o l . To throw some l i g h t upon mechanisms by which d i e t a r y f i b e r could influence plasma l i p o p r o t e i n s , heart and adipose t i s s u e l i p o p r o t e i n l i p a s e a c t i v i t i e s were measured a f t e r feeding some of the d i e t a r y f i b e r c o n t a i n i n g d i e t s . This key enzyme i n l i p o p r o t e i n metabolism i s one of the most important f a c t o r s determining plasma t r i g l y c e r i d e and plasma HDL concentrations (16).

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M a t e r i a l s and Methods Animals. Male SPF Sprague-Dawley r a t s (Anticimex, Stockholm, Sweden), weighing approximately 135 g at the s t a r t of the e x p e r i ment, were used. They were kept i n d i v i d u a l l y i n s t e e l - w i r e cages with free access to water and were adapted to a 12 h l i g h t and dark s h i f t . The room was a i r - c o n d i t i o n e d , maintained at 23 and 5o-60% r e l a t i v e humidity. The d i f f e r e n t d i e t s were fed ad l i b , i n metal containers designed to give minimal l o s s e s . Diets. A b a s a l d i e t with 20% c a s e i n , 20% f a t , wheat s t a r c h as main carbohydrate source and proper amounts of vitamins and minerals was prepared as described e a r l i e r (17). The v a r i o u s d i e t a r y f i b e r containing d i e t s were prepared by s u b s t i t u t i n g d i e t a r y f i b e r preparations f o r wheat s t a r c h . A n a l y s i s of d i e t a r y f i b e r . Total dietary fiber including both water-soluble and w a t e r - i n s o l u b l e components was analysed with an enzymic method as described by Asp et a l . (18). The d i e tary f i b e r was c h a r a c t e r i z e d by g a s - l i q u i d chromatographic assay of monosaccharides a f t e r a c i d - h y d r o l y s i s and g r a v i m e t r i c d e t e r mination of a c i d i n s o l u b l e l i g n i n . Uronic acids were assayed with a decarboxylation method. These analyses were performed as described by Theander and Aman (19). A n a l y s i s of plasma l i p i d s . HDL was separated by s e l e c t i v e p r e c i p i t a t i o n of very-low-density l i p o p r o t e i n (VLDL) and lowdensity l i p o p r o t e i n (LDL) by dextran sulphate and manganese c h l o r i d e (20), and HDL c h o l e s t e r o l was measured by c h o l e s t e r o l determination of the c l e a r supernatant f r a c t i o n . C h o l e s t e r o l and t r i g l y c e r i d e s were analysed by enzymic procedures (21,22). Experiment 1. D i e t s containing 5% high-methoxylated (HM) p e c t i n , 5% low-methoxylated (LM) p e c t i n , 5% guar gum or 20% wheat bran (corresponding to about 10% bran f i b e r ) were fed f o r 6 months to r a t s (15 i n each group) and compared with the b a s a l d i e t . A f t e r 6, 12 and 26 weeks, 5 r a t s i n each group were k i l l e d after 16 hours f a s t i n g by carbon dioxide n a r c o s i s . Blood was withdrawn by c a r d i a c puncture (17). Experiment 2. In t h i s experiment the b a s a l d i e t , a 5% HMp e c t i n d i e t and a 10% wheat bran d i e t (corresponding to 5% bran f i b e r ) were fed to groups of 7 r a t s both with and without 0.5% d i e t a r y c h o l e s t e r o l . For comparison, 10% wheat bran and 10% oat bran d i e t s were a l s o studied (without c h o l e s t e r o l ) . Plasma l i p i d s were analysed as i n Experiment 1. L i p o p r o t e i n l i p a s e a c t i v i t i e s i n adipose t i s s u e and heart muscle was assayed with t r i ( H) o l e o y l g l y c e r o l emulsion as substrate (23). A c t i v i t i e s are expressed as nmol of f a t t y a c i d released per minute per mg protein. 3

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S t a t i s t i c a l e v a l u a t i o n . Student's t - t e s t (two-tailed) was used f o r weight of r a t s and food intake. D i f f e r e n c e s i n plasma l i p i d s , l i p o p r o t e i n s and l i p o p r o t e i n l i p a s e a c t i v i t i e s were evaluated with Wilcoxon's t e s t ( t w o - t a i l e d ) . Results and D i s c u s s i o n Experiment 1. The d i e t a r y f i b e r content and composition of the v a r i o u s d i e t a r y f i b e r preparations used have been reported e a r l i e r (17) . The HM and LM p e c t i n preparations had 74 and 37% r e s p e c t i v e l y of t h e i r carboxyl groups methoxylated. The uronic a c i d content was 80 and 86% r e s p e c t i v e l y (dry weight b a s i s ) . The content of n e u t r a l sugars, mainly galactose, was 6 and 4% r e s p e c t i v e l y . The guar/gum p r e p a r a t i o n contained 89% n e u t r a l sugars (dry weight b a s i s ) , mainly mannose and g a l a c t o s e . The wheat bran contained 52% d i e t a r y f i b e r (dry weight b a s i s ) with a t y p i c a l composition dominated by arabinoxylan and c e l l u l o s e . The a c i d i n s o l u b l e l i g n i n content was 5%. Figure 1 shows the growth curves i n the f i r s t experiment. The guar gum group (G) had s l i g h t l y slower weight development than the other groups. When the weight increase was c a l c u l a t e d per u n i t energy consumed, the guar gum group had a s i g n i f i c a n t l y lower v a l u e , i n s p i t e of an 8% increase i n the food i n t a k e . F e c a l losses could not e x p l a i n t h i s lower weight development since f e c a l dry weight increased only 0.3 g/day and most of t h i s increase can be expected to represent undegraded guar gum. I t i s i n t e r e s t i n g i n t h i s context to r e c a l l an i n v e s t i g a t i o n (24) showing uncoupling of o x i d a t i v e phosphorylation i n l i v e r and heart mitochondria of r a t s given small doses of gum a r a b i c , gum t r a g a canth or modified c e l l u l o s e s . T o t a l plasma c h o l e s t e r o l (Figure 2) was s i g n i f i c a n t l y lowered by guar gum a f t e r 12 weeks but the p e c t i n s d i d not s i g n i f i c a n t l y a l t e r the l e v e l . Wheat bran increased t o t a l c h o l e s t e r o l at a l l the time points studied (17). HDL c h o l e s t e r o l (Figure 3) was a l s o lowered by guar gum but increased by wheat bran. The r e l a t i v e HDL concentration (percent of t o t a l c h o l e s t e r o l ) was c l o s e to 0.7 i n a l l cases. Plasma t r i g l y c e r i d e s decreased with age but were s i m i l a r i n a l l groups. On g e l e l e c t r o p h o r e s i s , no chylomicrons were demonstrable, i n d i c a t i n g that plasma t r i g l y c e r i d e concentrations e s s e n t i a l l y corresponded to VLDL concentrations. Experiment 2. As i n the f i r s t experiment, weight development and food intake was s i m i l a r i n the d i f f e r e n t gorups. Figure 4 shows t o t a l plasma c h o l e s t e r o l a f t e r 3 months on the d i f f e r e n t d i e t s . In the groups not fed d i e t a r y c h o l e s t e r o l p e c t i n gave a s l i g h t but s i g n i f i c a n t plasma c h o l e s t e r o l i n c r e a s e . As i n Experiment 1, wheat bran a l s o increased the t o t a l c h o l e s t e r o l and there seemed to be a dose-response r e l a t i o n s h i p .

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Ο

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Figure 1. Growth curves of rats fed various dietary fiber containing diets. Key: · , HM pectin, 5%; Δ, LM pectin, 5%; A, guar gum, 5%; M, wheat bran, 20%, corresponding to 10% branfiber;and O, basal diet.

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Figure 2. Total plasma cholesterol after 6 (I), 12 (II), and 26 (III) weeks in rats given diets containing different dietary fibers. Key: Group B, basal diet; Group H, high-methoxyl pectin diet; Group L, low-methoxyl pectin diet; Group G, guar gum diet; Group WB, wheat bran diet; *, Ρ < 0.05; and **, Ρ < 0.01. Mean values are given with their standard errors represented by vertical bars. (Reproduced with permission from Ref. 17. Copyright 1981, British Journal of Nutrition.) 2.2

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Figure 3. High-density-lipoprotein cholesterol after 6 (I), 12 (II) and 26 (III) weeks in rats given diets containing different dietary fibers. Key is the same as in Figure 2. Mean values are given with their standard errors represented by vertical bars. (Reproduced with permission from Ref. 17. Copyright 1981, British Journal

of Nutrition.)

ASP ET AL.

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Figure 4. Total plasma cholesterol after 3 months in rats given diets containing different dietary fibers, without cholesterol (left) and with 0.5% cholesterol (right). Key: Group B, basal diet; group WB5 and WB10, wheat bran diets with 5 or 10% wheat bran fiber; Group OB, oat bran diet with 10% fiber; Group P, pectin diet with 5% high-methoxylated pectin; Group C, basal diet with 0.5% cholesterol; Group WB5C, wheat bran diet (5% fiber) with 0.5% cholesterol; Group PC, pectin diet, 5%, with 0.5% cholesterol; *, Ρ < 0.05; and **, Ρ < 0.01. Mean values are given with their standard errors indicated by vertical bars.


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When 0.5% c h o l e s t e r o l was added to the d i e t s , t o t a l c h o l e s t e r o l l e v e l s decreased s l i g h t l y whereas HDL c h o l e s t e r o l concentrations f e l l by about 30%. When added to the c h o l e s t e r o l containing d i e t , 5% p e c t i n s i g n i f i c a n t l y decreased the t o t a l plasma c h o l e s t e r o l and increased the HDL c h o l e s t e r o l l e v e l (Figure 5). Wheat bran increased HDL c h o l e s t e r o l both with and without d i e t a r y c h o l e s terol. These changes demonstrate that the r e l a t i v e HDL concentration i . e . HDL c h o l e s t e r o l as percent of t o t a l c h o l e s t e r o l , was s t r o n g l y decreased by d i e t a r y c h o l e s t e r o l despite the s l i g h t reduction of the t o t a l plasma c h o l e s t e r o l l e v e l s (Figure 4, 5 ) . Despite i t s lack of e f f e c t i n r a t s fed without c h o l e s t e r o l , p e c t i n could p a r t l y reverse the negative e f f e c t of d i e t a r y c h o l e s t e r o l on the Total/HDL c h o l e s t e r o l r a t i o . Wheat bran d i d not s i g n i f i c a n t l y change t h i s r a t i o since i t l e d to s i m i l a r e l e v a t i o n s i n both t o t a l and HDL c h o l e s t e r o l . Oat bran d i d not change plasma c h o l e s t e r o l l e v e l s . Others (25) have shown that oat bran decreases t o t a l plasma c h o l e s t e r o l and increases HDL i n c h o l e s t e r o l fed r a t s . The e f f e c t seems to be r e l a t e d to s o l u b l e oat gums. The lack of e f f e c t of oat bran i n our experiment might be due to the f a c t that we studied t h i s f i b e r only i n c h o l e s t e r o l - f r e e d i e t s . Soluble gums may a l s o have been l o s t i n preparing t h i s f i b e r enriched oat bran (81% d i e t a r y f i b e r ) . Plasma t r i g l y c e r i d e s were not a l t e r e d by p e c t i n but s i g n i f i c a n t l y lowered i n the wheat bran group with 5% bran f i b e r and i n the oat bran group. L i p o p r o t e i n l i p a s e a c t i v i t y i n heart t i s s u e was not a l t e r e d by p e c t i n but s l i g h t l y increased i n the wheat bran group. In a d i pose t i s s u e the a c t i v i t y was s i g n i f i c a n t l y lowered i n the group fed p e c t i n . General

Discussion

The e v a l u a t i o n of e f f e c t s of d i e t a r y c o n s t i t u e n t s on plasma l i p i d and l i p o p r o t e i n s requires s e l e c t i v e measurements of i n d i v i dual l i p o p r o t e i n c l a s s e s . For example, the a d d i t i o n of c h o l e s t e r o l to the d i e t i n the r a t does not increase t o t a l plasma c h o l e s t e r o l l e v e l s ; i n the present study a s l i g h t reduction i n plasma c h o l e s t e r o l was i n f a c t seen. However, the HDL c h o l e s t e r o l f r a c t i o n was markedly reduced, and the VLDL and/or LDL c h o l e s t e r o l l e v e l must therefore have been increased. E x t r a p o l a t i o n from data i n humans would i n d i c a t e that t h i s s h i f t i n l i p o p r o t e i n p r o f i l e i s disadvantageous from the atherogenic point of view. The increase i n VLDL/ LDL c h o l e s t e r o l may r e a d i l y be explained by the d i e t a r y load of c h o l e s t e r o l which i s transported to p e r i p h e r a l t i s s u e s by these l i p o p r o t e i n p a r t i c l e s (_16) . The reduction i n HDL which are considered to be involved i n c h o l e s t e r o l transport from p e r i p h e r a l t i s s u e s to the l i v e r , i s however an i n t e r e s t i n g but so f a r unexplained phenomenon.

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WB WB 5 10

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Figure 5. High-density lipoprotein cholesterol after 3 months in rats given diets containing different dietary fibers, without cholesterol (left) or with 0.5% cholesterol (right). Key is the same as in Figure 4.

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The e f f e c t s of d i e t a r y f i b e r on plasma l i p o p r o t e i n s are in some cases, s t r o n g l y a f f e c t e d by the presence of c h o l e s t e r o l i n the d i e t . This study confirms that d i e t a r y c h o l e s t e r o l i s essent i a l f o r the plasma c h o l e s t e r o l lowering e f f e c t of p e c t i n . In f a c t no such e f f e c t was obtained i n the absence of c h o l e s t e r o l i n our high p r o t e i n / h i g h f a t d i e t s , and the e f f e c t s of p e c t i n might be i n t e r p r e t e d as a p a r t i a l r e v e r s a l of the disadvantageous e f f e c t s of d i e t a r y c h o l e s t e r o l on the plasma l i p o p r o t e i n p r o f i l e . Interference with the reabsorption of b i l e s a l t s leading to increased f e c a l e x c r e t i o n and de novo synthesis from c h o l e s t e r o l i s g e n e r a l l y regarded to be the main mechanism by which p e c t i n and other types of viscous f i b e r a f f e c t plasma l i p i d concentrat i o n s . Some studies i n d i c a t e , however, that the presence of d i e t a r y c h o l e s t e r o l might be important (26,27). T h i s i s s t r o n g l y supported by our data. The mechanism mTght be r e l a t e d to d i s t u r b e d m i c e l l a r formation a f f e c t i n g i n t e s t i n a l c h o l e s t e r o l absorption. The h i g h l y s i g n i f i c a n t favourable e f f e c t of p e c t i n ( i n the c h o l e s t e r o l containing d i e t s ) on the HDL/total c h o l e s t e r o l r a t i o may be r e l a t e d to a l t e r e d endogenous c h o l e s t e r o l synthesis due to decreased absorption of d i e t a r y c h o l e s t e r o l . Several mechanisms are involved i n the r e g u l a t i o n of plasma HDL l e v e l s . Besides the r a t e of production of HDL i n the l i v e r and i n t e s t i n e and the rate of e l i m i n a t i o n i n p e r i p h e r a l t i s s u e s , the pattern of i n t r a v a s c u l a r metabolism i s a l s o important i n the s e t t i n g of HDL concentrations. LPL c a t a l y z e s the r a t e - l i m i t i n g step i n the l i p o l y t i c degradation of t r i g l y c e r i d e - r i c h l i p o p r o t e i n s ; since t h i s r e a c t i o n i s a l s o associated with a t r a n s f e r of amphipathic surface components (e.g. c h o l e s t e r o l , phospholipids and apoproteins) to the HDL p a r t i c l e s , a high LPL a c t i v i t y w i l l g e n e r a l l y be associated with high nlasma l e v e l s of HDL (16). The increase i n HDL and t o t a l c h o l e s t e r o l i n the group fed bran d i d not seem r e l a t e d to d i e t a r y c h o l e s t e r o l . The increase i n heart t i s s u e l i p o p r o t e i n l i p a s e a c t i v i t y i n d i c a t e s an increased p e r i p h e r a l e l i m i n a t i o n of t r i g l y c e r i d e s i n muscular t i s s u e which i s consistent with an e l e v a t i o n i n HDL c h o l e s t e r o l . This i n c r e a s e , however, i s small compared with changes i n l i p o p r o t e i n l i p a s e a c t i v i t y induced by f o r instance ethanol (28). I t i s therefore more probable that the e f f e c t of wheat bran on HDL c h o l e s t e r o l i s a l s o r e l a t e d to a l t e r e d r a t e or s i t e of l i p i d absorption i n the intestine. Acknowledgment s This work was supported by grants from Pâhlsson^s Foundation, Malmo, and the Swedish Medical Research C o u n c i l , p r o j e c t no B82-03X-04745-07 and B82-03X-04966-06.

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