9 Dietary Fiber and the Bioavailability of Iron JOHN G. REINHOLD
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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.
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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.
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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
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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 ,
Kies; Nutritional Bioavailability of Iron ACS Symposium Series; American Chemical Society: Washington, DC, 1982.
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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 .
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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
Kies; Nutritional Bioavailability of Iron ACS Symposium Series; American Chemical Society: Washington, DC, 1982.
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differed
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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 ) .
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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.
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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.
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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 .
Kies; Nutritional Bioavailability of Iron ACS Symposium Series; American Chemical Society: Washington, DC, 1982.
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Effect of Dietary Fiber
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
Kies; Nutritional Bioavailability of Iron ACS Symposium Series; American Chemical Society: Washington, DC, 1982.
NUTRITIONAL BIOAVAILABILITY OF IRON
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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
Kies; Nutritional Bioavailability of Iron ACS Symposium Series; American Chemical Society: Washington, DC, 1982.
page.
9. REINHOLD
Effect of Dietary Fiber
Table I-continued. Authors, Ref. Animal year
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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.
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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
Kies; Nutritional Bioavailability of Iron ACS Symposium Series; American Chemical Society: Washington, DC, 1982.
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REINHOLD
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153
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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.
Kies; Nutritional Bioavailability of Iron ACS Symposium Series; American Chemical Society: Washington, DC, 1982.
154
NUTRITIONAL BIOAVAILABILITY OF IRON
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 .
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9.
REINHOLD
Effect of Dietary Fiber
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 -
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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
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NUTRITIONAL BIOAVAILABILITY OF IRON
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 .
Kies; Nutritional Bioavailability of Iron ACS Symposium Series; American Chemical Society: Washington, DC, 1982.
9. REINHOLD
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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
Kies; Nutritional Bioavailability of Iron ACS Symposium Series; American Chemical Society: Washington, DC, 1982.
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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.
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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.
Kies; Nutritional Bioavailability of Iron ACS Symposium Series; American Chemical Society: Washington, DC, 1982.
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REINHOLD
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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.
Kies; Nutritional Bioavailability of Iron ACS Symposium Series; American Chemical Society: Washington, DC, 1982.