Dietary Fiber and the Bioavailability of Iron - ACS Symposium Series

9 Dietary Fiber and the Bioavailability of Iron JOHN G. REINHOLD

Downloaded by AUBURN UNIV on April 18, 2017 | http://pubs.acs.org Publication Date: November 1, 1982 | doi: 10.1021/bk-1982-0203.ch009

University of Guadalajara, Faculty of Veterinary Medicine and Animal Science, Center for the Study of Nutrition, Apdo. Postal 406-1, Guadalajara, Jalisco, México.

Iron II combines with several components of dietary fiber to form complexes that are stable between pH 6.0 and 7.0. Iron so bound is released as the pH falls below 6.0, release becoming complete near pH 1.0. Binding is inhibited by ascorbate, citrate, cysteine, EDTA and phytate in low concentrations. The various components of dietary fiber differ in affinity for iron. Dietary fiber from different sources, e.g., wheat and maize, have d i f f e r i n g capabilities for binding iron. Increased consumption of dietary fiber or fiber-rich foods tends to impair iron absorption. Impairment is best demonstrated i f single fiber sources are used, and when the amount in the diet is 10 % or more. Consumption of large amounts of wheaten fiber by human subjects has been associated with increased fecal losses of iron and decreased iron balances. Concentrations of iron in serum tend to decrease. The presence of inhibitors of iron binding in diets may explain, in part, differences in response to fiber. Calculation of the amount of iron sequestered indicates that only when dietary fiber intakes are quite high will iron binding seriously interfere with absorption of iron. However, other actions of fiber contribute to impairment of iron availability. 0097-6156/82/0203-0143$06.00/0 © 1982 American Chemical Society Kies; Nutritional Bioavailability of Iron ACS Symposium Series; American Chemical Society: Washington, DC, 1982.


144

NUTRITIONAL BIOAVAILABILITY OF IRON

D i e t a r y f i b e r may i n t e r f e r e w i t h i r o n a b s o r p t i o n by s e v e r a l a c t i o n s . The i n c r e a s e i n w e i g h t and b u l k o f u n d i g e s t e d r e s i d u e s i n t h e g u t t h a t f o l lows i n t a k e o f f i b e r i n i n c r e a s e d amounts l e a d s t o d e c r e a s e d t r a n s i t t i m e s and i n c r e a s e d f r e q u e n c y of d e f e c a t i o n . F e c a l w e i g h t i n c r e a s e s . The time o f c o n t a c t between v i l l i and i r o n d e c r e a s e s w i t h l e s s e n e d o p p o r t u n i t y f o r a b s o r p t i o n . Eastwood and Kay (1) have l i k e n e d t h e b e h a v i o r o f d i e t a r y f i b e r t o t h a t o f a sponge w i t h b o t h f i b r o u s and amorphous p r o p e r t i e s . I r o n may e n t e r t h e p o r e s o f t h e f i b e r t o become compartmented and s p a t i a l l y h i n d e r e d from making c l o s e c o n t a c t w i t h t h e mucosa. The i n c r e a s e d f e c a l b u l k combined w i t h t h e a b r a s i v e n e s s o f d i e t a r y f i b e r may combine t o i n c r e a s e l o s s e s o f i r o n by t h e s l o u g h i n g o f mucos a l e p i t h e l i u m , n o r m a l l y a major pathway f o r e x c r e t i o n o f i r o n . Fiber provides a matrix f o r thegut f l o r a a n d s o may s t i m u l a t e i t s g r o w t h . W i t h i n c r e a s e d incorporation of iron into bacterial cells, iron

so d i v e r t e d i s no l o n g e r a v a i l a b l e f o r a b s o r p t i o n . The major components o f d i e t a r y f i b e r , c e l l u l o s e and t h e h e m i c e l l u l o s e s , form complexes w i t h i r o n ( 2 , 2 . ) . D i e t a r y f i b e r may promote t h e c o n v e r s i o n o f i r o n I I t o i r o n I I I i n some c i r c u m s t a n c e s . Such a c o n v e r s i o n would t e n d t o d e c r e a s e i r o n a v a i l a b i l i t y . D i e t a r y f i b e r i n c l u d e s c e l l u l o s e and l i g n i n which together comprise t h e a c i d - d e t e r g e n t f i b e r (ADF) (4) f r a c t i o n ; t h e h e m i c e l l u l o s e s , a complex g r o u p w i t h a p o l y m e r i z e d x y l o s e framework w i t h a r a b i n o s e , mannose, g a l a c t o s e , g l u c o s e , rhamnose, g l u c u r o n i c and g a l a c t u r o n i c a c i d s u b s t i t u t i o n s and d i f f e r i n g d e g r e e s o f b r a n c h i n g ; and p e c t i n , a m i x t u r e of m e t h y l - e s t e r i f i e d g a l a c t u r o n a n , g a l a c t a n , and araban. C e r e a l g r a i n s c o n t a i n l i t t l e p e c t i n . T o t a l d i e t a r y f i b e r i s c o n v e n i e n t l y i s o l a t e d and measured as n e u t r a l d e t e r g e n t f i b e r (NDF) w h i c h i n c l u d e s t h e f o r e g o i n g components (J5#fi). I n a d d i t i o n t o t h e d i e t a r y f i b e r occurring n a t u r a l l y i n foods, n o n d i g e s t i b l e p o l y s a c c h a r i d e s from seaweeds and o t h e r s o u r c e s , i n c l u d i n g gums, a r e i n c l u d e d and become i m p o r t a n t b e cause o f t h e i r w i d e s p r e a d use a s f o o d a d d i t i v e s . F o r d e t a i l e d i n f o r m a t i o n about t h e c o m p o s i t i o n o f d i e t a r y f i b e r s e e (6, 2# 8) .

Kies; Nutritional Bioavailability of Iron ACS Symposium Series; American Chemical Society: Washington, DC, 1982.

9.

REINHOLD

145

Effect of Dietary Fiber

Evidence that d i e t a r y f i b e r i n t e r f e r e d with absorpt i o n o f b i v a l e n t m e t a l s b y t h e i n t e s t i n e was f i r s t ob t a i n e d i n c o n n e c t i o n w i t h s t u d i e s o f human z i n c d e f i c i e n c y i n I r a n . Human s u b j e c t s who consumed p u r i f i e d p h y t a t e e x h i b i t e d s m a l l e r f e e a l l o s s e s o f z i n c and c a l c i u m t h a n t h e y d i d when t h e y a t e e q u i v a l e n t a m o u n t s o f p h y t a t e i n t h e form o f u n l e a v e n e d wheaten whole meal f l a t breads that are the staple food i n r u r a l Iran

(2)• B r e a d components o t h e r t h a n p h y t a t e were examined f o r t h e i r a b i l i t y t o b i n d m e t a l s . F i b e r , p r o t e i n and s t a r c h o f wheat formed s t a b l e complexes w i t h z i n c and


c a l c i u m , a n d l a t e r i r o n was f o u n d t o s h a r e t h i s b e h a v i o r . The m e t a l s combined w i t h p r o t e i n o r wheat s t a r c h ,

however, were r e l e a s e d d u r i n g d i g e s t i o n w i t h p e p t i d a s e s and amylases ( 2 , 1 0 ) . By c o n t r a s t d i e t a r y f i b e r , b e i n g r e s i s t a n t t o d i g e s t i v e s e c r e t i o n s , r e t a i n e d bound m e t a l i n t a c t . Removal o f p h y t a t e , w h i c h h a d i n t h e p a s t been h e l d t o be t h e main s o u r c e o f m e t a l c o m p l e x a t i o n by bread, d i d n o t decrease b u t tended t o enhance t h e b i n d i n g o f t h e m e t a l (2.) . F u r t h e r d o u b t a b o u t t h e r o l e o f

p h y t a t e as t h e m e t a l b i n d i n g a g e n t o f b r e a d s was i n t r o duced by t h e absence o f a c l o s e r e l a t i o n s h i p between t h e d e s t r u c t i o n o f p h y t a t e by a c t i o n o f l e a v e n and t h e s o l u b i l i t y o f z i n c ( 1 1 ) . S u b s e q u e n t l y , s t u d i e s by I s m a i l B e i g i e t a l . Q ) s h o w e d t h a t c e l l u l o s e f r o m some s o u r c e s , c e r t a i n c e l l u l o s e d e r i v a t i v e s , and h e m i c e l l u l o s e s

p r e p a r e d from wheat b r a n s h a r e d t h e a b i l i t y t o b i n d i r o n and z i n c . Camire and C l y d e s d a l e (12) r e c e n t l y d e scribed differences i n the iron binding c a p a b i l i t y of several cellulose preparations.

A f f i n i t y of Dietary Fiber Preparations

f o r Iron

Uptake o f i r o n I I by NDF suspended i n s o l u t i o n s o f t h e c o m p o s i t i o n d e s c r i b e d below and b u f f e r e d a t pH 6*4 i s r e c t i l i n e a r up t o i r o n c o n c e n t r a t i o n s o f about 1*5 ug/ml ( 1 3 ) . Above t h e l a t t e r c o n c e n t r a t i o n , t h e i r o n becomes u n s t a b l e

and t h e r e s u l t s e r r a t i c .

The

quantity

o f i r o n bound b y NDF o f wheat exceeded t h a t bound b y t h e NDF o f maize by about 25 % . B i n d i n g by ADF and by c e l l u l o s e ( f i n e l y d i v i d e d f i l t e r paper o r a b s o r b e n t c o t t o n ) were e q u a l

and about

half

o f t h e amount o f

i r o n bound by wheat NDF. F o r measurement o f b i n d i n g , 20 mg o f f i b e r were suspended i n 10 ml o f a s o l u t i o n c o n t a i n i n g 7.5 g o f N a C l , 5.0g o f D - g l u c o s e ,


146


0.3 g o f KC1, sodium a c e t a t e 1.0 mMol, i m i d a z o l e 0.5 mMol, HC1, 0.2 mMol, a s c o r b i c a c i d 0.28 mMol and i r o n as FeS04 0.0129 mMol p e r l i t e r . pH was a d j u s t e d t o 6.40 + 0.05 . A f t e r e q u i l i b r a t i o n f o r 30min, t h e f i b e r was removed by c e n t r i f u g a t i o n and i r o n measured i n t h e s o l u t i o n w i t h the a i d o f s u l f o n a t e d bathophenanthrol i n e (13). When i r o n bound by f i b e r a t s e v e r a l i r o n c o n c e n t r a t i o n s was p l o t t e d a g a i n s t t h e r a t i o : bound i r o n / f r e e iron, straight lines resulted. Intercepts with the a x i s f o r bound i r o n y i e l d e d c o e f f i c i e n t s o f b i n d i n g f o r wheat NDF, 0.39; maize NDF, 0.30; maize o r wheat ADF, 0.24; c e l l u l o s e 0.22 mg i r o n / g f i b e r ( 1 3 ) . Monnier e t a l (14) u s i n g c o n d i t i o n s q u i t e d i f f e r e n t f r o m t h o s e d e s c r i b e d above, f o u n d no i r o n t o be bound by c e l l u l o s e , b u t d i d f i n d t h a t p e c t i n bound i r o n s t r o n g l y . Water-and a l k a l i - s o l u b l e h e m i c e l l u l o s e s prep a r e d from r i c e bound i r o n (tood e t a l , 1 5 ) . Copper and z i n c were a l s o bound. The m e t a l s were r e l e a sed by h e m i c e l l u l a s e and p e p t i d a s e a c t i o n . These hemic e l l u l o s e i s o l a t e s i n c l u d e d c o n s i d e r a b l e amounts o f d i g e s t i b l e p r o t e i n and c o n s e q u e n t l y do n o t conform t o t h e c o n c e p t o f f i b e r as a n o n - d i g e s t i b l e r e s i d u e . However, c l o s e a s s o c i a t i o n s o f f i b e r and p r o t e i n do o c c u r and t h e i r i m p l i c a t i o n s f o r f i b e r b e h a v i o r must be r e c o g n i z e d Mod e t a l (15) a s s i g n a r o l e t o f i b e r bound p r o t e i n i n b i n d i n g o f m e t a l s . Thompson and Weber (16) o b s e r v e d t h a t i o n exchange p r o p e r t i e s o f d i e t a r y fitoer depended upon method o f p r e p a r a t i o n .


4

E f f e c t o f pH upon B i n d i n g o f I r o n by D i e t a r y

Fiber

B i n d i n g o f i r o n by d i e t a r y f i b e r approaches a maximum a s pH a p p r o a c h e s 7.0 ( 1 3 ) • I t i s m i n i m a l i n t h e n e i g h b o r h o o d o f pH 1.0 Thompson and Weber (16) and R e i l l y (12) showed t h a t t h e e f f e c t s o f pH were r e v e r s i b l e o v e r t h e r a n g e 1.0 t o 7.0.Camire and C l y d e s d a l e (12) found a marked change i n b i n d i n g o f i r o n by c e l l u l o s e t o ocaur between pH 5.0 and 6.0 a f t e r b o i l i n g , and by l i g n i n a f t e r t o a s t i n g , b u t n o t by t o a s t e d o r b o i l e d wheat b r a n . Working w i t h NDF p r e p a r e d by t h e method o f R o b e r t s o n and Van S o e s t (3) $ R e i n h o l d e t a l (13) showed t h a t b i n d i n g o f i r o n t r a c e d a s i n u s o i d a l p a t h between pH 5.0 and 7.0 w i t h a m i d p o i n t a t about pH 5.8. NDF f r o m wheat and maize d e s c r i b e d i d e n t i c a l c u r v e s w h i c h


9.

REINHOLD

differed

147

Effect of Dietary Fiber i n h e i g h t because

of difference

in affinity

for

i r o n between t h e two. Wheat and maize b r a n s behaved l i k e t h e i r NDFs. The l o c a t i o n s and c o n f i g u r a t i o n s o f t h e c u r v e s were not a l t e r e d by r e m o v a l o f p h y t a t e . B i n d i n g o f i r o n by c e l l u l o s e or ADF p r e p a r a t i o n s a l s o d e c r e a s e d markedly between pH 7.0 and 5.0 b u t t o a l e s s e r e x t e n t t h a n d i d t h e NDFs ( 1 3 ) .


I n h i b i t i o n of Iron Binding B i n d i n g o f i r o n by d i e t a r y f i b e r i s s t r o n g l y i n h i b i t e d by a s c o r b i c a c i d , c i t r a t e , c y s t e i n e , EDTA or p h y t a t e i n c o n c e n t r a t i o n s as lew as 100 y u M o l s / L i t e r (A3). The i n h i b i t o r s have t h e common p r o p e r t y o f b e i n g able ylic

t o form s o l u b l e amino a c i d s and

complexes w i t h i r o n . t h e i r amides i n h i b i t

The decarboxbinding

m o d e r a t e l y as do l y s i n e and h i s t i d i n e . O t h e r amino a c i d s e i t h e r do not i n t e r f e r e w i t h b i n d i n g o f i r o n f i b e r o r do so o n l y w e a k l y . C a l c i u m (as a c e t a t e ) and phosphate a c t as moderate i n h i b i t o r s . The d e t e r g e n t s sodium l a u r y l s u l f o n a t e or c e t y l t r i m e t h y l a m m o n i u m bromide had no e f f e c t on i r o n b i n d i n g by f i b e r ( 1 3 ) . S t a b i l i t y of Fiber-Bound t i n a l segments

Iron i n Presence

of I n t e s -

Segments o f r a t i n t e s t i n e r e a d i l y a b s o r b i r o n from an i r o n - c o n t a i n i n g s a l i n e g l u c o s e s o l u t i o n s i m i l a r t o t h a t d e s c r i b e d above. The up-take o f i r o n by t h e segments i s d e c r e a s e d s i g n i f i c a n t l y by NDF o r nond i g e s t i b l e r e s i d u e s p r e p a r e d from wheat b r a n by s u c c e s s i v e t r e a t m e n t w i t h a m y l o l y t i c and p e p t i d e - s p l i t t i n g enzymes. On t h e o t h e r hand, f i b e r o f maize p r o duces r e l a t i v e l y l i t t l e i n t e r f e r e n c e . E x a m i n a t i o n o f some 40 wheat f i b e r p r e p a r a t i o n s y i e l d e d a modal v a l u e f o r i n t e r f e r e n c e o f 36 %, w i t h a h i g h o f 78% ( 1 8 ) . Uptake o f f i b e r - b o u n d i r o n was not i n c r e a s e d by t h e presence of substances t h a t i n h i b i t e d i r o n b i n d i n g i n v i t r o , such as a s c o r b a t e , c y s t e i n e , e t c . They, i n t u r n , i n h i b i t e d uptake o f i r o n i n d e p e n d e n t l y o f f i b e r , so t h a t t h e a c t i o n s o f f i b e r p r e p a r a t i o n s and s o l u b l e c h e l a t o r s were a d d i t i v e . L o w e r i n g t h e pH o f t h e s o l u t i o n s t o 4.5 or l e s s appeared t o p e r m i t some uptake o f f i b e r - b o u n d i r o n , b u t d i d not do s o c o n -

Amerlcan Chemical Society Library 1155 ieth st N. w.

Katttagton, D. C. 20036 Kies; Nutritional Bioavailability of Iron ACS Symposium Series; American Chemical Society: Washington, DC, 1982.

148


s i s t e r v t l y . These e x p e r i m e n t s i n d i c a t e t h a t complexes o f i r o n w i t h d i e t a r y f i b e r a r e not e a s i l y d i s r u p t e d by t h e i r o n a c c e p t o r s o f e i t h e r s m a l l o r l a r g e i n t e s tine.


D i e t a r y f i b e r and

the o x i d a t i v e s t a t e of d i e t a r y i r o n

I t has l o n g been known t h a t non-heme i r o n i s a b s o r b e d o n l y as t h e f e r r o u s form from t h e i n t e s t i n e . I t appears t h a t the presence of d i e t a r y f i b e r p r e p a r ations favors conversion of i r o n I I to iron I I I w i t h i n t h e range o f pH p r e v a i l i n g i n t h e i n t e s t i n a l c o n t e n t s ( R e i n h o l d and Garzon, u n p u b l i s h e d , 1981). K o j i m a e t a l (19) observed c o n s i d e r a b l e o x i d a t i o n o f Fe I I t o Fe I I I d u r i n g s o l u b i l i z a t i o n o f t h e i r o n o f cooked p i n t o bean s u s p e n s i o n s by c i t r i c a c i d between pH 4.0 and 7.0 EDTA and o t h e r c h e l a t i n g a g e n t s a c t e d i n a s i m i l a r manner, and i t i s p o s s i b l e t h a t t h e bean f i b e r may have promoted t h e c o n v e r s i o n . H a r r i s and A i s e n (20) have shewn t h a t o x i d a t i o n o f i r o n i s f a c i l i t a t e d by i r o n b i n d i n g a g e n t s . N o j e i m and C l y d e s d a l e (21) r e p o r t t h a t t h e c o n v e r s i o n o f Fe I I t o Fe I I I i s pHdependent. F o r m a t i o n o f Fe I I I i s f a v o r e d a t pH 6.2 and t h e r e v e r s e a t pH 2.7. The E f f e c t o f D i e t a r y F i b e r upon A b s o r p t i o n by A n i m a l s

of Iron

C e r t a i n r e q u i r e m e n t s must be f u l f i l l e d i n o r d e r t o s u c c e s s f u l l y demonstrate an e f f e c t o f d i e t a r y f i b e r upon i r o n a v a i l a b i l i t y i n m o n o g a s t r i c a n i m a l s : (a) i n c l u s i o n o f enough f i b e r i n t h e d i e t t o produce t h e m o d i f i c a t i o n s i n p h y s i o l o g i c a l f u n c t i o n s of the gut a s s o c i a t e d w i t h f i b e r consumption, e.g. changed mot i l i t y , f e c a l volume and w e i g h t , w a t e r - h o l d i n g , i o n exchanging b e h a v i o r and o t h e r s , (b) l i m i t a t i o n o f i r o n i n t a k e , (c) o b s e r v a t i o n f o r a s u f f i c i e n t t i m e t o p e r m i t t h e e f f e c t s o f f i b e r t o be m a n i f e s t e d , and (d) use o f s p e c i e s w i t h a l i m i t e d c a p a b i l i t y f o r d e s t r u c t i o n o f f i b e r . Lee and Oace (22) q u e s t i o n t h e s u i t a b i l i t y o f t h e r a t i n t h i s c o n n e c t i o n because o f t h e l o n g s o j o u r n o f d i g e s t a i n a c a p a c i o u s cecum and consequent d e g r a d a t i o n o f f i b e r , p a r t i c u l a r l y x y l a n s . They suggest r e s t r a i n t i n e x t r a p o l a t i o n o f f i n d i n g s for r a t s to other s p e c i e s .



9.

REINHOLD


149

D e s p i t e t h i s drawback, a number o f s t u d i e s based a l m o s t e n t i r e l y upon t h e use o f r a t s have shown t h a t d i e t a r y f i b e r s from v a r i o u s s o u r c e s may i m p a i r i r o n a b s o r p t i o n ( T a b l e 1 ) • The f i b e r s o u r c e s examined most o f t e n were f i b e r - r i c h m i l l f r a c t i o n s o f wheat, g e n e r a l l y b r a n . The use o f i s o l a t e d f i b e r components i s c o n f i n e d l a r g e l y t o c e l l u l o s e . A l t h o u g h wheat b r a n i s r i c h i n p h y t a t e , t h e work o f M o r r i s and E l l i s (34) s u p p o r t e d by subsequent p u b l i c a t i o n s from t h e same s o u r c e , i n d i c a t e s t h a t i n t e r f e r e n c e by p h y t a t e w i t h i r o n a b s o r p t i o n i s n o t a p p r e c i a b l e , and can be d i s r e g a r d e d . Liebman and D r i s k e l l (35) and Hunter (36) have a l s o f o u n d no i n t e r f e r e n c e by p h y t a t e w i t h i r o n metabo l i s m , c o n f i r m i n g t h e e a r l i e r r e p o r t o f Cowan e t a l (22) • However, Simpson e t a l (61) v e r y r e c e n t l y r e c e n t l y r e p o r t e d t h a t a p h o s p h a t e - r i c h e x t r a c t o f dephyt i n i z e d b r a n i n h i b i t e d i r o n a b s o r p t i o n . Thus, i t i s not p e r m i s s i b l e t o equate b r a n w i t h f i b e r c o m p l e t e l y . Among s i n g l e f i b e r s o u r c e s , c e l l u l o s e d e c r e a s e d i r o n a b s o r p t i o n when f e d i n s u f f i c i e n t amounts t o r a t s (23,33.) b u t n o t t o monkeys (22) o r c h i c k e n s (2JJ • Agar, c a r r a g e e n a n , a l g i n a t e and f u c o i d a n d e c r e a s e d i r o n b a l ance (2J3) o r i r o n uptake (23) i n r a t s . The d i f f e r e n c e between t h e r e s p o n s e o f i r o n - d e p l e t e d and i r o n - r e p l e t e r a t s t o a l g i n a t e i s o f i n t e r e s t . I r o n a b s o r p t i o n was d e c r e a s e d i n t h e l a t t e r b u t n o t i n t h e former (23). D i e t a r y F i b e r and I r o n A b s o r p t i o n by Humans Widdowson and McCance (38) i n 1942 measured i r o n b a l a n c e s o f men and women w h i l e t h e y a t e d i e t s i n w h i c h wheaten b r e a d o f 92% e x t r a c t i o n r a t e o r w h i t e b r e a d were t h e p r i n c i p a l s o u r c e s o f energy f o r e i g h t o r more weeks. The b r e a d , made o f f l o u r s o f h i g h e x t r a c t i o n r a t e , lowered i r o n b a l a n c e s d e s p i t e i t s h i g h e r i r o n c o n t e n t , a l t h o u g h b a l a n c e s d i d n o t become n e g a t i v e . Walker e t a l (39) made a s i m i l a r comparison o f i r o n b a l a n c e s w h i l e w h i t e o r brown b r e a d s were e a t e n , a l t h o u g h a t a lower l e v e l o f i n t a k e ( e s t i m a t e d t o be 30 t o 40 % o f t o t a l energy i n t a k e ) . I r o n b a l a n c e s were l o w e r e d d u r i n g each p e r i o d o f brown b r e a d consumption. The a u t h o r s d i d n o t e v a l u a t e t h e i r f i n d i n g s s t a t i s t i c a l l y , however, a p p l i c a t i o n o f t h e t t e s t t o t h e d a t a shows t h e d i f f e r e n c e i n i r o n b a l a n c e s between t h e




Table I The e f f e c t o f d i e t a r y f i b e r s o r f i b e r - r i c h f o o d s on iron b i o a v a i l a b i l i t y i n animals. Authors, Ref. Animal F i b e r source year

Criteria

Bioavailability

S t i l e s e t 23 al,1976

Rat

Whole body count

Decreased Decreased No e f f e c t

Ranhotra et a l , 1979

24

Rat

Corn p e r i c a r p Cellulose Peanut h u l l s (7.5 t o 30 %, 18 days) Cellulose i n corp.into bread(10-30%)

Hb r e pletion

Decreased

Lee e t a l , 1979 25

High c e l l u l o s e bread Bran,soy o r veg.flour supplements

Hb r e pietion

No

Rat

effect

Decreased

Miller, 1979

26

Anemic Wheat s h o r t s rat (70-210 gAg diet)

Hb r e pletion

No

Spiller et a l , 1980

27

PigWheat b r a n tail Semi-purified monkey c o r n b r a n Cellulose Pectin (3,6,9 g/day)

Balance

Decreased

Harmuth28 Hoene e t al,1980

Woelbling et a l , 1980

29

Rat

Carrageenan BalAgar ance Alginate Guar gum C a r o b bean gum (10% l e v e l ) Rat, Alginate Fe Jejunal Guar gum uptake segment Anemic A l g i n a t e rat Guar gum 5 9

Continued

effect

Decreased Decreased Decreased No e f f e c t No e f f e c t Decreased Decreased No No

effect effect

on n e x t


page.

9. REINHOLD


Table I-continued. Authors, Ref. Animal year


B e c k e r e t 30 a l , 1980

Rat,jejunal segment Anemic rat

F i b e r source

Fucoidan

151

Criteria

Bioavailability

39" Fe uptake

Decreased

Decreased

Fucoidan

Thompson, 31 Weber, 1981

Chick

Wheat b r a n Corn bran Soy b r a n Oat h u l l s Cellulose Rice bran (6% level)

Iron i n liver, tibia

No e f f e c t No e f f e c t No e f f e c t No e f f e c t No e f f e c t Decreased

HarmuthHoene et a l , 1981

32

Rat

Whole wheat, B a l a n c e r y e breads bran-supplemented

Decreased Decreased

GarciaLopez, Wyatt, 1981

33

Rat

C e l l u l o s e , 5% Hb r e Cellulose,10% pletion Cellulose,15%

No e f f e c t Decreased Decreased

Ranhotra et a l

66 R a t

Iranian flatbread

Hb r e pletion

No

Wiemer, Kies

67

Weanling mice

Hemicellulose

Balance

Decreased

Dog

Lignin Hemicellulose Pectin

Duodeno- D e c r e a s e d Decreased jejunal perfusion Small decrease No e f f e c t

Fernandez, 69 Phillips

Cellulose Reinhold et a l

18 R a t

Wheat NDF Maize NDF

effect

Uptake, Decreased intestina l s e g - Decreased ments.


152


periods

NUTRITIONAL BIOAVAILABILITY OF IRON of white

and

brown b r e a d s

t o be

highly

signifi-

c a n t . T h i s i s c o n t r a r y t o t h e i r c o n c l u s i o n t h a t "the r e t e n t i o n o f i r o n was v i r t u a l l y t h e same f o r low and h i g h p h y t a t e diets''the two b r e a d s b e i n g i d e n t i f i e d by t h e i r p h y t a t e c o n t e n t s , ( P h y t a t e a t the time was c o n s i d e r e d t h e major a n t i m e t a b o l i t e f o r i r o n ) . C u l l u m b i n e e t a l (40) e v a l u a t e d i r o n b a l a n c e s w h i l e e i t h e r w h i t e o r brown r i c e was b e i n g e a t e n . A l t h o u g h i r o n r e t e n t i o n was lower w h i l e brown r i c e s e r v e d as t h e main energy s o u r c e , t h e d i f f e r e n c e s were s m a l l and n o t s i g n i f i c a n t . Bjorn-Rasmussen (41) f o u n d a r e m a r k a b l y c o n s i s t e n t r e l a t i o n s h i p between i r o n uptake o f men and t h e negat i v e l o g a r i t h m o f t h e q u a n t i t y o f b r a n added t o t h e diet. The f o r e g o i n g and more r e c e n t s t u d i e s o f i r o n u t i l i z a t i o n by humans as a f f e c t e d by consumption o f d i e t a r y f i b e r s o r o f f i b e r - r i c h f o o d s a r e summarized i n T a b l e 2. As w i t h s t u d i e s o f a n i m a l s , i n v e s t i g a t i o n s o f p u r i f i e d f i b e r components a r e few, t h e main dependence b e i n g upon f i b e r - r i c h f o o d s t u f f s , e s p e c i a l l y wheat b r a n as t h e s o u r c e o f f i b e r i n t a k e enhancement. The composit i o n o f t h e d i e t used d u r i n g b a l a n c e s t u d i e s may a f f e c t the r e s p o n s e o f i r o n metabolism t o f i b e r consumption. Thus, d i e t s c o n t a i n i n g f r u i t s and v e g e t a b l e s i n abundance may d e c r e a s e b i n d i n g o f i r o n by d i e t a r y f i b e r because o f i n h i b i t i o n by a s c o r b i c , c i t r i c and o t h e r a c i d s present i n these foods. Increased absorption of i r o n woold be f a v o r e d . Such a c i d s have been f o u n d t o be augmentors o f i r o n a b s o r p t i o n (59#61). The unique b e h a v i o r o f i r o n i n t h e experiments o f K e l s a y e t a l (52) i n w h i c h d i e t a r y f i b e r i n t a k e s were e l e v a t e d by consumption o f f r u i t s and v e g e t a b l e s may have i t s o r i g i n i n t h i s f a c t o r . O n l y i r o n among t h e s e v e r a l b i valent c a t i o n s studied f a i l e d to respond with negative b a l a n c e s , A s i m i l a r a c t i o n may h a v e i n f l u e n c e d t h e r e s u l t s o f o t h e r i n v e s t i g a t o r s . Thus, the c o n v e n t i o n a l

f o o d s l i s t e d by S a n d s t e a d e t a l (50) as f o r m i n g p a r t o f the d i e t of subjects p a r t i c i p a t i n g i n t h e i r balance s t u d i e s i n c l u d e d s e v e r a l s o u r c e s o f a s c o r b a t e and c i t r a t e . The e f f e c t s o f a s c o r b i c a c i d and o f meat a r e c l e a r l y shown by t h e experiments o f Simpson e t a l ( 6 1 ) . The l a t t e r demonstrated t h a t removal o f p h y t a t e from b r a n does not d i m i n i s h i t s a c t i v i t y i n i m p a i r i n g i r o n a b s o r p t i o n by humans. They d i d , however, f i n d t h a t t h e


9.

REINHOLD


153


Table I I The e f f e c t o f d i e t a r y f i b e r s o f f i b e r - r i c h f o o d s on i r o n b i o a v a i l a b i l i t y i n humans. Criteria

Bioavailability

Bread, 9 2 % extraction wheat f l o u r

Balance

Decreased

Walker e t i39 a l , 1948

Bread,95-100% extraction wheat f l o u r

Balance

Decreased (see t e x t )

Cullumbine 40 e t al,1950

Brown r i c e

Balance

No

41 Bj6rn-Rasmussen, 1974

Increments o f wheat b r a n i n bread F o r t i f i e d white vs f o r t i f i e d wholemeal b r e a d

Uptake o f radioiron by r b c

White v s w h o l e meal c h a p a t t i s S i f t e d v s unsifted flour

Whole body count Whole body count

Wheat bran,36

Serum

Decreased by whole meal D e c r e a s e d by unsifted flour i r o n Decreased

Wheat b r a n

Serum

i r o n Decreased

High f i b e r d i e t 6 months Vegans

H e m a t o l o g i c No e f f e c t

Authors, Ref. year

Fiber

Widdowson, 38 McCance 1942

Vellar 1968

et a l 42

Elwood e t al,1970 Hoglund 1970

43 44

45 Jenkins e t al,1975 Persson 46 e t al,1975 47 Brodribb e t al,1976 Sanders e t 48 al,1977 Dobbs e t a , l 49 1977 Sandstead 50 e t al,1977

source

Wholemeal bread,lOOg/day Wheat bran Corn b r a n (26 g/day)

Serum

effect

Negative correlation r= -0.92 Smaller r i s e i r o n f o r wholemeal b r e a d

Serum i r o n Normal etc. Decreased Whole body c o u n t No e f f e c t Balance No e f f e c t

Continued on next page.


154


Table II-continued. Authors, year Ref.

Criteria

O l s z o n e t a l 51 1978

High f i b e r

K e l s a y e t a l 52

Fruits,vegetabl e s , 23. 8g NDE/ day. P e c t i n 15g/day

Lei et a l 1980 Monnier e t al,1980 Downloaded by AUBURN UNIV on April 18, 2017 | http://pubs.acs.org Publication Date: November 1, 1982 | doi: 10.1021/bk-1982-0203.ch009

F i b e r source

53

14

Morris et a l 1980 54

diet

Pectin Cellulose Bran m u f f i n Dephytinized bran muffin, 36g bran/day Strained, pears

Oski e t a l 1980

55

Van Dokkum 1980

56

Increments o f bran

Faraji et al,1981

57

Bazari* Bazari + cellulose,lOg

Anderson e t al,1981

58

Bioavailability

Fecal Neg.correl. iron with fecal solids(fiber) B a l a n c e No e f f e c t

B a l a n c e No

effect

Uptake o f radioiron by r b c Uptake o f radioiron by r b c

Decreased No e f f e c t Decreased Decreased

Uptake o f D e c r e a s e d radioiron by r b c Iron Decreased excretion a t high intakes Balance Decreased Serum i r o n D e c r e a s e d Balance No e f f e c t Fecal iron Increased Serum i r o n D e c r e a s e d Hematolog- No e f f e c t ic

Vegetarian d i e t , 31 % fiber Godara e t 59 C e l l u l o s e , 2 1 g Balance Decreased al,1981 Serum i r o n D e c r e a s e d daily MacPhail e t Absorption ElevenWheat b r a n al,1981 60 added t o maize o f added fold iron decrease porridge with added f e r r o u s sulfate Simpson e t 61 Wheat b r a n Uptake o f D e c r e a s e al,1981 Dephytinized radioiron wheat b r a n Decrease Supernate o f latter Decrease *A f i b e r - r i c h I r a n i a n F l a t b r e a d s u p p l y i n g about 60% of t h e enrgy i n t a k e d u r i n g t h e s t u d y .


9.

REINHOLD


155

s u p e r n a t a n t s o l u t i o n r e s u l t i n g from d e p h y t i n i z a t i o n was somewhat more i n h i b i t o r y t h a n t h e f i b e r - c o n t a i n i n g residue. Under l e s s o p u l e n t c o n d i t i o n s t h a n t h e p r e c e d i n g A m e r i c a n s t u d i e s , F a r a j i e t a l (57) demonstrated a d -


verse e f f e c t s of h i g h f i b e r d i e t s i n the form of I r a n i a n f i b e r - r i c h f l a t b r e a d upon i r o n m e t a b o l i s m

Elwood e t a l (43) compared i r o n a b s o r p t i o n from c h a p a t t i s made from w h i t e f l o u r w i t h t h a t from c h a p a t t i s made from wholemeal f l o u r . A b s o r p t i o n from t h e l a t t e r was l o w e r . S i m i l a r l y , Dobbs and B a i r d (49) showed t h a t t h e p e r c e n t a g e or i r o n a b s o r b e d from w h i t e b r e a d was c o n s i d e r a b l y h i g h e r than t h a t a b s o r b e d f r o m wholemeal b r e a d . Serum i r o n c o n c e n t r a t i o n s d e c r e a s e d f o l l o w i n g i n g e s t i o n o f wheat b r a n ( J e n k i n s e t al,45) or wholemeal b r e a d as compared w i t h w h i t e b r e a d ( P e r s s o n e t a l , 4 6 ) . F o r t i f i e d w h i t e b r e a d produced a g r e a t e r r i s e i n serum i r o n c o n c e n t r a t i o n s t h a n d i d wholemeal b r e a d w i t h a s i m i l a r l e v e l of f o r t i f i c a t i o n ( V e l l a r e t a l , 42). High f i b e r d i e t s administered t o patients s u f f e r i n g from d i v e r t i c u l a r d i s e a s e d i d n o t lower hemoglobin c o n c e n t r a t i o n s o v e r a s i x month p e r i o d ( B r o d r i b b and Humphreys, 4 2 ) . P r o l o n g e d consumption o f v e g e t a r i a n d i e t s which a r e i n h e r e n t l y r i c h i n d i e t a r y f i b e r d i d n o t i m p a i r i r o n m e t a b o l i s m as judged by h e m a t o l o g i c c r i t e r i a (48,58). A common baby f o o d , s t r a i n e d p e a r s , i n h i b i t e d i r o n a b s o r p t i o n i n t h e p r e s e n c e o f human m i l k a c c o r d i n g t o O s k i and Landau ( 5 5 ) . A l t h o u g h t h e a u t h o r s d i d n o t a t t r i b u t e the a c t i o n t o d i e t a r y f i b e r , i t i s a p o s s i b l e suspect. Use o f an i n t u b a t i o n t e c h n i q u e e n a b l e d Matseshe e t a l . ( 6 2 ) t o show t h a t i r o n i n t r o d u c e d d i r e c t l y i n t o t h e s m a l l i n t e s t i n e o f human s u b j e c t s i n t h e p r e s e n c e o f c e r e a l s was r e c o v e r e d l e s s r a p i d l y and c o m p l e t e l y t h a n i r o n from f e r r o u s s u l f a t e o r r e d u c e d i r o n i n t h e p r e s e n c e o f meat. Bran caused an 1 1 - f o l d d e c r e a s e i n absorption of i r o n i n the s t u d i e s of McPhail e t a l ( 6 0 ) . T h i s impairment was not o b s e r v e d when i r o n was g i v e n i n t h e form o f F e ( I I I ) E D T A , a r e s p o n s e t h a t i s c o m p a t i b l e w i t h t h e a b i l i t y o f EDTA t o r e l e a s e i r o n from i t s combination w i t h d i e t a r y f i b e r . E x a m i n a t i o n o f t h e a b i l i t y o f i s o l a t e d f i b e r components t o i n t e r f e r e w i t h i r o n a b s o r p t i o n has y i e l d e d


156


c o n f l i c t i n g r e s u l t s * Godara e t a l * ( 5 9 ) f e d 21 g o f c e l l u l o s e d a i l y f o r 21 days, A s i g n i f i c a n t d e c r e a s e i n i r o n b a l a n c e and serum i r o n c o n c e n t r a t i o n s o c c u r r e d . In the e x p e r i m e n t s o f F a r a j i e t a l ( 5 2 ) h a l f as much c e l l u l o s e f a i l e d t o produce s i g n i f i c a n t changes i n i r o n b a l a n c e , a l t h o u g h serum i r o n c o n c e n t r a t i o n s f e l l . T h e r e i s no agreement, a l s o , c o n c e r n i n g the a c t i o n o f p e c t i n . Thus, Monnier e t a l (14) r e p o r t e d a d e c r e a s e d r a d i o a c t i v e i r o n uptake accompanying p e c t i n ingestion, w h i l e L e i e t a l (53) saw no change i n i r o n b a l a n c e t o be a s s o c i a t e d w i t h p e c t i n a d m i n i s t r a t i o n . Downloaded by AUBURN UNIV on April 18, 2017 | http://pubs.acs.org Publication Date: November 1, 1982 | doi: 10.1021/bk-1982-0203.ch009

#

E s t i m a t i o n o f the amount o f in cereal-rich diets

i r o n complexed by

fiber

The p r o p o r t i o n o f d i e t a r y i r o n bound by d i e t a r y f i b e r may be e s t i m a t e d by use o f the c o e f f i c i e n t s (13) d e s c r i b e d i n the S e c t i o n : A f f i n i t y o f f i b e r f o r i r o n . Such e s t i m a t e s are a p p l i c a b l e t o t h e numerous p o p u l a t i o n s t h a t d e r i v e major p o r t i o n s o f t h e i r d i e t s f r o m wheat and maize. Thus, i n C e n t r a l Mexico t h e median d a i l y consumption of maize has been e s t i m a t e d t o p r o v i d e 14 g of NDF (63). T h i s f i g u r e m u l t i p l i e d by 0.30, t h e c o e f f i c i e n t f o r maize NDF, y i e l d s 4.2mg o f i r o n bound by t h e NDF. W i t h a d a i l y i n t a k e o f 19 mg o f i r o n i n t h i s r e g i o n o f Mexico, the amount complexed i s t r i v i a l , p a r t i c u l a r l y s i n c e consumption of p r o t e c t i v e f o o d s , i n c l u d i n g f r u i t s and v e g e t a b l e s , i s a p p r e c i a b l e . H o w e v e r , i n r u r a l I r a n , NDF i n t a k e s i n the form

o f unleavened f l a t wheaten b r e a d s may exceed 50 g d a i l y . F i f t y g m u l t i p l i e d by the c o e f f i c i e n t f o r NDF o f wheat, 0.38, g i v e s 19mg o f bound i r o n , a f i g u r e t h a t would d e c r e a s e a v a i l a b l e i r o n s u b s t a n t i a l l y , a l though i r o n i n t a k e s i n I r a n t e n d t o be h i g h (64). However, consumption o f p r o t e c t i v e f o o d s i s l i k e l y t o be low because o f g e o g r a p h i c , s e a s o n a l and economic restraints. In a d d i t i o n t o t h e complexant a c t i o n o f f i b e r , i t s h o u l d be r e c a l l e d t h a t o t h e r a c t i o n s , e.g. changes i n t h e p h y s i o l o g i c a l b e h a v i o r o f t h e gut and i n c r e a s e d p r o l i f e r a t i o n o f gut f l o r a , may promote l o s s e s o f i r o n .


9. REINHOLD


Further


157

studies

A d d i t i o n a l measurements o f t h e c o e f f i c i e n t s o f i r o n b i n d i n g by d i e t a r y f i b e r s from v a r i o u s s o u r c e s a r e needed, p a r t i c u l a r l y because t h e p u b l i s h e d c o e f f i c i e n t s a r e based on s i n g l e samples o f wheat and maize b r a n s . The need i s made g r e a t e r by t h e f i n d i n g o f Thompson e t a l (65) t h a t method o f f i b e r p r e p a r a t i o n a f f e c t ed i o n exchange c a p a c i t y f o r copper and z i n c . I t would be h e l p f u l t o l e a r n i f i r o n i s s i m i l a r l y a f f e c t e d . F u r t h e r s t u d i e s o f t h e importance o f t h e p r o t e i n t h a t a p p e a r s t o be an i n t r i n s i c component o f some d i e t a r y f i b e r s i n b i n d i n g o f i r o n and o t h e r c a t i o n s a r e needed. The e x t e n t o f b i n d i n g o f f e r r i c i r o n by d i e t a r y f i b e r s needs t o be e v a l u a t e d . Measurements o f i r o n b i n d i n g by v a r i o u s d i e t a r y f i b e r s i n v i v o l i k e t h o s e done b y F e r n a n d e z a n d P h i l l i p s (69) u s i n g i s o l a t e d s e g m e n t s o f i n t e s t i n e i n s i t u

would a s s i s t i n the a p p r a i s a l o f t h e extent o f i n t e r ference w i t h i r o n absorption. Balance studies o f l a r g e r omnivera a l s o a r e needed. Further studies of the e f f e c t s of dietary f i b e r f r o m v a r i o u s s o u r c e s upon i r o n u t i l i z a t i o n by human s u b j e c t s a r e n e c e s s a r y . Some e x i s t i n g s t u d i e s a r e i n c o n c l u s i v e because o f t h e i r s h o r t d u r a t i o n ; o t h e r s because o f t h e s m a l l samples s t u d i e d . Long term s t u d i e s o f t h e f i b e r - r i c h , low energy d i e t s o f many l e s s d e v e l o p e d r e g i o n s would a l s o be i m p o r t a n t f o r e v a l u a t i o n o f t h e iron deficiency that often p r e v a i l s . Acknowledgements I thank my w i f e , S a l l y Edwards R e i n h o l d , f o r h e l p i n r e v i e w i n g t h e l i t e r a t u r e and M i s s J u d i t h B a r b a f o r typing the manuscript. Addenda S e v e r a l r e l e v a n t s t u d i e s have appeared s i n c e t h e m a n u s c r i p t was completed. R a n h o t r a e t al«(66) examined the a v a i l a b i l i t y o f the i r o n of f i v e types o f I r a n i a n f l a t b r e a d s t o r a t s by use o f t h e hemoglobin r e p l e t i o n method. They f o u n d no d i r e c t r e l a t i o n s h i p t o c o n t e n t o f f i b e r ( o r p h y t a t e o r p r o t e i n ) . Wiemer



158


and Kies (67) observed that the addition of hemicellulose in the form of psyllium to the diets of weanling mice increased iron losses in feces. Fernandez and P h i l l i p s (68) measured the binding of iron i n v i t r o by l i g nin, hemicellulose (psyllium mucilage), pectin and alpha c e l l u l o s e . A f f i n i t i e s for iron of the f i r s t two substances were high, that of pectin less, and that of the cellulose negligible. Citrate and EDTA inhibited binding. In further studies made i n vivo, l i g n i n and hemicellulose introduced into duodenal jejunal segments of dogs were potent inhibitors of iron absorption. Pectin was less inhibitory and alpha cellulose was ineffective (69). Literature cited 1. Eastwood,M.A.; Kay,R.M. Am.J.Clin.Nutr.1979,32,364 2. Reinhold,J.G.; I s m a i l - B e i g i , F . ; F a r a j i , B . Nutr. Rep.Int. 1975, 12,75. 3. I s m a i l - B e i g i , F . ; F a r a j i , B . ; Reinhold,J.G.Am.J.Clin Nutr. 1977, 30, 1721. 4. Van Soest,P.J. J.Assoc.Off.Anal.Chem. 1963, 46, 825. 5. Robertson,J.B.; Van Soest,P.J. Proc.69th.Meeting Am. Soc. Animal Sci., Madison,Wisconsin, 1977. 6. Van Soest,P.J.; Robertson,J.B. Nutr.Rev. 1977, 35, 12. 7. Cummings,J.H. in Fiber in Human N u t r i t i o n . S p i l l e r , G.A.; Amen,R.J., eds. Plenum Press, New York, 1976, p.1. 8. Southgate, D.A.T. in Fiber in Human N u t r i t i o n . S p i l l e r , G . A . ; Amen,R.J.,eds.Plenum Press, New York, 1976, p.31. 9. Reinhold,J.G.; Nasr,K.; Lahimgarzadeh,A.; Hedayati, H. Lancet 1973, 1, 283. 10.Reinhold,J.G.; F a r a j i , B . ; Abadi,P.; Ismail-Beigi,F. in Trace Elements in Human Health and Disease. Prasad, A . S . , e d . Academic Press, New York, 1976, 1, 163. 1 1 . R e i n h o l d , J . G . ;Parsa,A.: K a r i m i a n , N . ; Hammick,J.W.; Ismail-Beigi,F. J.Nutr. 1974, 105, 976. 1 2 . C a m i r e , A . L . ;Clydesdale,F.M. J.Food S c i . 1981, 46, 548. 13.Reinhold,J.G.; Garcia L.,J.S.; Garzón,P. Am.J.Clin. Nutr. 1981, 34, 1384.



9.

REINHOLD


159

14.Monnier,L.; Coletti,C.; Aguirre,L.;Miranze,J. Am.J. Clin. Nutr. 1980, 33, 1225. 15.Mod,R.R.; Ory,R.L.; Morris,N.M.; Normand,F.L. J.Agric. Food Chem. 1981, 29, 449. 16.Thompson,S.A.; Weber,C.W. J.Food Sci. 1979, 44,752. 17.Reilly,C. Biochem.Soc.Trans. 1979,9,202. 18.Reinhold,J.G.; García-L,P.M.; Arias-Amado,L.; Garzón, P. 1982, in Dietary Fiber in Health and Disease. G.V.Vahouny and Kritchevsky,D.,eds. Plenum Publ.Co., New York, N.Y. p.117. 19.Kojima,N.; Wallace,O.; Bates,G.W. Am.J.Clin.Nutr. 1981, 34, 1392. 20.Harris,D.C.; Aisen,P. Biochim.Biophys.Acta. 1973,329, 156. 21.Nojeim,S.J.; Clydesdale,F.M. J.Food Sci. 1981, 46, 606. 22.Lee,B.A.; Oace,S.J. Fed.Proc. 1980,39,785. 23.Stiles,L.W.; Rivers,J.M.; Hackler,L.R.; Van Campen, D.R. Fed.Proc. 1976, 35, 744. 24.Ranhotra,G.S.; Lee,C.; Gelroth,J.A. Cereal Chem.1979, 56,156. 25.Lee,C.; Gelroth,J.A.; Ranhotra,G.S. Fed.Proc. 1979, 38,473. 26.Miller,J. Cereal Chem. 1979, 56, 253. 27.Spiller,G.A.; Chernoff,M.C.; Gares,J.E. Nutr.Rep.Int. 1980, 22, 353. 28.Harmuth-Hoene,A.E.; Schelenz,R. J.Nutr.1980, 110, 1774. 29.Woelbling,R.H.; Becker,G.; Forth,W. Digestion 1980, 20,403. Chem.Abst. 1980, 93, 230987. 30.Becker,G.; Osterlok.; Schaefer,W.; Forth,W.; PaskinsHurlburt,A.J.; Tanaka,G.; Skoryna,S.C. Digestion 1981 21,6. Chem.Abst. 1980, 93, 216024. 31.Thompson,S.A.; Weber,C.W. Poultry Sci. 1981, 60,840. 32.Harmuth-Hoene,A.E.; Schelenz,R.; Fretzdorff,B.: Rabe,E.; Seibel,W. Getreide,Mehl.,Brot.1981,35,65. Chem.Abst. 1981,94, 190712. 33.García-Lopez,J.S.; Wyatt,J. Private Communication. 1981. 34.Morris,E.R.; Ellis,R. J.Nutr. 1980,110,2000 35.Liebman,M.; Driskell,J. Nutr.Rep.Int. 1979, 19, 281. 36.Hunter,J.E. J.Nutr.1981, 111, 841. 37.Cowan,J.W.; Esfahani,M.; Salji,J.D.; Azzam,S.A. J.Nutr. 1966, 90, 423.



160


38.Widdowson,E.M.; McCance,R.A. Lancet 1942, 1, 588. 39.Walker,A.R.P.; Fox,F.W.; Irving,J.T. Biochem.J. 1948, 42,452. 40.Cullumbine,H.; Basnayake,V.; Lemottee,J.; Wickramanayake,T.W. Br.J.Nutr.1950, 4, 101. 41.Björn-Rasmussen,E. Nutr.Metab. 1974,16,101. 42.Vellar,O.D.; Borchgrevink,C.; Natvig,H. Acta Med. Scand. 1968, 183, 251. 43.Elwood,P.C., Benjamin,I.T., Fry,F.A.; Eakins,J.O.; Brown,D.A.; de Koch,P.C.; Shah, J.V. Am.J.Clin.Nutr. 1970, 23,1267. 44.Hoglund,S. Acta Med.Scand.Suppl. 1970, 518,1. 45.Jenkins,P.J.A.; Hill,M.S.; Cummings,J.H. Am.J.Clin. Nutr. 1975, 28, 1408. 46.Persson,L.; Raby,K.; Fonns-Bech,P.; Jensen,E. Lancet 1975, 2, 1208. 47.Brodribb,A.J.M.; Humphreys,D.M. Br.Med.J. 1976, 1, 424. 48.Sanders,T.A.B.; E l l i s , F . R . Br.Med.J.1977,2,636. 49.Dobbs,R.J.; Baird,I.M. Br.Med.J. 1977,1,1641. 50.Sandstead,H.H.; Muñoz,J.M.; Jacob,R.A.; Klevay,L.M.; Reck,S.J.; Logan,Jr.,G.M.; Dintzis,F.R.; Inglett,G. E.; Shuey,W.C. Am.J.Clin.Nutr. 1978,31,S180. 51.Olzson,E.; Isaksson,B.; Nörrby,A.; S o l v e l l , L . Am.J. Clin.Nutr.1978, 31, 106. 52.Kelsay,J.L.; Behall,K.M.; Prather,E.S. Am.J.Clin. Nutr. 1979, 32, 1876. 53.Lei,K.Y.; Davis,M.W.; Fang,M.M.; Young,L.C. Nutr.Rep. Int. 1980, 22, 459. 54.Morris,E.R.; Simpson,K.M.; Cook,J.D. Am.J.Clin.Nutr. 1980, 33, 941. 55.Oski,F.A.; Landow,S.A. Am.J.Dis.Child. 1980, 134,459. 56.Van Dokkum,W. Ber.Int.Ges.Getreidechem. 1980, 10,207. Chem.Abst.1981, 94, 207584. 57.Faraji,B.; Reinhold,J.G.; Abadi,P. Nutr.Rep.Int. 1981,23,267. 58.Anderson,B.M.; Gibson,E.S.; Sabry,J.H. Am.J.Clin. Nutr. 1981,34,1042. 59.Godara,R.; Kaur,A.P.; Bhat,C.M. Am.J.Clin.Nutr. 1981, 34,1083. 60.MacPhail,A.P.; Bothwell,T.H.; Torrance,J.D.; Derman, D.P.; Beswoda,W.R.; Charlton,R.W.; Mayat,F. B r . J . Nutr. 1981, 45,215.



9.

REINHOLD


161

61.Simpson,K.M.; Morris,E.R.; Cook,J.D. Am.J.Clin.Nutr. 1981, 34, 1469. 62.Matseshe,J.W.; P h i l l i p s , S . F . ; Malegalada,J.-R.; McCall,J.T. Am.J.Clin.Nutr. 1980, 33, 1946. 63.Reinhold,J.G.; Garcia L., J.S.; Am.J.Clin.Nutr. 1979 32,1326. 64.Haghshenass,M.; Mahloudji,M.; Reinhold,J.G.;Mohamadi, M. Am.J.Clin.Nutr. 1972, 25, 1143. 65.Thompson,S.A.; Weber,C.M.; Berry,J.W. Fed.Proc. 1980 39,785. 66.Ranhotra,G.S.; Gelroth,J.A.; Torrence,F.A.: Bock, M.A.; Winterringer,G.L.; Faridi,H.A.; Finney,P.L. Cereal Chem. 1981, 58, 471. Chem.Abst.1981,95, 167422. 67.Wiemer,K.; Kies,C. Nutr.Rept.Int. 1981 24, 165. 68.Fernandez ,R.; P h i l l i p s , S . F . Am.J.Clin.Nutr. 1982, 35,100 69.Fernandez,R.; P h i l l i p s , S . F . Am.J.Clin.Nutr. 1982, 35,107 RECEIVED August 13, 1982.


Dietary Fiber and the Bioavailability of Iron - ACS Symposium Series

Recommend Documents