Bioavailability of Iron and Other Trace Minerals from Human Milk

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Bioavailability of Iron and Other Trace Minerals from Human Milk CHARLES W. WEBER and LINDA A. VAUGHAN

1

University of Arizona, Department of Nutrition and Food Science, Tucson, AZ 85721 WILLIAM A. STINI University of Arizona, Department of Anthropology, Tucson, AZ 85721

The iron in human milk is in a chemical form which has a higher degree of availability than either cow's milk or infant formula. The reason for this higher availability has not been determined but theorized to be because of the type of ligand to which the iron is attached. One of the possible ligands discussed was lactoferrin which has a decreasing role of importance as an iron carrier as cited by current research papers. The ligand showing the greatest promise is a low molecular weight ligand to which iron has been found bound in high amounts. The role and/or mechanism of the iron ligand in its absorption is unknown and needs to be further elucidated. Iron deficiency in infancy remains a common nutritional problem. In infants, milk feeding represents the basis of nutrition and an essential source of iron during infancy. It is felt that iron deficiency becomes a problem after the first four mounths of l i f e . One of the most effective and widespread methods of preventing this deficiency is the use of iron-fortified formulas. The iron levels in iron-fortified formulas are approximately ten times the concentration found in human milk. The controversies concerning human milk versus formulas or cow's milk is the availability of the iron. The iron in human milk is stated to be quite bioavailable, but questions arise concerning the need for iron supplements for infants who are exclusively breast-fed. Further unanswered question or questions is the mechanism involved in human milk which causes i t to have a high bioavailability. Some data and theories 1

Current address: Arizona State University, Department of Home Economics, Tempe, AZ 85281 0097-6156/82/0203-0173$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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NUTRITIONAL BIOAVAILABILITY OF IRON

as to how human milk achieves this greater bioavailability are to be presented in the following discussion.


Lactoferrin L a c t o f e r r i n was f i r s t i d e n t i f i e d as a r e d p r o t e i n f r a c t i o n i n human m i l k ( 1 ) . The m i l k p r o t e i n has been c a l l e d by v a r i o u s names of r e d m i l k p r o t e i n , e k k r i n o s i d e r o p h i l i n , and l a c t o t r a n s f e r r i n which i s i n t u r n very s i m i l a r i n many r e s p e c t s to t r a n s f e r r i n , the i r o n b i n d i n g p r o t e i n of serum. The c o n c e n t r a t i o n of l a c t o f e r r i n i n human m i l k i s u n u s a l l y r i c h with a range of 7 mg/ml i n colostrum to approximately 1 mg/ml i n mature milk ( 2 ) . However, the bovine colostrum c o n t a i n s l a c t o f e r r i n a t c o n c e n t r a t i o n s o f 5 mg/ml, which drops v e r y r a p i d l y with stage of l a c t a t i o n to where mature bovine m i l k c o n t a i n s 20-200 ug/ml of l a c t r o f e r r i n ( 3 ) . L a c t o f e r r i n i s a l s o found i n v a r i o u s other exocrine s e c r e t i o n s of the body such as v a g i n a l , n a s a l , b r o n c h i a l and i n t e s t i n a l (4H6). The a b i l i t y of l a c t o f e r r i n to i n h i b i t the growth of c e r t a i n microorganisms " i n v i t r o " has been w e l l documented. The evidence f o r such a c t i v i t y " i n v i v o " i s not as w e l l d e f i n e d ( 7 ) . The r o l e of l a c t o f e r r i n i n a n t i m i c r o b i a l a c t i v i t y i n the gut w i l l not be d i s cussed i n t h i s a r t i c l e . Lactoferrin's Physical Properties L a c t o f e r r i n has been i s o l a t e d and i d e n t i f i e d from a wide v a r i e t y of animal s p e c i e s . However, most of the s t u d i e s on s t r u c t u r e and i r o n - b i n d i n g p r o p e r t i e s have involved e i t h e r human or bovine p r o t e i n s ( 2 ) . L a c t o f e r r i n c l o s e l y resembles t r a n s f e r r i n i n molecular weight of 75,000 to 90,000 and c o n s i s t s of a s i n g l e p o l y p e p t i d e c h a i n that binds two f e r r i c i o n s . The p i of t r a n s f e r r i n i s 5.9 w h i l e that of l a c t o f e r r i n i s approximately 9.0 (8) and has an even higher a s s o c i a t i o n constant f o r i r o n - b i n d i n g . L a c t o f e r r i n has the property of r e t a i n i n g i t s i r o n even i n the presence o f a r e l a t i v e l y l o w - a f f i r n i t y i r o n c h e l a t o r such as c i t r a t e below pH 4.0. Transf e r r i n , on the other hand, looses i t s i r o n when the pH i s lowered from 6 to 5 (7). There i s extensive informat i o n i n the l i t e r a t u r e concerning the p h y s i c a l propert i e s of l a c t o f e r r i n which w i l l not be covered i n t h i s paper. 1

L a c t o f e r r i n s Role i n Iron Absorption Infants have a r e l a t i v e l y e f f i c i e n t i r o n a b s o r p t i o n of b r e a s t m i l k (9, 10). The c l o s e p h y s i c a l p r o p e r t i e s between l a c t o f e r r i n and t r a n s f e r r i n would suggest that

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

WEBER ET AL.

Minerals from Human Milk

l a c t o f e r r i n i s i n v o l v e d i n the t r a n s p o r t a t i o n as a l i g and from the lumen to the i n t e s t i n a l mucosa i n a r e a d i l y absorbed form. Hubbers and Rummel (11) proposed a scheme where alimentary i r o n binds to a l i g a n d which i n t u r n t r a n s f e r s the f e r r i c i o n to a mucosal b i n d i n g prot e i n which i s then transported i n s i d e the mucosal c e l l (Table I ) . Table I - Proposed Scheme f o r Iron Absorption Mechanism. Downloaded by UNIV OF CALIFORNIA SANTA BARBARA on May 27, 2018 | https://pubs.acs.org Publication Date: November 1, 1982 | doi: 10.1021/bk-1982-0203.ch011

Lumen

[Lii-Fe]

Mucosa Fe-Ferrit i n or — Fe Transferrin

Lamina LMW — -> Lig.-Fe

Propria +

3

Fe TransFerrin

In the case of i n f a n t s , the l i g a n d may v e r y w e l l be the l a c t o f e r r i n which t r a n s p o r t s the f e r r i c i o n e i t h e r to the c e l l mucosal b i n d i n g p r o t e i n or i n t o the mucosal c e l l d i r e c t l y . Inside the mucosal c e l l the i r o n i s bound to e i t h e r t r a n s f e r r i n or f e r r i t i n f o r storage. Rat experiments have demonstrated that the absorbed i r o n passes from i n t e s t i n a l c e l l s to p o r t a l plasma l a r g e l y i n a low molecular weight (LMW) form (12). An a d d i t i o n a l f a c t o r would be the age of the i n f a n t i n which the r o l e of g a s t r i c a c i d i t y and p r o t e o l y t i c enzyme would have to be considered. As the young i n f a n t ages the d i g e s t i v e system develops i t s a b i l i t y to funct i o n as a complete organ. In neonates, however, i r o n a b s o r p t i o n appears to be l e s s dependent on intermediary i r o n metabolism and more on the i r o n s u p p l i e d by m i l k . L a c t o f e r r i n ' s r o l e i n i r o n a b s o r p t i o n was demons t r a t e d by the a d d i t i o n of l a c t o f e r r i n , presumably i r o n saturated, to a l a c t o f e r r i n f r e e simulated human m i l k . Administered to a d u l t s i t d i d not i n c r e a s e i r o n absorpt i o n (13). The a d d i t i o n of a p o l a c t o f e r r i n was shown to a c t u a l l y i n h i b i t i r o n uptake by r a t and guinea-pig i n everted duodenal sacs, while the a d d i t i o n of Fe - l a c t o f e r r i n had no e f f e c t on uptake of i r o n (14). An add i t i o n a l study demonstrated a negative r e l a t i o n s h i p between duodenal l a c t o f e r r i n c o n c e n t r a t i o n and i r o n a b s o r p t i o n i n a d u l t s (15). These r e s u l t s would suggest that l a c t o f e r r i n has no r o l e or even a negative r o l e i n i r o n absorption. Further, a d d i t i o n a l studies brings i n to question the r o l e , i f any at a l l , t h a t ' l a c t o f e r r i n has i n i r o n a b s o r p t i o n . McMillan et a l . (13) have shown that the i r o n i n human milk, d e s p i t e the h i g h l a c t o f e r r i n content, i s more r e a d i l y absorbed than i r o n from a simul a t e d human m i l k of comparable i r o n content. The 2



NUTRITIONAL BIOAVAILABILITY OF IRON a d d i t i o n of l a c t o f e r r i n to the simulated m i l k f u r t h e r decreased i r o n a b s o r p t i o n . They f u r t h e r demonstrated that t h i s a v a i l a b i l i t y was not a f f e c t e d by b o i l i n g the m i l k which would denature the p r o t e i n s . A p o i n t to cons i d e r was the f a c t that the study was conducted on a d u l t s . A second study which demonstrated h i g h b i o a v a i l a b i l i t y of b r e a s t - m i l k i r o n , used the e x t r i n s i c tag method and fed the b r e a s t - m i l k to s i x month o l d i n f a n t s (10). T h e i r r e s u l t s suggested that breast m i l k does c o n t a i n a f a c t o r or f a c t o r s which a c t i v e l y a i d i n i r o n absorption. The a n a l y s i s of human m i l k f o r the d i s t r i b u t i o n of i r o n i n t o the v a r i o u s components found i r o n i n three f r a c t i o n s of l i p i d , low molecular weight form and l a c t o f e r r i n (16). The t o t a l c o n c e n t r a t i o n of m i l k i r o n var i e d from 0.26 to 0.73 mg/ml with 15 to 46% of the i r o n bound to the l i p i d f r a c t i o n , and 18 to 50% found i n a low molecular weight f r a c t i o n . S u r p r i s i n g l y , only a small amount of i r o n was bound to the l a c t o f e r r i n , which was saturated at 1-4%. These r e s u l t s even f u r t h e r comp l i c a t e the r o l e of l a c t o f e r r i n i n i r o n a b s o r p t i o n by infants. Further experimental work needs to be done to d e f i n e the r o l e of l a c t o f e r r i n i n i r o n a b s o r p t i o n , i f any at a l l . Trace M i n e r a l Cocentrations i n M i l k With the exact r o l e of l a c t o f e r r i n u n c e r t a i n and the mechanism of i r o n a b s o r p t i o n a l s o unknown, the conc e n t r a t i o n of i r o n and other t r a c e elements i n human m i l k i s a c o n t r o v e r s a l item. The data i n v o l v i n g i r o n l e v e l s i n breast m i l k date from the e a r l y f i f t i e s to the present time* During the stage of l a c t a t i o n , colostrum, e a r l y and mature m i l k samples are known to decrease i n i r o n c o n c e n t r a t i o n w i t h time, see Table II (17,18). The comparison of mature b r e a s t milk, 7 days or o l d e r , f i n d s a range i n i r o n c o n c e n t r a t i o n from 0.21 to 1.28 m g / l i t e r . Weekly, d a i l y and d i u r i n a l v a r i a t i o n w i t h i n a given day were demonstrated f o r i r o n , copper and z i n c i n human m i l k samples (20). Great v a r i a t i o n s were found w i t h i n a given day on totHil y i e l d , f a t , and m i n e r a l l e v e l s (17,20). Table I I shows the v a r i a t i o n i n breast m i l k c o n c e n t r a t i o n f o r i r o n and w i t h v a r i o u s claims as to the c o r r e c t v a l u e s f o r human m i l k i r o n l e v e l s . The d i f f e r e n c e s can be p a r t i a l l y explained by sampling techniques, but probably r e f l e c t the wide v a r i a t i o n found by the d i f f e r e n t l a b o r a t o r i e s f o r i r o n l e v e l s . The maternal d i e t can a f f e c t the i r o n n u t r i t i o n d u r i n g l a c t a t i o n . L a c t a t i n g r a t s were fed three l e v e l s and the i r o n s t a t u s of t h e i r pups had a d e f i n i t e r e l a t i o n s h i p to d i e t a r y i r o n l e v e l s (27).


WEBER ET AL.

Table I I .


Fe mg/liter 0.40 0.36 1.00 0.60 0.21 0.86 1.28 0.49 0.46


The Average Iron Concentration of Human M i l k from V a r i o u s Sources Reference Stage o f Lactation 1st

3rd 6th 4th 2nd 2nd 1st

- 5 t h day 5th day 1st week week - 2nd month - 12th week - 6th week - 6th month - 37th week - 32nd month

(26) (25) (24) (23) (20) (22) (21) (18) (17)

The b r e a s t m i l k c o n c e n t r a t i o n o f copper and z i n c were found t o be j u s t as v a r i a b l e as those demonstrated for i r o n . Copper-values were demonstrated to range from 0.24 to 1.34 ppm, while z i n c was found to range from 5.1 to 1.1 ppm i n mature b r e a s t m i l k samples (17, JjblO). One o f the g r e a t e s t f a c t o r s i n c o n c e n t r a t i o n v a r i a t i o n was found w i t h i n the woman h e r s e l f (17,20). T h i s d i u r i n a l e f f e c t was j u s t one of many f a c t o r s which could l e a d t o the l a r g e v a r i a t i o n found i n t r a c e m i n e r a l concentrations of breast milk. Iron Absorption Recent s t u d i e s have demonstrated that i r o n i s b e t t e r absorbed from human m i l k than from e i t h e r cow's m i l k o r formula. Furthermore, t h a t human m i l k can prov i d e s u f f i c i e n t i r o n f o r i n f a n t s during t h e i r f i r s t year of l i f e (10,13,17,28). Breast m i l k and cow's m i l k a r e e q u a l l y poor i n i r o n , c o n t a i n i n g an average of almost 1 m g / l i t e r . Saarinen's (10) study demonstrated t h a t i n f a n t s b r e a s t f e d throughout the f i r s t s i x to seven months o f l i f e a t t a i n e d greater i r o n s t o r e s than i n f a n t s f e d a cow's m i l k formula. The percent a b s o r p t i o n of breast m i l k , cow's m i l k and formula i s g i v e n i n Table I I I . Table I I I .

Percent Iron Absorption From Breast M i l k , Cow's M i l k and Formula % Absorption Reference Formula Breast Cow's & Iron Milk Milk (28) 10 70 30 3 15 (13) 9 12 49 (10) 19 3-12 (13,29,30) 15-70 9-30



NUTRITIONAL

BIOAVAILABILITY OF IRON

The a b s o r p t i o n values f o r breast milk range from 15-70%, while cow's m i l k range from 9-30% and formula + i r o n average 3-12% a b s o r p t i o n (10,13,28-30). The a b s o r p t i o n values were determined under v a r i o u s c o n d i t i o n s . In some s t u d i e s the breast m i l k samples were t e s t e d i n a d u l t s and not i n i n f a n t s , while another study used an e x t r i n s i c tag. The body i r o n s t a t u s was determined s e v e r a l ways by measuring e i t h e r serum f e r r i t i n , hemoglobin, serum t r a n s f e r r i n s a t u r a t i o n and/or serum i r o n . I t was because of these v a r i o u s c o n d i t i o n s used to measure the percent i r o n absorbed that the wide ranges were probably observed. However, the breast m i l k was always absorbed at a higher l e v e l i n each p a r t i c u l a r study examined than was cow's m i l k or formula. The cow's milk had a higher a b s o r p t i o n r a t e than d i d the formula + i r o n (Table I I I ) . Using the data from three d i f f e r e n t l a b o r a t o r i e s (17,18,20) the intakes per day were c a l c u l a t e d f o r i n f a n t s from 1-3 months of age (Table IV). The m i l k v o l u me of 650 ml was used as an average of s e v e r a l i n v e s t i gator's data (20,31). Table IV.

Trace M i n e r a l Intakes Per Day f o r 1-3 Month Old Infants Consuming Breast M i l k .

M i l k Volume/ day

Fe

Cu mg/day

Zn Reference

(17,32) 650 ml of milk 0.32 1.04 0.28 (20) 650 ml of m i l k 1.26 0.27 0.13 0.72 650 ml of milk (18) 0.21 0.23 RDA of m i l k 10.00 0.30* 3.00 *suggested d a i l y i n t a k e of 0.08 mg/kg/day. The intake values f o r i r o n , copper arid z i n c were c a l c u l a t e d by m u l t i p l y i n g the m i l k c o n c e n t r a t i o n values by the volume of milk consumed per day. I n t e r e s t i n g l y , the data from the three d i f f e r e n t sources had s i m i l a r intakes f o r i r o n , copper and z i n c (Table I V ) . I t should be noted that i n t a k e s f o r a l l t r a c e elements were below the RDA's given f o r i n f a n t s QD. Obviously, the RDA's do not apply to i n f a n t s who are breast f e d but are values to be used f o r formula fed i n f a n t s . The g r e a t e s t d i s p a r i t y i s observed f o r the i r o n requirement which i s 10 mg/ day, while breast fed i n f a n t s have an intake of 0.27 mg/ day. The high a v a i l a b i l i t y of b r e a s t m i l k i r o n can account f o r maintaining i r o n s t a t u s i n the i n f a n t up to s i x months of age who i s e x c l u s i v e l y b r e a s t f e d . Further c a l c u l a t i o n s were made to determine the mg of i r o n absorbed per day i n i n f a n t s fed breast milk


11.

WEBER ET AL.


179


versus those f e d cow's m i l k and/or formula (Table V ) . The v a l u e s were c a l c u l a t e d based upon m i l k i n t a k e v a l u e s f o r the f i r s t through the t h i r d month o f age. Breast milk f u r n i s h e d a higher absorbed q u a n t i t y o f i r o n per day than d i d e i t h e r cow's m i l k o r formula.

Table V. Mg o f Iron Absorbed Per Day from M i l k and Formula Sources. Stage of Breast Formula & Cow's Formula Lactation Milk Milk Iron 1st month 2nd month 3rd month

0.15 0.13 0.12

0.07 0.07 0.08

0.03 0.04 0.04

0.76 0.80 0.88

The i r o n f o r t i f i e d formula s u p p l i e d the g r e a t e s t a v a i l a b l e i r o n to the i n f a n t . I n t e r e s t i n g l y , the t o t a l q u a n t i t y o f i r o n absorbed per day f o r b r e a s t m i l k decreased from f i r s t t o t h i r d month, while cow's milk, formula and formula + i r o n increased i n absorpt i o n . T h i s was caused because the i r o n c o n c e n t r a t i o n of breast m i l k decreases with stage o f l a c t a t i o n . The cow's m i l k and formula a r e constant. T h e i r i n c r e a s e i n absorbed i r o n i s due t o the i n c r e a s e i n volume o f m i l k consumed by the i n f a n t . Human m i l k i s a complex, h i g h l y v a r i a b l e substance with v a r i o u s f a c t o r s l i s t e d below which can change the c o n c e n t r a t i o n of t r a c e elements and p o s s i b l y the a v a i l a b i l i t y o f i r o n . Trace mineral l e v e l s were found t o decrease with time during l a c t a t i o n . The development o f the d i g e s t i v e system o f the i n f a n t with age w i l l a f f e c t p o t e n t i a l a b s o r p t i o n r a t e of i r o n . The a b s o r p t i o n mechanism i t s e l f i s f a r from being t o t a l l y understood. The r o l e of l a c t o f e r r i n i n i r o n a b s o r p t i o n i s i n doubt from the c o n f l i c t i n g data a v a i l a b l e . A d i f f e r e n t l i g a n d i n human m i l k may be the reason i t i s so a v a i l a b l e versus other sources, but at t h i s p o i n t i n time has not been i d e n t i f i e d . For these obvious reasons f u r t h e r work i s necessary to e l u c i d a t e why b r e a s t m i l k i r o n has such a high a v a i l a b i l i t y . Acknowledgement s A r i z o n a A g r i c u l t u r a l Experiment

S t a t i o n No. 3547

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June 2,


Bioavailability of Iron and Other Trace Minerals from Human Milk

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