Leguminous Seed Fiber - ACS Symposium Series (ACS Publications)

Leguminous Seed Fiber Uses in Disease States and Effects on Carbohydrate Digestion in Vitro and Absorption in Vivo THOMAS M. S. WOLEVER, DAVID J. A. JENKINS, ALEXANDRA L. JENKINS, M A R Y JANE THORNE, and LILIAN U. THOMPSON University of Toronto, Department of Nutritional Sciences, Toronto, Ontario, Canada RODNEY H. TAYLOR Downloaded by UNIV LAVAL on July 11, 2016 | http://pubs.acs.org Publication Date: April 11, 1983 | doi: 10.1021/bk-1983-0214.ch002

Central Middlesex Hospital, London, England The f i b e r hypothesis suggested that diabetes and heart disease are the r e s u l t , at l e a s t i n p a r t , of a lack of f i b e r i n the diet. This paper examines some of the recent evidence concerning the mechanism by which d i e t a r y f i b e r a f f e c t s carbohydrate metabolism, and how t h i s , i n turn, may be of use in the treatment of these d i s o r d e r s . I t is suggested that the r a t e of d i g e s t i o n and absorption of carbohydrate from the small i n t e s t i n e i s a major determinant of the p h y s i o l o g i c a l response t o a food. Both the r a t e of d i f f u s i o n of glucose i n vitro from g l u c o s e / f i b e r mixtures, and the r a t e o f i n vitro d i g e s t i o n of foods, are p r o p o r t i o n a l t o the in v i v o blood glucose responses seen a f t e r feeding the f i b e r s o r the foods. In t h i s context d i e t a r y f i b e r d e r i v e d from leguminous seeds, taken e i t h e r p u r i f i e d , o r in its n a t u r a l s t a t e (i.e. e a t i n g the bean itself) has been shown t o be most e f f e c t i v e i n reducing blood glucose and serum lipid c o n c e n t r a t i o n s . This s t r o n g l y supports the increased consumption of beans for h e a l t h reasons. Current i n t e r e s t i n d i e t a r y f i b e r began about ten years ago when B u r k i t t and Trowel1 hypothesized that diabetes and heart disease were f i b e r d e f i c i e n c y d i s o r d e r s (1). Since then there has been i n c r e a s i n g research on the e f f e c t s o f d i e t a r y f i b e r on carbohydrate and l i p i d metabolism. Such work was pioneered and stimulated i n large part by Dr. J . Anderson of Lexington, Kentucky who f i r s t used high carbohydrate/high f i b e r d i e t s t o t r e a t diabetes (2^) and Dr. D. Kritchevsky who has examined the e f f e c t s o f f i b e r on the metabolism of c h o l e s t e r o l 03)· Our own i n t e r e s t i n d i e t a r y f i b e r was stimulated by the o r i g i n a l l y suggested mechanism by which p r i m i t i v e d i e t s a f f e c t carbohydrate metabolism. According t o the hypothesis, the

0097-6156/83/0214-0017$06.00/0 © 1983 American Chemical Society

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

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f i b e r - r i c h energy d i l u t e p r i m i t i v e d i e t t r a v e l l e d the f u l l length of the small i n t e s t i n e r e l e a s i n g i t s products of d i g e s t i o n slowly ( F i g . l a ) . By c o n t r a s t , the r e f i n e d Western d i e t was seen to be r a p i d l y absorbed i n the upper small i n t e s t i n e ( F i g . l b ) . The consequences of a f i b e r - r i c h meal, i t was supposed, would be a slow, prolonged and r e l a t i v e l y small r i s e i n the blood glucose l e v e l , compared with a r a p i d r i s e a f t e r a r e f i n e d , f i b e r depleted meal ( F i g . 2 ) .

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E f f e c t of Leguminous F i b e r on Gut Physiology To see whether f i b e r might slow the a b s o r p t i o n of m a t e r i a l from the i n t e s t i n e we used a simple d i a l y s i s model. S o l u t i o n s o f glucose were placed i n s i d e semipermeable d i a l y s i s bags with and without the a d d i t i o n of equal amounts of d i f f e r e n t types of d i e t a r y f i b e r ; wheat bran, p e c t i n , methyl c e l l u l o s e , gum tragacanth and guar gum. Compared with the f i b e r - f r e e c o n t r o l , a l l types of f i b e r produced some impedance to the outward passage of glucose, but the most e f f e c t i v e were the most v i s c o u s substances guar and tragacanth. When these same f i v e f i b e r preparations were added i n 12 g d i e t a r y f i b e r equivalents to 50 g o r a l GTT taken by normal volunteers there was a f l a t t e n i n g of both the glucose and i n s u l i n responses ( 4 ) . Again guar and tragacanth, the most viscous m a t e r i a l s , were the most e f f e c t i v e . The question obviously arose as to whether the f l a t t e r blood glucose responses a f t e r guar were the r e s u l t of malabsorption of glucose caused by a much reduced r a t e of a b s o r p t i o n . However s t u d i e s using u r i n a r y xylose e x c r e t i o n as a measure of carbohydrate absorption suggested that a f t e r a guar c o n t a i n i n g GTT there was delayed but complete absorption of the carbohydrate load ( 4 ) . The l a c k of symptoms of carbohydrate malabsorption a l s o s t r o n g l y supported t h i s . In a d d i t i o n to slowed absorption i n the small i n t e s t i n e , a reduced r a t e of g a s t r i c emptying and decreased upper g a s t r o i n t e s t i n a l m o t i l i t y may a l s o be f a c t o r s r e s p o n s i b l e f o r reduced glucose l e v e l s a f t e r f i b e r c o n t a i n i n g meals. Guar and p e c t i n have been shown by i s o t o p i c s t u d i e s to delay g a s t r i c emptying i n both normals (5) and p o s t g a s t r i c surgery p a t i e n t s (6i,jO. In a d d i t i o n breath hydrogen s t u d i e s have demonstrated that viscous f i b e r increases the mouth to cecum t r a n s i t time ( 4 ) . However as a model of the e f f e c t of f i b e r i n the small i n t e s t i n e , the % r e d u c t i o n of d i f f u s i o n of glucose from d i a l y s i s bags by each of the f o u r v i s c o u s d i e t a r y f i b e r s (guar gum, tragacanth, p e c t i n and methyl c e l l u l o s e ) was p r o p o r t i o n a l t o the degree t o which each f i b e r reduced the blood glucose response ( r = 0.9938) ( F i g . 3 ) . The c o e f f i c i e n t of determination f o r t h i s r e g r e s s i o n l i n e suggests that over 95% of the r e d u c t i o n i n the blood glucose response by each f i b e r may be accounted f o r by impaired d i f f u s i o n of glucose from the small i n t e s t i n e (8,9.)· The dynamic v i s c o s i t y of 1% s o l u t i o n s of the f i b e r s were



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Leguminous Seed Fiber

Figure 1. Hypothetical effect on upper gastrointestinal function of high-fiber diets containing low energy density foods (A) and low-fiber diets of high energy density foods (B).


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Figure 3. Mean (n = 6 normal subjects) blood glucose area (calculated geo metrically for the 0, 15, 30, 45, and 60 min blood glucose concentrations) of 50 g glucose tolerance tests containing 12 g dietary fiber from guar, gum tragacanth, pectin, or methyl cellulose. The mean blood glucose area is expressed as a percent of the control (fiber-free) blood glucose area and plotted against the concentration at 3 h of glucose in the dialysate surrounding a dialysis bag that contains 30 mL 0.1 M glucose solution and 1 g of guar, gum tragacanth, pectin, or methyl cellulose expressed as a percent of the control (fiber-free) dialysate glucose concentration (r — 0.99, ρ < 0.01).


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measured by Stokes method and were as f o l l o w s : guar, 1.3 N.sec/m; gum tragacanth, 0.52 N.sec/m; p e c t i n , 0.21 N.sec/m; and methyl c e l l u l o s e , 0.07 N.sec/m ( 4 ) . Because of the small numbers the r e l a t i o n s h i p s between v i s c o s i t y of the i n d i v i d u a l f i b r e s and the i n v i t r o r e d u c t i o n of d i f f u s i o n of glucose from d i a l y s i s bags (r = 0.917), and v i s c o s i t y and the i n v i v o r e d u c t i o n of blood glucose responses (r = 0.913) d i d not reach s i g n i f i c a n c e .


Use of F i b e r i n Treatment of Diabetes S i m i l a r reductions of the p o s t p r a n d i a l glucose r i s e a f t e r a meal have been seen i n d i a b e t i c s given guar and p e c t i n (10). Moreover, i n metabolic ward s t u d i e s on 18 d i a b e t i c s , the m a j o r i t y of whom were t a k i n g i n s u l i n , the a d d i t i o n of 14 to 26 g guar per day t o the d i e t f o r 5 days r e s u l t e d i n a 50% r e d u c t i o n i n u r i n a r y glucose output compared with a 5 day c o n t r o l period (11) ( F i g . 4 ) . In these s t u d i e s guar was given i n d i v i d e d doses with each meal, mixed i n t o f r u i t j u i c e s , soups and mashed potato, or baked i n t o breads and c r i s p b r e a d s . Others have a l s o used viscous f i b e r s to t r e a t d i a b e t i c s and found decreased f a s t i n g blood glucose l e v e l s and u r i n a r y glucose e x c r e t i o n with Konjac Mannan (12) and guar (L3). P a r t i c u l a t e f i b e r ( i . e . bran and c e l l u l o s e ) has not produced such marked or c o n s i s t e n t e f f e c t s . Nevertheless two s t u d i e s have shown reduced p o s t p r a n d i a l blood glucose, d a i l y g l y c o s u r i a , i n s u l i n requirement and frequency of hypoglycemic episodes i n d i a b e t i c s under metabolic ward c o n d i t i o n s (14,15). In a d d i t i o n wheatbran has been shown to improve glucose t o l e r a n c e on longer term supplementation of newly diagnosed n o n - i n s u l i n r e q u i r i n g d i a b e t i c s , (16) and i n non-diabetics with d i v e r t i c u l a r disease (17). Nevertheless the e f f e c t s of wheat bran on blood glucose responses to glucose and s t a r c h , glucose k i n e t i c s and plasma i n s u l i n concentrations have not always been confirmed (4,18,19). Importance of Mixing F i b e r Supplements with Food Guar has not always been used s u c c e s s f u l l y i n d i a b e t e s ; (20,21) the reason here i s probably that guar was not given pre-mixed with the carbohydrate p o r t i o n of meals. To i l l u s t r a t e t h i s , we found i n a group of healthy volunteers that guar given j u s t 2 min before a glucose t o l e r a n c e t e s t was without e f f e c t on the r e s u l t i n g blood glucose response ( F i g . 5 ) , while the same amount of guar mixed with the glucose r e s u l t e d i n the expected f l a t t e n i n g (22). Therapeutic use of F i b e r i n Diabetes: Need f o r F i b e r Supplemented Foods Long term use of v i s c o u s f i b e r i s only p o s s i b l e i f p a l a t a b l e


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Figure 4. Overall mean (± SEM) daily urinary glucose loss in 18 diabetics (22 studies) over 5 d without (control) and with 14-26 g guar per day added to metabolically controlled diets.


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supplements are a v a i l a b l e . A guar c r i s p b r e a d produced by Speywood L a b o r a t o r i e s (Bingham, Nottingham, England) i s the only preparation known t o the authors where f i b e r has been e f f e c t i v e l y and p a l a t a b l y pre-mixed with the d i e t a r y carbohydrate · Each s l i c e o f c r i s p b r e a d contained 1 g guar, and d i a b e t i c p a t i e n t s consumed 14-26 s l i c e s per day depending upon t h e i r c a l o r i e intake (1 s l i c e per 100 k c a l ) . In a d d i t i o n t o the 50% r e d u c t i o n o f u r i n a r y glucose e x c r e t i o n seen using t h i s product i n metabolic ward s t u d i e s , (23) i t has allowed a 20% r e d u c t i o n i n i n s u l i n dose over the f i r s t three mouths o f use t o be maintained i n a group o f 6 i n s u l i n r e q u i r i n g d i a b e t i c s f o r over a one year period (24). No reductions i n serum C a , P O 4 , Z n or C u o r hemoglobin concentration were observed i n 8 p a t i e n t s over a s i x month period (24). On the other hand t o t a l and LDL c h o l e s t e r o l were decreased s i g n i f i c a n t l y (5.0 + 0.2 t o 4.5 + 0.3 mmol/1 ρ 0.05; and 3.2 + 0.2 t o 2.6 + 0.3 mmol/1 ρ 0.01 r e s p e c t i v e l y ) and HDL and TG showed no change (1.2 + 0.2 t o 1.3 + 0.1 mmol/1 and 1.2 + 0.2 t o 1.3 + 0.3 mmol/1 r e s p e c t i v e l y ) (24). These f i n d i n g s confirm s i m i l a r e f f e c t s o f guar c r i s p b r e a d on serum l i p i d s of h y p e r l i p i d e m i c p a t i e n t s (25). + +


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Slowly Digested Carbohydrate i n Whole Foods In the same way that d i e t a r y f i b e r may a l t e r a b s o r p t i o n of carbohydrate from foods with which i t i s mixed, so may d i f f e r e n t foods make t h e i r carbohydrate a v a i l a b l e f o r a b s o r p t i o n at d i f f e r e n t r a t e s . When p o r t i o n s o f 14 d i f f e r n e t foods (wholemeal bread, white and wholemeal r i c e and s p a g h e t t i , m i l l e t , buckwheat, i n s t a n t mashed potato, p o r r i d g e oats, sweet potato, kidney and soya beans, marrowfat peas and r e d l e n t i l s ) each c o n t a i n i n g 2 g carbohydrate were mixed with human d i g e s t i v e j u i c e s (obtained from duodenal a s p i r a t i o n ) and placed i n d i a l y s i s bags there was a wide spectrum o f rates o f r e l e a s e of the carbohydrate they contained (26). Bread and g r a i n products released t h e i r carbohydrate at over twice the r a t e as d i d the leguminous seeds (p ε > ο ««

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Glycaemic Index Figure 7. The glycémie index (see text or Figure 6) of 14 foods plotted against the concentration of sugars, in the dialysate at 1 and 5 h, released during in vitro digestion of the same foods. Carbohydrate concentration in the dialysate is expressed as the difference between the sugar concentration in the dialysate that surrounds the dialysis bag containing the digestive juices plus food (active) and the sugar concentration surrounding the dialysis bag containing the digestive juices (Lu = Lundh juice) alone. Key: 0, 1 h; and Φ, 0.5 h.



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i s s t i l l a matter of debate (35). In our metabolic ward s t u d i e s with guar 9 p a t i e n t s had l e s s than 40% carbohydrate i n the d i e t s and 14 had over 40%. Supplementation of the d i e t s with guar produced a s i g n i f i c a n t l y g r e a t e r r e d u c t i o n of the u r i n a r y glucose l o s s i n the high carbohydrate group (64 + 7% v s . 33 + 10% ρ < 0.02) (36). This improvement i n carbohydrate t o l e r a n c e with high carbohydrate d i e t s may i n part e x p l a i n the success reported i n some studies using wheat bran (37). The v a l i d i t y of high carbohydrate/high f i b e r d i e t s has been e s t a b l i s h e d by the pioneer work of Dr. J . Anderson using d i e t s high i n both f i b e r and carbohydrate taken i n unprocessed c e r e a l s , c e r e a l products, leguminous seeds and l e a f y vegetables ( 2 , 3 8 - 4 0 ) . Qf p a r t i c u l a r i n t e r e s t to us i s the f a c t that such high carbohydrate d i e t s might a l s o be c l a s s e d as low g l y c é m i e index d i e t s . Patients o r i g i n a l l y consuming 43% carbohydrate d i e t s were switched to 70% carbohydrate high f i b e r d i e t s and showed improved c o n t r o l and g r e a t l y reduced i n s u l i n requirements. Those on l e s s than 20 u n i t s of i n s u l i n d a i l y could have i t withdrawn. These b e n e f i t s were maintained longterm on an outpatient b a s i s i f p a t i e n t s kept to 60% carbohydrate high f i b e r d i e t s . The advantages o f low g l y c é m i e index d i e t s f o r d i a b e t i c s may not be confined to improved blood glucose c o n t r o l . Beans have been used s u c c e s s f u l l y to t r e a t hypercholesterolemic i n d i v i d u a l s i n Sishuan p r o v i n c e , China (41). In a d d i t i o n i t has been shown that locust bean gum reduced serum l i p i d s i n h y p e r l i p i d e m i c i n d i v i d u a l s (42). Reduction of blood l i p i d l e v e l s i s important to d i a b e t i c i n d i v i d u a l s who are at a g r e a t l y increased r i s k of developing c a r d i o v a s c u l a r disease than the general population (43). E f f e c t i v e d i e t a r y means f o r achieving t h i s are welcome at a time when i n c r e a s i n g side e f f e c t s of hypolipidemic drug therapy w i t h , f o r example c l o f i b r a t e , are being discovered (44-47). Conclusion D i e t a r y f i b e r i s only one o f s e v e r a l p o s s i b l e pharmacologi c a l l y a c t i v e substances found i n foods, and present i n high concentrations i n leguminous seeds which 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 t r a t e s of d i g e s t i o n and blood glucose responses of d i f f e r e n t meals. Enzyme i n h i b i t o r s , l e c t i n s and saponins are other so c a l l e d a n t i n u t r i t i o n a l f a c t o r s , a l s o a s s o c i a t e d with d i e t a r y f i b e r which are able to a l t e r small i n t e s t i n a l f u n c t i o n (48). The g a s t r o i n t e s t i n a l t r a c t evolved to d e a l with these c o n s t i t u e n t s i n foods so that while t o x i c i n large amounts (as i n uncooked beans) small amounts may have b e n e f i c i a l e f f e c t s . These a n t i n u t r i e n t s have now l a r g e l y been e l i m i n a t e d from the Western d i e t by r e f i n i n g and h i g h l y processing our foods. However, as with d i e t a r y f i b e r , we are l i k e l y i n the future to see s p e c i f i c combinations of them reincorporated i n small amounts i n t o our d i e t f o r reasons of h e a l t h . The studies on d i e t a r y f i b e r have opened the way f o r t h i s with t h e i r demonstrations of


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health benefits for diabetics, and possible relevance to the general population for the prevention of disease. It is also likely in the future, as more knowledge becomes available, that we shall see the food industry playing a role in the pharmacological manipulation of the diet for health using plant derived substances. Acknowledgments


DJAJ is in receipt of a grant from the Canadian Diabetes Association and both DJAJ and LUT are in receipt of a strategic grant from the Natural Sciences and Engineering Research Council. RHT is a Wellcome Senior Research Fellow in Clinical Science. Literature Cited 1. Burkitt, D.P.; Trowell, H.C. "Refined Carbohydrate Foods and Disease"; Academic Press, London, 1975. 2. Kiehm, I.G.; Anderson, J.W.; Ward, K. Amer. J. Clin. Nutr. 1976,29,895-899. 3. Kritchevsky, D. Proc VII Int Symp on Drugs Affecting Lipid Metabolism 1980, pp. 333-338. 4. Jenkins, D.J.Α.; Wolever, T.M.S.; Leeds, A.R.; Gassull, M.A.; Dilawari, J.B.; Goff, D.V.; Metz, G.L.; Alberti, K.G.M.M. Brit. Med. J. 1978,1,1392-1394. 5. Holt, S.; Heading, R.C.; Carter, D.C.; Prescott, L.F.; Tothill, P. Lancet 1979,1,636-639. 6. Leeds, A.R.; Ralphs, D.N.; Bonlos, P.; Ebied, F.; Metz, G.L.; Dalawari, J.; Elliott, Α.; Jenkins, D.J.A. Proc. Nutr. Soc. 1978,37,23 (Abstract). 7. Leeds, A.R.; Ralphs, D.N.L.; Ebied, F.; Metz, G.; Dilawari, J.Β. Lancet 1981,1,1075-1078. 8. Elsenhaus, B.; Sufke, U.; Blume, R.; Caspary, W.F. Clin. Sci. 1980,59,373-380. 9. Johnson, I.T.; Gee, J.M. Proc. Nutr. Soc. 1980,39,52 (Abstract). 10. Jenkins, D.J.Α.; Leeds, A.R.; Gassull, M.A.; Wolever, T.M.S.; Goff, D.V.; Alberti, K.G.M.M.; Hockaday, T.D.R. Lancet 1976,2,172-174. 11. Jenkins, D.J.Α.; Wolever, T.M.S.; Nineham, R.; Bacon, S.; Smith, R.; Hockaday, T.D.R. Adv. Exp. Med. Biol. 119,275-279. 12. Doi, K.; Matsuura, M.; Kawara, Α.; Baba, S. Lancet 1979,1, 987-988. 13. Aro, Α.; Uusitripa, M.; Vontilainen, Ε.; Hersio, K.; Korhonen, T., Sirtonen, O. Diabetologia 1981,21,29-33. 14. Monnier, L.H.; Blotman, M.J.; Coletti, C.; Monnier, M.P.; Mironze, J. Diabetologia 1981,20,12-17.



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37. Kahaner, Ν.; Fuchs, H.M.; Flock, M.H. Am. J. Clin. Nutr. 1976,29,1437-1442. 38. Anderson, J.W.; Ward, K. Diabetes Care 1978,1,77-82. 39. Anderson, J.W.; Chen, W.L. Am. J. Clin. Nutr. 1979,32,346-363. 40. Anderson, J.W.; Ward, K. Am. J. Clin. Nutr. 32,2312-2321. 41. Bingwen, L.; Zhaofeng, W.; Wanzhen, L.; Rongjue, Z. Chinese Med. J. 1981,94,455-458. 42. Zavoral, J.H.; Fields, D.; Hansen, M.; Hannon, P.; Kuba, K.; Franty, I.; Jacobs, D. American Chem. Soc. Div. Agr. Food Chem. 183rd Meeting 1982. 43. Ostrander, L.D.; Francis, T.; Hayner, N.S.; Kjelsberg, M.D.; Epstein, F.H. Ann. Int. Med. 1965,62,1188-1198. 44. Coronary Drug Project Research Group New. Eng. J. Med. 296,1185-1190. 45. Axelson, O.; Jagesson, C. Lancet 1980,2,1081. 46. Reddy, J.K. Proc VII Int. Symp on Drugs Affecting Lipid Metabolism pp. 301-309. 47. Oliver, M.F.; Heady, J.Α.; Morris, J.N.; Cooper, J.; Geizerova, H.; Gyarfas, I., Green, K.J.; Strassen, T. Report from the committee of principal investigators. Brit. Heart J . 40,1069-1118. 48. Jenkins, D.J.A. "Current Topics in Nutrition and Disease Vol 4: Nutritional Pharmacology" Ed.; Spiller GA, Alan R Liss Inc. New York, pp. 117-145. RECEIVED October 29,1982


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