Dietary Pectin: Effect on Metabolic Processes in Rats - American

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Dietary Pectin: Effect on Metabolic Processes in Rats MEI L I N G W. C H A N G U.S. Department of Agriculture, Agricultural Research Service, Beltsville Human Nutrition Research Center, Carbohydrate Nutrition Laboratory, Beltsville, M D 20705

Dietary pectin affects l i p i d metabolism, especially that of cholesterol. One of the explanations proposed to explain an action of pectin on cholesterol metabolism is through its a b i l i t y to bind b i l e acids and bile salts. However, pectin also has the property of forming a gel in water. This gel lowers the intestinal absorption of cholesterol and thereby decreases liver cholesterol. Recently, evidence has been obtained that the presence of pectin in a cholesterol diet increases the excretion of cholesterol esters. Results from the administration of cholesterol-4- C in the diet showed that the presence of pectin slows gastric emptying and results in more labeled cholesterol as well as cholesterol esters in a l l segments of the gut. These observations indicate that the higher levels of cholesterol esters were mainly exogenous. The functional role of pectin can be influenced by many factors such as its degree of esterification, its chain length and also the quantity and quality of other dietary ingredients. The effect of pectin on lowering of l i v e r cholesterol in rats receiving diets containing corn o i l or lard with or without cholesterol was greater with lard-pectin than with corn o i l - p e c t i n . The excretion of fecal free fatty acids was markedly greater; among them oleic acid was the highest in rats fed the pectin as compared to the pectin-free diet. Pectin also affects carbohydrate metabolism, reducing the postprandial rise in blood glucose and serum insulin. These effects of pectin could be beneficial in reducing risk factors associated with heart disease and diabetes. 14

This chapter not subject to U.S. copyright. Published 1983, American Chemical Society

Furda; Unconventional Sources of Dietary Fiber ACS Symposium Series; American Chemical Society: Washington, DC, 1983.

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Metabolic processes a f f e c t e d by d i e t a r y p e c t i n have been recognized f o r more than 2 decades. E f f e c t s of d i e t a r y p e c t i n on l i p i d and carbohydrate metabolism are important and b e n e f i c i a l to our h e a l t h . P e c t i n lowers serum c h o l e s t e r o l i n humans (j_-6) and serum and l i v e r c h o l e s t e r o l i n r a t s (7_, 8) as well as i n many other species (9-13). The i n g e s t i o n of c h o l e s t e r o l increases serum c h o l e s t e r o l l e v e l s (14, 15). A high l e v e l o f serum c h o l e s t e r o l i s g e n e r a l l y considered a r i s k f a c t o r associated with coronary heart disease (16, 17). The c h o l e s t e r o l - l o w e r i n g property of d i e t a r y p e c t i n would thus be expected to reduce the incidence o f heart problems. One of the e a r l y studies on the e f f e c t of d i e t a r y p e c t i n on c h o l e s t e r o l metabolism i n r a t s was c a r r i e d out by L i n et a l . (18). They found that more c h o l e s t e r o l was excreted i n r a t s fed a c h o l e s t e r o l d i e t containing p e c t i n than i n r a t s fed a c o n t r o l d i e t and suggested that p e c t i n i n h i b i t e d exogenous c h o l e s t e r o l absorpt i o n . L a t e r , Hyun et a l . (19), by using a cannulated t h o r a c i c duct technique with r a t s , measured the q u a n t i t a t i v e absorption o f c h o l e s t e r o l - 4 - 4 c from t e s t emulsions i n the i n t e s t i n e and observed that the absorption o f l a b e l e d c h o l e s t e r o l was s i g n i f i c a n t l y depressed by the presence o f p e c t i n i n the emulsion and the lowering was due p r i m a r i l y to a decrease i n e s t e r i f i e d cholest e r o l . T h i s f i n d i n g supported the e a r l y r e s u l t s (18). However, the mechanism involved i n the a c t i o n o f p e c t i n on i n h i b i t i n g c h o l e s t e r o l absorption i s not c l e a r at t h i s time. Many i n v e s t i g a t o r s have reported that d i e t a r y p e c t i n increased f e c a l e x c r e t i o n of b i l e acids as well as n e u t r a l s t e r o l (8^, 20) . The hypocholesterolemic p r o p e r t i e s o f p e c t i n may be due to i t s a b i l i t y to bind b i l e acids (21-24). L e v e i l l e and Sauberl i c h (21) , using everted i n t e s t i n a l sacs from the r a t , reported that p e c t i n depressed taurocholate absorption. They suggested that a p o s s i b l e mechanism f o r the hypolipemic a c t i o n o f p e c t i n involved the binding of b i l e s a l t s or b i l e acids which would r e s u l t i n reduced absorption o f c h o l e s t e r o l and i n t u r n i n lower serum c h o l e s t e r o l l e v e l s . In a d d i t i o n , the binding o f b i l e acids and an increased b i l e a c i d e x c r e t i o n would increase turnover o f c h o l e s t e r o l into b i l e acids and provide l e s s c h o l e s t e r o l to the c i r c u l a t i o n (24). Jenkins (25) p o s t u l a t e d that gums and viscous f i b e r s may reduce serum c h o l e s t e r o l by mechanisms other than simply i n c r e a s i n g l o s s o f b i l e s a l t . In our laboratory, we have observed that p e c t i n increased c h o l e s t e r o l ester e x c r e t i o n i n r a t s fed a c h o l e s t e r o l - c o n t a i n i n g d i e t (26). An e a r l y report (27) i n d i c a t e d that f e c a l excretion o f endogenous c h o l e s t e r o l ester could be i n f l u e n c e d by the type o f f a t . Polyunsaturated f a t (corn o i l ) as compared with saturated f a t (lard) a c c e l e r a t e d c h o l e s t e r o l e s t e r , but not t o t a l cholest e r o l excretion (27). I t was suggested t h a t , under c e r t a i n circumstances, c h o l e s t e r o l ester e x c r e t i o n was one o f the major pathways of c h o l e s t e r o l catabolism and a process f o r lowering body c h o l e s t e r o l and might e x p l a i n why corn o i l lowers serum 1

Furda; Unconventional Sources of Dietary Fiber ACS Symposium Series; American Chemical Society: Washington, DC, 1983.

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cholesterol level. P e c t i n as well as corn o i l i s considered to be an hypocholesterolemic agent. Recently, we have c a r r i e d out a study with young r a t s to e l u c i d a t e how p e c t i n a f f e c t s c h o l e s t e r o l ester excretion. C h o l e s t e r o l - 4 - ^ C was used as a t r a c e r i n the d i e t during the l a s t meals f o l l o w i n g 3-week feeding of unlabeled d i e t s . The d i e t contained 0.5% c h o l e s t e r o l , 10% corn o i l , e i t h e r with 5% p e c t i n or 5% c e l l u l o s e ( c o n t r o l d i e t ) . Rats were k i l l e d 4 hours a f t e r the l a s t 2-hour meal feeding. The general status o f the experimental r a t s i s shown i n Table I. The food intake i n the l a s t feeding was s l i g h t l y more i n the p e c t i n group than i n the c e l l u l o s e group. The percent of the consumed 14c-cholesterol which passed from the stomach into the i n t e s t i n e was 28.6 and 34.8 i n the p e c t i n and c e l l u l o s e groups, r e s p e c t i v e l y (Table I I ) , and the actual amount was 63.0 mg i n the p e c t i n group and 65.3 mg i n the c e l l u l o s e group. Thus, the d i f f e r e n c e of c h o l e s t e r o l l e v e l s i n the contents of i n t e s t i n a l sections between d i e t groups was not a t t r i b u t e d to the intake. The low percentage o f c h o l e s t e r o l that passed into the i n t e s t i n e i n p e c t i n - f e d r a t s at t h i s p e r i o d i s c o n s i s t e n t with the reports that p e c t i n delays the g a s t r i c emptying r a t e (28). The contents found i n the duodenum and jejunum were very small. Therefore, the samples from the same d i e t group were pooled. A l l data were from pooled samples. The ingested l a b e l e d c h o l e s t e r o l , both f r e e and e s t e r i f i e d , r e t a i n e d i n the duodenum, jejunum, ileum, and cecum (Table II) was higher i n p e c t i n - f e d than i n c e l l u l o s e - f e d r a t s . S i m i l a r l y , the nonl a b e l e d t o t a l c h o l e s t e r o l e s t e r s i n these sections was also higher i n the p e c t i n - f e d than i n the c e l l u l o s e - f e d r a t s . The r e s u l t s 1

Table I General Status of Experimental Rats

Cellulose diet

Body weight, g Initial Final L i v e r s i z e , g/100 g body weight Food intake, g ( l a s t meal) T o t a l labeled c h o l e s t e r o l intake, mg/rat Serum c h o l e s t e r o l , mg/100 ml Serum glucose, mg/100 ml Fecal e s t e r i f i e d c h o l e s t e r o l , g / g (pooled sample) Fecal n e u t r a l c h o l e s t e r o l ( f r e e ) , g / g (pooled sample) m

m

160 249 4.15 9.38

+ 4 + 5 + 0.10 + 0.55

46.9 256 166

+ 2.8 + 14 + 6

Pectin diet

159 243 4.08 10.99

+ + + +

3 4 0.47 0.47

50.0 235 144

+ + +

2.3 14 9

0,.66 32.0

Furda; Unconventional Sources of Dietary Fiber ACS Symposium Series; American Chemical Society: Washington, DC, 1983.

13.5 50.0

Furda; Unconventional Sources of Dietary Fiber ACS Symposium Series; American Chemical Society: Washington, DC, 1983.

26.219

3.714

1.709

1.744

7.88

18.05

0.147

0.26

4

4

1.76

0.49

1.18

103.548

75.84

25.38

14.806

cecum

6.151

1.573 5.997 24.366

43.216

4.108 7.876 17.700

0.06 0.41

0.839

1.464

0.07

0.149

1 4

0.784

0.311

0.864

0.02

63.0 (28.6%)

156.9 (71.4%)

219.9

1

P e c t i n d i e t - c h o l e s t e r o l content,* mg Total C Total C-esterified cholesterol esterified cholesterol

* A l l values are o f pooled groups o f 4 r a t s . * * One r a t i n c e l l u l o s e d i e t group had l i t t l e content, which might have passed i n t o colon or as f e c e s .

T o t a l (from duodenum to cecum) 62.38

49.64

0.63

Jejunum

Cecum**

0.029

0.26

Duodenum

11.85

65.3 (34.8%)

Stomach emptying

Ileum

122.3 (65.2%)

Stomach retained

0.114

187.6

4

Consumed

1

C e l l u l o s e d i e t - c h o l e s t e r o l content,* mg Total CTotal l C-esterified cholesterol esterified cholesterol

4

Table II C h o l e s t e r o l Contents o f Rat D i g e s t i v e T r a c t Segments 4 Hours A f t e r a 2-Hour-Meal-Feeding o f a C h o l e s t e r o l - 4 - * C D i e t Containing E i t h e r C e l l u l o s e or P e c t i n

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147

Dietary Pectin

provided p o s i t i v e evidence supporting the contention that p e c t i n lowers c h o l e s t e r o l absorption and that c h o l e s t e r o l ester i s one o f the f r a c t i o n s i n v o l v e d . The o r i g i n o f l a b e l e d c h o l e s t e r o l e s t e r s i n the lumen was not c l e a r , s i n c e l a b e l e d c h o l e s t e r o l i n the d i e t was i n the f r e e form. The conditions i n the lumen g e n e r a l l y favor h y d r o l y s i s o f c h o l e s t e r o l e s t e r s and there i s l i t t l e , i f any, i n t r a l u m i n a l e s t e r i f i c a t i o n (29). S t e r o l e s t e r hydrolase (cholest e r o l esterase, EC 3.1.1.13) systems are pH-dependent. The optimal pH f o r h y d r o l y s i s i s 6.7 and f o r e s t e r i f i c a t i o n i s 6.2 (30). Therefore, a p o s s i b l e explanation f o r the presence o f l a b e l e d c h o l e s t e r o l esters i n the i n t e s t i n a l lumen was due t o a pH environment f a v o r i n g s y n t h e s i s . The gel-forming property o f p e c t i n might maintain a more a c i d i c pH o f the chyme as i t leaves the stomach and enters the upper part o f the proximal i n t e s t i n e , thus f a v o r i n g c h o l e s t e r o l e s t e r s y n t h e s i s . Cholesterol esters cannot be d i r e c t l y absorbed by the mucosal c e l l (29). The source o f the nonlabeled c h o l e s t e r o l e s t e r i n the lumen could not be determined under present experimental c o n d i t i o n s . The present data showed that c h o l e s t e r o l e s t e r s were mainly i n the i l e a l s e c t i o n o f the small i n t e s t i n e . This could be due t o the unabsorbed c h o l e s t e r o l from the upper proximal region passing down t o the ileum where the absorption o f c h o l e s t e r o l i s l e s s e f f i c i e n t (31_, 32). The p r o f i l e o f f a t t y acids i n c h o l e s t e r o l esters showed a d i f f e r e n c e between the two d i e t groups (Table III) . The high l e v e l s o f palmitate and stéarate esters presumably o r i g i n a t e d from the d i e t a r y f a t . Since the absorption o f palmitate and stéarate i s low, more o f these f a t t y acids were a v a i l a b l e i n the i n t e s t i n e f o r e s t e r i f i c a t i o n . The percentage o f o l e a t e was three times greater i n the c e l l u l o s e - d i e t group than i n the p e c t i n - d i e t group.

The

Table I I I P r o f i l e o f F a t t y A c i d E s t e r s i n the C r y s t a l l i z e d Fecal Cholesterol Esters Diet Cellulose

Pectin

30 32 6 23 8

43 19 21 7 4 2

Fatty acids, % Palmitate Stéarate Transoctadecenate Oleate Linoleate Arachidate

American Chemlctf Society Library 1155 16th St. N. W. Furda; Unconventional Sources Fiber D. C.of Dietary 2003fi ACS Symposium Series; American Chemical Society: Washington, DC, 1983.

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It i s p o s s i b l e that the source (endogenous versus endogenous + exogenous) of the esters may be r e s p o n s i b l e f o r the d i f f e r e n c e . I t has been reported that o l e i c a c i d i s most r e a d i l y e s t e r i f i e d with c h o l e s t e r o l during i t s absorption (33, 34). Furthermore, Swell and Treadwell (34) a l s o reported that the c h o l e s t e r o l e s t e r which accumulated to the greatest extent, i r r e s p e c t i v e of the f a t t y a c i d fed, was c h o l e s t e r o l o l e a t e . Thus, the endogenous c h o l e s t e r o l e s t e r s may be r i c h i n o l e i c a c i d . The r e s u l t s obtained i n d i c a t e that d i e t a r y p e c t i n i n f l u e n c e d the synthesis o f c h o l e s t e r o l esters i n the i n t e s t i n a l lumen, thereby p r o v i d i n g a p o s s i b l e mechanism by which p e c t i n can i n f l u e n c e c h o l e s t e r o l metabolism. The e f f e c t i v e n e s s o f p e c t i n i n lowering c h o l e s t e r o l i n t i s s u e s can be i n f l u e n c e d by many f a c t o r s : (1) The type o f pec­ t i n - that with methoxy groups and with high v i s c o s i t y (35_, 36) was reported to be more e f f e c t i v e . The r e s u l t s from a comparative study o f several types of p e c t i n by Mokady (36) are shown i n Table IV. N e i t h e r a high degree o f methylation nor h i g h - v i s c o s i t y alone was very e f f e c t i v e ; (2) the l e v e l o f d i e t a r y f a t - with a h i g h - f a t d i e t (2% corn o i l plus 18% beef t a l l o w ) , p e c t i n has no e f f e c t on serum c h o l e s t e r o l l e v e l (37). T s a i et a l . also reported that with

Table IV* Degree o f Methylation and R e l a t i v e V i s c o s i t y o f Test Substances and Comparison of Blood C h o l e s t e r o l with E x c r e t i o n o f L i p i d s i n the Feces Degree o f methylation

Relative viscosity

(%) Control Pectin Pectin Pectin Pectin Pectin Algin

1 2 3 S MR

7.8 8.2 4.1 7.7 7.8

2.9 6.0 23.5 2.4 2.6 10.2

T o t a l blood cholesterol

(mg 87 79 66 75 72 72 77

+ + + + + + +

%)

Fecal lipids

1

(g/rat) 2

5.2 5.2 2.8"* 3.0 2.8 2.8 3.2

0.272 1.245 2.000 1.060 1.503 1.300 1.367

Total fecal sterols (mg/rat) 30.4 84.6 113.3 67.6 82.0 89.0 38.0

Pooled mean value o f 8 animals f o r the e n t i r e p e r i o d o f 12 days. 2 Mean f o r 8 animals _+ SE. 3

Ρ