Zinc Bioavailability from Vegetarian Diets - ACS Symposium Series

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Zinc Bioavailability from Vegetarian Diets Influence of Dietary Fiber, Ascorbic Acid, and Past Dietary Practices C. KIES, E. YOUNG, and L. McENDREE University of Nebraska, Lincoln, NE 68583

Differences in food consumption patterns may result not only in changes in nutrient consumption patterns but also, directly or indirectly, in the availability of these nutrients. In a preliminary evaluation zinc utilization by omnivore (plant and animal product eaters) and vegetarian subjects consuming laboratory controlled vegetarian diets were compared. Fecal zinc excretions and zinc balances of subjects indicated better utilization of zinc from the vegetarian diets by the practicing vegetarian subjects than by the omnivore subjects consuming the vegetarian diets. While both fiber and ascorbic acid additions tended to decrease zinc utilization by omnivores and by vegetarians, the effect was less pronounced with the vegetarians than with the omnivores. This suggests that with time adaptation may have occurred. However, all subjects responded in a directionally similar manner to experimental variables of ascorbic acid and fiber supplementation. Historically, the first human zinc-responsive syndrome was recognized in 1961 by Prasad (1,2) in Egyptian boys whose diets were composed largely of bread and beans. Zinc deficiency in these patients, characterized by dwarfism and hypogonadism, responded to zinc supplementation. Analysis of the food consumed by the human patients suggested i t contained adequate zinc. Pigs also developed zinc deficiency symptoms when fed similar diets even though rations contained adequate zinc as judged by requirements set using purified rations (3). One factor common to both

0097-6156/83/0210-0115$06.00/0 © 1983 American Chemical Society Inglett; Nutritional Bioavailability of Zinc ACS Symposium Series; American Chemical Society: Washington, DC, 1983.

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s i t u a t i o n s was the consumption of foods l a r g e l y of p l a n t o r i g i n , c e r e a l s and legumes w i t h l i t t l e or no animal products. I t has g e n e r a l l y been concluded that the d e f i c i e n c i e s must have r e s u l t e d from a decreased a v a i l a b i l i t y of d i e t a r y z i n c or an a c c e l e r a t e d l o s s of z i n c from the body or both. These f i n d i n g s have i m p l i c a t i o n s f o r z i n c n u t r i t i o n of a l l c l a s s e s of v e g e t a r i a n s . T h e o r e t i c a l l y , as omnivore d i e t s which contain v a r i a b l e amounts of meat and vegetable products become l e s s meat o r i e n t a t e d and more p l a n t product o r i e n t a t e d , the p o s s i b i l i t i e s of inadequacies i n z i n c n u t r i t i o n become greater. As reviewed r e c e n t l y by Solomons ( 4 ) , many d i e t a r y and nond i e t a r y f a c t o r s may a f f e c t the b i o a v a i l a b i l i t y of z i n c . Dietary f a c t o r s are subdivided i n t o " i n t r i n s i c f a c t o r s " and " e x t r i n s i c f a c t o r s " . " I n t r i n s i c f a c t o r s " r e l a t e to the chemical nature of z i n c i t s e l f . " E x t r i n s i c f a c t o r s " i n c l u d e non-heme i r o n , e t h y l enediaminetetraacetic a c i d (EDTA), d i e t a r y f i b e r , p h y t i c a c i d , calcium, copper and s p e c i f i c foods such as cow's m i l k , cheese, c o f f e e , eggs, c e l e r y and lemon which have been demonstrated to decrease z i n c b i o a v a i l a b i l i t y as w e l l as other f a c t o r s which may increase z i n c u t i l i z a t i o n . G e n e r a l l y foods of animal o r i g i n have been found to be higher i n z i n c content than those of p l a n t o r i g i n (5,7). Legumes, whole g r a i n s , and l e a f y vegetables may contain s i g n i f i c a n t amounts of z i n c but the z i n c content of most f r u i t s and vegetables i s q u i t e modest (6). Processing of raw products a l s o may have an adverse e f f e c t on the z i n c content of foods. White bread contains about one-fourth of the z i n c o r i g i n a l l y present i n the u n r e f i n e d wheat, the z i n c content of degermed corn meal i s roughly one-half that i n dry corn, and precooked, quick p o l i s h e d r i c e (dry) contains l e s s than o n e - t h i r d the amount of z i n c of unprocessed g r a i n C5). Zinc a b s o r p t i o n from a number of food substances, p a r t i c u l a r l y those of p l a n t o r i g i n s , has been questioned. Found w i d e l y d i s t r i b u t e d i n foods of p l a n t o r i g i n , phytate has been demons t r a t e d to be a c h e l a t i n g agent complexing w i t h z i n c to form a compound i n s o l u b l e at normal i n t e s t i n a l pH. Evidence i n d i c a t e s that phytate impairs both the a b s o r p t i o n of d i e t a r y z i n c and the r e a b s o r p t i o n of endogenously secreted z i n c (3,8,9). Excessive d i e t a r y calcium i n the presence of phytate has been found to have p a r t i c u l a r l y adverse e f f e c t s on z i n c a b s o r p t i o n (8). Since high l e v e l s of phytate and h i g h l e v e l s of f i b e r tend to occur s i m u l taneously i n foods, the r e l a t i v e i n f l u e n c e of these two f a c t o r s has been d i f f i c u l t to separate. Recently, i t has been reported that non-heme but not heme i r o n adversely a f f e c t s z i n c a b s o r p t i o n (10). Since f i b e r , phytate and non-heme i r o n are l i k e l y to be supplied i n l a r g e r amounts i n v e g e t a r i a n than i n omnivore d i e t s , i t would be assumed that the z i n c content of v e g e t a r i a n d i e t s i s l e s s w e l l u t i l i z e d than that of omnivore d i e t s .

Inglett; Nutritional Bioavailability of Zinc ACS Symposium Series; American Chemical Society: Washington, DC, 1983.

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Zinc Bioavailability from Vegetarian Diets

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Zinc N u t r i t i o n a l Status of Vegetarians R e l a t i v e l y few d i e t a r y surveys of n u t r i e n t i n t a k e s of veget a r i a n s have i n c l u d e d a c a l c u l a t i o n of z i n c i n t a k e s . Handbook a n a l y t i c a l values f o r z i n c contents of a wide v a r i e t y of food substances have only r e c e n t l y become a v a i l a b l e which may i n p a r t account f o r t h i s omission. Zinc s t a t u s of 49 Seventh Day A d v e n t i s t Canadian women who had been consuming v e g e t a r i a n d i e t s f o r an average of 19 ± 17 years were reported by Anderson e t a l . (11). As c a l c u l a t e d from 3-day d i e t a r y d i a r i e s , mean d i e t a r y f i b e r i n t a k e of t h i s group was 30.9 ± 110 g/day, which i s r e l a t i v e l y h i g h , and the mean z i n c intake was 9.2 ± 2.5 g/day, which i s considerably l e s s than the NRC RDA recommendation of 15 mg/day. Furthermore, 82% of the z i n c i n t a k e came from products of p l a n t o r i g i n i n c l u d i n g 26% from d r i e d legumes, nuts and soy products. Never-the-less, blood serum z i n c l e v e l s (99.3 ± 23.9 ug/dl) and h a i r z i n c l e v e l s (L87 ± 44 ug/g) were w e l l w i t h i n normal l e v e l s . Thus, i n s p i t e of low z i n c i n t a k e w i t h z i n c s u p p l i e d l a r g e l y from foods b e l i e v e d t o c o n t a i n z i n c of low b i o a v a i l a b i l i t y , those women were seemingly i n adequate z i n c n u t r i t i o n a l s t a t u s . Zinc i n t a k e s of 6 Swedish vegans ( i n d i v i d u a l s who consume no food of animal o r i g i n at a l l ) u s i n g chemical analyses of d i e t s from a d u p l i c a t e p o r t i o n sampling technique approach were i n c l u d e d i n a study by A b d u l l a e t a l . (12). D i e t a r y f i b e r i n t a k e of male subjects was 62 ± 9 g/day and t h a t of female s u b j e c t s was 43 ± 9 g/day. Zinc i n t a k e of male s u b j e c t s was 13 ± 2.3 mg/day and that of female subjects was 6.5 ± 1.3 mg/day, so as i n the study of lacto-ovo-vegetarians by Anderson e t a l . , s u b j e c t s were found t o have r e l a t i v e l y high i n t a k e s of f i b e r and r e l a t i v e l y low i n t a k e s of z i n c w i t h the z i n c that was s u p p l i e d being from foods b e l i e v e d to e x h i b i t low z i n c b i o a v a i l a b i l i t y . Zinc i n t a k e s and consumption of s e v e r a l other n u t r i e n t s using three-day d i a r i e s were determined f o r 12 pregnant ovo-lacto-veget a r i a n women, 5 non-pregnant o v o - l a c t o - v e g e t a r i a n women, and 6 pregnant omnivore women by King e t a l . (13). These were compared to s e v e r a l parameters of z i n c n u t r i t i o n a l s t a t u s . Energy i n t a k e of the non-pregnant v e g e t a r i a n women was much lower f o r t h i s group than f o r the pregnant v e g e t a r i a n or pregnant omnivore groups (1329 vs. 2446 vs. 2003 kcal/day, r e s p e c t i v e l y ) . Zinc i n t a k e s from food f o r these three groups (non-pregnant v e g e t a r i a n , pregnant v e g e t a r i a n and pregnant omnivores) were 6.4, 12.4, and 14.4 mg/day, r e s p e c t i v e l y ; and from food p l u s z i n c supplements were 6.4, 29.6 and 16.1 mg/day, r e s p e c t i v e l y . U r i n a r y z i n c e x c r e t i o n l e v e l s roughly followed the z i n c i n t a k e p a t t e r n being 0.17, 0.34 and 0.41 mg/g c r e a t i n i n e , r e s p e c t i v e l y , f o r the three groups. H a i r z i n c l e v e l s were approximately the same f o r a l l three groups. However, blood plasma z i n c l e v e l s f o r the nonpregnant v e g e t a r i a n s , the pregnant vegetarians and the pregnant omnivores were 80, 60 and 66 u g / d l , r e s p e c t i v e l y , suggesting that

Inglett; Nutritional Bioavailability of Zinc ACS Symposium Series; American Chemical Society: Washington, DC, 1983.

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t h i s parameter of z i n c s t a t u s was more a f f e c t e d by pregnancy than by l e v e l of z i n c i n t a k e or by source o f d i e t a r y z i n c . In a study conducted i n t h i s l a b o r a t o r y , 23 Seventh Day A d v e n t i s t students were s u b j e c t s ; 14 claimed t o be vegetarians and 9 claimed t o be omnivores (14,15). A l l were students a t Union C o l l e g e - L i n c o l n , Nebraska, a Seventh-Day A d v e n t i s t i n s t i t u t i o n , and consumed most meals (and other food) a t the Union College c a f e t e r i a which i s operated as a l a c t o - o v o - v e g e t a r i a n food s e r v i c e . Subjects consumed s e l f - s e l e c t e d d i e t s . M a t e r i a l s c o l l e c t e d i n c l u d e d 3-day d i e t a r y d i a r i e s kept by the s u b j e c t s themselves, samples of a l l foods served i n the food s e r v i c e u n i t and s e r v i n g s i z e s of a l l foods served, and f a s t i n g blood samples during the study p e r i o d from a l l s u b j e c t s . Zinc contents of food samples and blood serum samples were analyzed by atomic a b s o r p t i o n spectrophotometry u s i n g a V a r i a n Techtron Atomic Absorption Spectrophotometer. D i e t a r y z i n c i n t a k e was c a l c u l a t e d f o r each subject using the 3-day d i e t a r y d i a r y i n f o r m a t i o n and a n a l y t i c a l data from food sample analyses. Handbook i n f o r m a t i o n was used f o r foods not consumed a t the Union C o l l e g e c a f e t e r i a (5-7). As shown i n Table I , the mean z i n c i n t a k e s of the v e g e t a r i a n s u b j e c t s was found t o be 8.49 mg/day ± 2.35 and that of the omnivores was 8.09 mg/day ± 2.30. Although the ranges i n i n t a k e i n both groups were great, 4.78 - 14.89 mg f o r the vegetarians and 5.09 - 11.31 mg f o r the omnivore group, not a s i n g l e subject had a 3-day mean i n t a k e of z i n c which met o r exceeded 100% of the NRC RDA's of 15 mg/day. Approximately one-half of the s u b j e c t s i n both groups had 3-day mean values of l e s s than 50% of the NRC RDA's f o r z i n c f o r the age/sex group i n v e s t i g a t e d . Thus, i t would appear that some r i s k o f z i n c d e f i c i e n c y f o r these i n d i v i duals might e x i s t . Mean blood serum z i n c l e v e l s of the v e g e t a r i a n subjects was 75.5 ug/dl ± 4.81 w i t h a range of 67.9 - 86.0 ug/dl and that f o r the omnivore subjects was 72.6 ug/dl ± 5.70 w i t h a range of 64.8 83.1 u g / d l . Blood serum z i n c l e v e l s were weakly p o s i t i v e l y c o r r e l a t e d w i t h i n t a k e l e v e l s but w i t h the number of subjects i n v o l v e d , t h i s c o r r e l a t i o n was not s t a t i s t i c a l l y s i g n i f i c a n t . While the mean values were w i t h i n normal ranges f o r blood serum z i n c l e v e l s , some i n d i v i d u a l values f e l l s l i g h t l y below the 70 ug/dl lower acceptable l e v e l . Thus, blood serum z i n c l e v e l s f o r both groups could be s a i d t o be only m a r g i n a l l y acceptable. The omnivore s u b j e c t s tended t o have s l i g h t l y lower blood serum z i n c l e v e l s j u s t as they tended t o have s l i g h t l y lower i n t a k e l e v e l s of z i n c . I t i s important t o r e s t r e s s that these i n d i v i d u a l s were omnivores ( s e l f - d e s i g n a t e d ) who a c t u a l l y were consuming very l i t t l e meat a t the time the study was conducted. I t would appear on the b a s i s of r e s u l t s of these four s t u d i e s t h a t vegetarians tend t o have low z i n c i n t a k e l e v e l s . Furthermore, most of the z i n c i n these d i e t s appears t o be provided from foods w i t h low z i n c b i o a v a i l a b i l i t y . Never-the-less,

Inglett; Nutritional Bioavailability of Zinc ACS Symposium Series; American Chemical Society: Washington, DC, 1983.

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z i n c n u t r i t i o n a l s t a t u s as judged by biochemical parameters appeared t o be i n the normal range. Table I Zinc Status of Vegetarians and Omnivores 7th Day A d v e n t i s t Students E a t i n g i n a Lacto-Ovo-Vegetarian Food S e r v i c e Mean values Vegetarians Omnivores

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No. of s u b j e c t s Zn i n t a k e , mg/day

14 8.49

Standard d e v i a t i o n Range % below 50% RDA % above 75% RDA % above 100% RDA

±2.35 4.78-14.89 48 26 0

Blood serum Zn, ug/dl

75.5 ±4.81 67.9-86.0

Standard d e v i a t i o n Range

9 8.09 ±2.30 5.09-11.31 53 9 0 72.6 ±5.70 64.8-83.1

Comparative Zinc U t i l i z a t i o n by Vegetarians and Omnivores Vegetarian d i e t s tend to provide z i n c i n lower amounts than that present i n omnivore d i e t s . Furthermore, z i n c provided by foods from vegetable o r i g i n s tends t o be l e s s a v a i l a b l e than that provided by foods of animal o r i g i n . E f f e c t of feeding a l a c t o - o v o - v e g e t a r i a n d i e t on z i n c s t a t u s was s t u d i e s by Freeland e t a l . (16). F o l l o w i n g feeding of a l a c t o - o v o - v e g e t a r i a n d i e t f o r three weeks, z i n c a b s o r p t i o n was measured i n 11 females. Zinc a b s o r p t i o n was determined by z i n c t o l e r a n c e t e s t s i n plasma and s a l i v a a f t e r i n g e s t i o n of 50 mg z i n c s u l f a t e p r i o r t o and a t the end of d i e t a r y treatment. The z i n c content of the s u b j e c t s s a l i v a s i g n i f i c a n t l y decreased from the i n i t i a l average of 131 ppm to an average of 92 ppm. Plasma l e v e l s showed a tendency to decrease. These changes i n d i c a t e that a v e g e t a r i a n d i e t may reduce z i n c a b s o r p t i o n . The o b j e c t i v e of a p r o j e c t conducted i n t h i s l a b o r a t o r y was to determine whether o r not v e g e t a r i a n s u b j e c t s and omnivore subjects u t i l i z e z i n c t o a s i m i l a r degree when f e d l a b o r a t o r y c o n t r o l l e d v e g e t a r i a n d i e t s (14,15). This was a composited p r o j e c t i n v o l v i n g the recombination of data from s e v e r a l s t u d i e s . Because of the considerable numbers of Seventh-Day A d v e n t i s t s who r e s i d e i n L i n c o l n , because of the l o c a t i o n of Union C o l l e g e , a Seventh-Day A d v e n t i s t i n s t i t u t i o n , 1

Inglett; Nutritional Bioavailability of Zinc ACS Symposium Series; American Chemical Society: Washington, DC, 1983.

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or because of i n t e r e s t of Seventh-Day A d v e n t i s t s i n n u t r i t i o n and human h e a l t h , we f i n d that a number of v e g e t a r i a n s , p r i m a r i l y Seventh-Day A d v e n t i s t s , a r e v o l u n t e e r i n g as d i e t s u b j e c t s f o r our general human n u t r i t i o n metabolism s t u d i e s . On the surface i t might seem a d v i s a b l e t o bar p a r t i c i p a t i o n of these i n d i v i d u a l s i n order t o reduce v a r i a b i l i t y w i t h i n each experimental group popu l a t i o n , but f o r e t h i c a l , l e g a l and p r a c t i c a l reasons t h i s approach was not r e a l l y a v i a b l e o p t i o n . I n the current p r o j e c t , data were drawn from s e v e r a l s t u d i e s during which s i m i l a r but not i d e n t i c a l v e g e t a r i a n d i e t s were f e d f o r 21-28 days. While object i v e s of these s t u d i e s v a r i e d and d i f f e r e n t experimental v a r i a b l e s i n the form of supplements were given, data were drawn from c o n t r o l periods during which no supplements were given. Data f o r 12 vegetarians and 12 omnivores were used. A l l foods f e d were sampled. Complete u r i n e and s t o o l c o l l e c t i o n s were made. Zinc content o f u r i n e , feces and food were determined by atomic a b s o r p t i o n spectrophotometry. Mean z i n c i n t a k e s v a r i e d s l i g h t l y between the two groups being 8.32 mg/day f o r the v e g e t a r i a n group and 8.86 mg/day f o r the omnivore group. Zinc i n t a k e s a l s o v a r i e d somewhat among s u b j e c t s w i t h i n each group. This v a r i a t i o n was i n part due t o v a r i a t i o n i n food i n t a k e because of d i f f e r e n c e s i n c a l o r i c i n t a k e of the subjects and i n part due t o v a r i a t i o n i n z i n c content of the d i f f e r e n t b a s a l d i e t s used i n the d i f f e r e n t s t u d i e s . I n any case, z i n c i n t a k e was m a r g i n a l l y low i n comparison t o NRC RDA s f o r z i n c (15 mg/day) but, by chance, was reasonably c l o s e t o a c t u a l z i n c i n t a k e s of Seventh-Day A d v e n t i s t students consuming s e l f - s e l e c t e d d i e t s as discussed e a r l i e r . M a r g i n a l i n t a k e s of t e s t n u t r i e n t s are u s u a l l y s e n s i t i v e l e v e l s f o r b i o l o g i c a l e v a l u a t i o n . As shown i n Table I I , mean f e c a l z i n c l o s s was 6.91 mg/ day f o r the v e g e t a r i a n s u b j e c t s and 9.10 mg/day f o r the omnivore s u b j e c t s , d i f f e r e n c e s which were s t a t i s t i c a l l y s i g n i f i c a n t (P