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Supplement: Nutrient Composition for Fortified Complementary Foods

Iron and Ascorbic Acid: Proposed Fortification Levels and Recommended Iron Compounds¹

Sean R. Lynch^*,2 and Rebecca J. Stoltzfus

^* Department of Internal Medicine, Eastern Virginia Medical School, Norfolk, VA 23501 and Division of Nutritional Sciences, Cornell University, Ithaca, NY 14222

²To whom correspondence should be addressed. E-mail: srlynch{at}visi.net.

	ABSTRACT

TOP ABSTRACT Enhancers of nonheme iron... Enhancing properties of ascorbic... Effect of ascorbic acid... Importance of the form... Effective fortification... Conclusions and recommendations LITERATURE CITED

 
An adequate supply of dietary iron during the 1st 24 mo of life is essential for preventing iron deficiency with its attendant negative effects on mental, motor and emotional development as well as later cognitive performance. Iron reserves and the small amount of highly bioavailable iron in human milk are adequate to satisfy the iron requirements of breast-fed infants of adequate birth weight for the 1st 6 mo of life. Thereafter, complementary foods, iron supplements or both are needed to meet this requirement. Complementary foods should not displace the consumption of human milk. The quantities eaten, particularly by younger infants, may therefore be quite small. As a consequence it is essential that the iron be supplied in a highly bioavailable form. This can be achieved by fortifying complementary foods with ferrous sulfate and ascorbic acid provided that the ascorbic acid is not lost during storage or meal preparation. Suggested fortification levels for ferrous sulfate and ascorbic acid for some types of complementary foods are given. The use of ferrous fumarate or an elemental iron powder instead of ferrous sulfate has not been evaluated adequately. There is a need to develop alternative strategies for improving iron bioavailability in complementary foods because it may not be possible to preserve ascorbic acid activity in many of them.

KEY WORDS: • infant nutrition • complementary foods • iron • ascorbic acid

The body iron present at birth is sufficient for the physiological requirements of babies of normal birth weight during the 1st 6 mo of life. After this the infant rapidly becomes dependent on an adequate supply of readily absorbed dietary iron. Body iron content should increase by 70% between ages 4 and 12 mo (1). Based on a factorial model, the estimated average daily requirement for absorbed iron from age 7–12 mo has been estimated to be 0.69 mg (2). A little less iron is needed after age12 mo, 0.63 mg/d for a child aged 18 mo. Normal birth weight breast-fed infants rarely develop iron deficiency before age 6 mo. However, the risk increases rapidly during the next 3 mo in those who continue to be breast-fed if other dietary items do not include a rich source of highly bioavailable iron (1).

Human milk contains 0.35 mg iron/L (2). It is very well absorbed. Saarinen et al. (3), using an extrinsic iron tag method, demonstrated that 6-mo-old infants absorb 49% of the iron in human milk. The reported intakes of human milk in developing countries average 674, 616 and 549 g/d in infants aged 6–8, 9–11 and 12–23 mo, respectively (4). Between 6 and 12 mo, infants would be expected to absorb 0.11 mg/d from human milk [16% of the estimated average requirement for absorbed iron (2)]. During the 2nd y of life, average absorption from human milk would be 0.09 mg/d (14% of the estimated average requirement for absorbed iron of an 18-mo-old child). More than 80% of the child’s requirement, 0.58 mg/d for infants aged 7 to 12 mo and 0.54 mg/d for children aged 13–24 mo, must therefore be supplied by complementary foods, iron supplements or both.

Animal flesh is the most readily available source of iron for human beings because it contains heme, which is always well absorbed, and it promotes the absorption of other (nonheme) dietary iron (5). Vegetable foods are often rich in factors that make nonheme iron less available for absorption. All of the nonheme iron in a meal that is soluble in gastric juice enters a common pool. The interactions of the iron with inhibitors and enhancers of absorption present in the meal determine the efficiency with which the iron can be absorbed from this pool. Inhibitory factors usually predominate in vegetable foods, particularly those eaten in developing countries. Of these, the most important are phytates in cereal grains and legumes, and polyphenols in tea, coffee, cocoa and certain vegetables and cereal grains. Calcium and animal or vegetable proteins other than those present in animal or fish flesh reduce nonheme iron absorption to a lesser extent (5).

The promotion of breast-feeding is an essential element of nutritional interventions during infancy and early childhood. Any attempt to supply the additional iron needs by the introduction of complementary foods must ensure that they do not replace available human milk. This is especially important in the 2nd 6 mo of life, the time when iron requirements are highest. The quantities of complementary foods consumed may be relatively small. It is therefore essential that the iron source used in fortification is readily available for absorption. The incorporation of meat or fish products should be encouraged where possible because of the high bioavailability of their heme iron. Infants would be expected to absorb as much as 25–50% of the iron provided in the form of heme because they have not yet acquired significant iron stores (9). Walter et al. (10) showed that feeding cookies fortified with bovine hemoglobin to schoolchildren was very effective in improving iron status. However, this will not be a practical option in many settings. Methods for improving the bioavailability of the nonheme iron are therefore particularly important, especially for the commonly used cereal-based complementary foods. It may not be possible to add large concentrations of fortification iron to some of these foods because iron induces organoleptic changes.

	Enhancers of nonheme iron absorption

TOP ABSTRACT Enhancers of nonheme iron... Enhancing properties of ascorbic... Effect of ascorbic acid... Importance of the form... Effective fortification... Conclusions and recommendations LITERATURE CITED

 
Ascorbic acid is the most efficient promoter of nonheme iron absorption. Moore and Dubach (11), who were among the earliest investigators to use radioisotopes to study iron absorption, first demonstrated the enhancing properties of ascorbic acid. Both fruit juices and crystalline ascorbic acid were effective. They also reported that the enhancing properties were dose related and dependent on the presence of ascorbic acid in the lumen of the upper gastrointestinal tract. Intravenously injected ascorbic acid was without effect.

The enhancing effects of ascorbic acid on the absorption of nonheme iron have been demonstrated in a large number of human studies using radioisotopes to measure iron absorption (12), but it has no effect on the absorption of heme iron. Ascorbic acid acts as a common nonheme pool ligand, increasing the absorption of both intrinsic food iron and fortification iron compounds that are soluble in gastric juice (12). It is effective only when eaten with the meal. In one study, 500 mg of ascorbic acid taken with the test meal increased absorption sixfold whereas the same quantity had little effect when consumed 4 and 8 h earlier (13). The mechanism of action appears to be complex. The initial step in the absorption of elemental iron depends on the uptake of soluble ferrous iron by a recently characterized transmembrane transporter, divalent metal transporter 1 (14). Ascorbic acid acts in the lumen of the stomach and duodenum both by reducing ferric food iron to the ferrous state and by preserving its solubility as the luminal pH rises in the duodenum (15).

It has been suggested that other organic acids may also enhance iron absorption. However, despite encouraging observations made over 50 y ago by Groen et al. (16), the effects of other organic acids on iron bioavailability have not been studied rigorously. The experiments that have been done have yielded inconsistent results. Some investigators reported modest enhancing properties for lactic (17), citric, malic and tartaric acids (18). Oxalic acid was inhibitory. Lactic acid induced a threefold increase in iron absorption from maize and sorghum gruel. Citric, malic and tartaric acids produced a two- to threefold improvement in percentage absorption from a low bioavailability rice-based meal. Derman et al. (19) demonstrated a dose-related but limited enhancing effect of citric acid on iron absorption from an isolated soy protein drink. The same group also studied the effects of fruit juices on iron absorption from a rice meal (20). There was a close correlation between iron absorption and the ascorbic acid content of the fruits tested, but a significant although weaker correlation between iron absorption and the quantity of citric acid was also evident. In this report, malic acid content was inversely correlated with absorption. On the other hand, Hallberg and Rossander (21) observed significant inhibition of nonheme iron absorption when citric acid (1 g) was added to a low bioavailability meal comprising maize, rice and black beans. Glahn et al. (22) also demonstrated decreased iron uptake by Caco-2 cells from high bioavailability infant formulas containing large quantities of citrate. They concluded that citrate may diminish the enhancing properties of ascorbic acid and cysteine.

Two iron chelates have been used to promote adequate iron absorption from vegetable meals. The iron in sodium iron EDTA is absorbed two-to-three times as well as food iron when it is added to inhibitory meals (23). It is not suitable for the fortification of complementary foods because it is not possible to add sufficient iron without exceeding the acceptable daily intake for EDTA. Some evidence suggests that amino acid chelates, such as iron bisglycinate, may be useful for fortifying milk products. Available information is not sufficient for recommendations to be made for the possible use of these compounds.

In summary, the incorporation of heme or the addition of ascorbic acid and a soluble iron salt are the only established practical methods for providing adequate quantities of bioavailable iron in complementary foods.

	Enhancing properties of ascorbic acid: quantitative considerations

TOP ABSTRACT Enhancers of nonheme iron... Enhancing properties of ascorbic... Effect of ascorbic acid... Importance of the form... Effective fortification... Conclusions and recommendations LITERATURE CITED

 
The experimental designs of the studies summarized in this section varied considerably. The conclusions that we have drawn are at best tentative. In considering the effects of ascorbic acid, we have made no distinction between experiments carried out in adult volunteers and those that involved children because the observations of Hurrell et al. (24) demonstrated that the proportional effects of inhibitors and enhancers of iron absorption are the same in adults and infants. We have also combined observations from studies in which the effects of ascorbic acid on the absorption of intrinsic food iron were measured with those in which the effects of ascorbic acid on the absorption of fortification iron, added as ferrous sulfate, were evaluated because ferrous sulfate equilibrates rapidly with the common nonheme pool in the stomach. The interactions of ascorbic acid with intrinsic food iron and fortification iron added as ferrous sulfate appear to be identical.

Ascorbic acid is useful for reducing the influence of all the recognized inhibitors of nonheme iron absorption including phytates, polyphenols and calcium as well as vegetable and certain animal proteins. Cook and Monsen (13) were the first to evaluate its quantitative effect rigorously. A linear relationship was observed between log percentage absorption and the molar ratio of ascorbic acid to iron in a meal comprised of egg white, dextrimaltose, corn oil, calcium and phosphate. The meal contained 4.1 mg of elemental iron added as ferrous sulfate. The major inhibitors of iron absorption in the meal were calcium and proteins present in egg albumen. The experiment also demonstrated that the greatest proportional effect was seen for molar ratios of ascorbic acid to iron that were <10 (12). Although there was considerable interstudy variability, a similar quantitative effect was evident when the results of 34 experiments using maize and rice meals were analyzed (12). Phytate is the most important inhibitor of iron absorption in cereal foods (25) and would be expected to have been the major inhibitory factor in these meals. Ascorbic acid is therefore clearly effective in reversing the inhibitory effects of phytate.

	Effect of ascorbic acid on iron absorption from foods used for complementary feeding

TOP ABSTRACT Enhancers of nonheme iron... Enhancing properties of ascorbic... Effect of ascorbic acid... Importance of the form... Effective fortification... Conclusions and recommendations LITERATURE CITED

 
Complementary foods used in developing countries are most commonly prepared from cereal grains, cow’s milk and legumes (especially soybeans). One or more of the food sources may sometimes be combined in one complementary food. As indicated above, phytates are the most important iron absorption inhibitors in cereal foods. The interaction among phytates, ascorbic acid and iron therefore merits particular attention. Specific recommendations for the removal of phytate and the addition of ascorbic acid to cereal-based complementary foods could be very valuable for designing effective fortification strategies for early childhood. The effects of polyphenols are less important but significant in a few specific instances, particularly where sorghum is used (26). The major inhibitors of iron absorption in cow’s milk and cow’s milk–based products are calcium (27) and the milk proteins (28). Phytates are also the major inhibitors in soybean products (29), although a soybean protein or protein-related moiety also reduces iron bioavailability (30).

Cereal foods.

The International Nutritional Anemia Consultative Group published a detailed analysis 20 years ago of the effects of cereals on iron bioavailability (31). Based on the reanalysis of 20 published studies, it concluded that iron is poorly absorbed from all cereal grain foods with the exception of low extraction wheat flour. Mean absorption values (corrected to 40% reference absorption) for maize-based meals were 2.4–6%. Corresponding values for sorghum, rice and low extraction wheat flour were 2.8–4.4, 1.2–11.6 and 12–56%, respectively. The most plausible explanation for the variability in absorption was considered to be differences in phytate content. The very low absorption from sorghum meals was probably due to the presence of polyphenol inhibitors in addition to phytate.

As indicated above, ascorbic acid appears to be valuable in reversing the inhibitory properties of maize and rice meals (12). Cook et al. (32) evaluated more rigorously the effectiveness of ascorbic acid for improving iron absorption from several different cereal grains. They measured iron absorption from 50-g cereal meals prepared from rice, wheat, maize and sweet quinoa in adult volunteers. Iron was absorbed poorly from all the meals in the absence of ascorbic acid. The absorption was 2.3–3.7 times greater in the maize, wheat and rice flour meals after the addition of 50 mg of ascorbic acid. The improvement was significantly less for sweet quinoa (1.7 times).

Phytates are the major inhibitors of iron absorption in wheat. Most of the phytate is removed in the milling of low extraction wheat flour, which made it possible for Hallberg et al. (33) to quantitatively study the inhibitory properties of sodium phytate. There was an inverse relationship between percentage of iron absorption and phytate for meals containing 2–250 mg of phytate (expressed as phytate phosphorus). Ascorbic acid was effective in reversing the inhibitory effect of phytate in a dose-dependent fashion. The greatest increase in absolute absorption was observed at low phytate concentrations; the greatest proportional enhancement was observed with the highest phytate concentrations.

From the practical point of view, it is important to establish how much iron would be absorbed from a cereal-based complementary food under optimal conditions (adequate ascorbic acid and lowest amount of phytate). This issue was addressed most directly in another study (34). Full-term infants with a mean age of 32 wk absorbed 8.5% of the iron in a low phytate wheat flour cereal meal fortified with 2.7 mg of ferrous sulfate iron and ascorbic acid (molar ratio of ascorbic acid to iron, 2:1). The meals contained 25 g of dried cereal. Based on the assumption that the daily intake for the proposed complementary food to be used in Central and South America will be 40 g for infants aged 6–11 mo and 60 g for children aged 12–23 mo (C. Lutter, 2002, personal communication), the low phytate cereal meal fortified with iron and ascorbic acid evaluated by Davidsson et al. (34) would be expected to supply 0.37 mg/d of absorbed iron for infants aged 6–11 mo and 0.55 mg/d for children aged 12–23 mo. These values represent 65% of the calculated average requirement for breast-fed infants aged 6–12 mo (0.58 mg/d) and >100% of the requirement during the 2nd y of life (0.54 mg/d).

Cow’s milk.

Iron in human milk is very well absorbed. Absorption from cow’s milk is much lower. The higher calcium concentration in cow’s milk is the primary reason (27), but milk proteins also inhibit iron uptake (28). The addition of ascorbic acid markedly improves iron absorption from cow’s milk and infant formulas based on cow’s milk (19,35–42). For example, the addition of ascorbic acid at a concentration of 100 mg/L (molar ratio of ascorbic acid to iron, 2:1) to cow’s milk containing ferrous sulfate (15 mg/L) increased absorption approximately twofold (39,43). Approximately 10% of the iron was absorbed. Unmodified cow’s milk may not be an optimal complementary food during the 1st 12 mo of life because it induces gastrointestinal bleeding in some infants (44). However Hertrampf et al. (45) recently reported that the National Supplementary Food Program in Chile reduced the prevalence of anemia in children aged 12–18 mo from 27.3 to 8.8%. Children under age 18 mo receive 2 kg of powdered milk per month from this program. If all the milk is given to the child, each receives 67 g/d. The milk is fortified with 10 mg of iron and 70 mg of ascorbic acid per 100 g in addition to other micronutrients. The molar ratio of ascorbic acid to iron is 2:1. It is therefore reasonable to assume that 10% of the iron is absorbed, providing 0.67 mg/d (116% of the calculated requirements for breast-fed infants aged 7–12 mo and 124% for children who are older than 1 y).

Soy products.

Iron is poorly absorbed from soybean protein products that are used as complementary foods (46,47). Reported absorption values were between 1.1% and 2.8% and the total amount of iron absorbed from meals eaten by iron-replete adult volunteers (corrected for reference absorption of 40%) was between 0.10 mg and 0.25 mg (31). Although the relative improvement in absorption obtained after the addition of ascorbic acid to a meal containing isolated soy protein was comparable with that observed with cow’s milk, the absolute increase was much smaller (19,38,48). When 100 mg of ascorbic acid was added to a meal containing isolated soy protein (4 mg of iron, molar ratio of ascorbic acid to iron, 8:1), absorption increased from 0.6 to 3.2% (48). However, the absolute amount of iron absorbed was still very small (0.13 mg). The addition of ascorbic acid at 40 mg/100 g to a soy-based infant formula containing iron at 6 mg/100 g (molar ratio of ascorbic acid to iron, 2) did not increase absorption significantly (38). When the ascorbic acid concentration was raised to 80 mg/100 g, absorption was significantly higher (6.9% compared with 1.8%). There was no further increase with the addition of ascorbic acid at 160 mg/100 g. In another experiment these investigators directly compared the effect of increasing the ascorbic acid concentrations from 40 to 80 mg/100 g in two infant formulas, one milk based and the other soy based. Mean absorption from the soy-based formula increased from 2.4 to 7.2% whereas the corresponding values for the milk-based formula were 5.3 and 19.5%.

All of these observations indicate that more ascorbic acid will be needed to ensure adequate iron bioavailability in complementary foods containing soy than is the case for cow’s milk– or cereal-based foods. However, a study by Rios et al. (49) suggests that the absorption for iron-fortified soy formula and infant cereal containing soy protein may be better than these observations would suggest, but the effect of ascorbic acid was not evaluated. Furthermore, Hertrampf et al. (50) reported that soy formula (2.5 mg intrinsic iron, 12 mg iron as ferrous sulfate and 54 mg ascorbic acid per liter) was as effective as cow’s milk in preventing iron deficiency in infants. The latter observations should be interpreted with caution because these children had also been eating meat and solid foods for several months before the evaluation.

The effect on iron absorption of removing phytate from infant formulas based on soy protein isolate and fortified with ferrous sulfate (16 mg/L) and ascorbic acid (110 mg/L, molar ratio of ascorbic acid to iron, 2:1) was studied by Davidsson et al. (51). Iron absorption increased from 3.9 to 8.7% when all of the phytic acid was removed. Doubling the ascorbic acid content of the formula with its native phytate content increased absorption from 5.9 to 9.6%. Once again, high levels of ascorbic acid or the combination of phytate removal and ascorbic acid addition yields a level of iron absorption sufficient to meet the infant’s iron needs.

Foods containing polyphenols.

Polyphenols are more inhibitory to iron absorption than are phytates. Ascorbic acid is less effective in reversing their inhibitory properties (52). However, the interactions among polyphenols, iron and ascorbic acid are less significant for iron absorption from complementary foods unless the children are also given drinks such as tea and chocolate-flavored milk. Only sorghum-based cereal foods are likely to contain polyphenols.

	Importance of the form of iron used for fortification

TOP ABSTRACT Enhancers of nonheme iron... Enhancing properties of ascorbic... Effect of ascorbic acid... Importance of the form... Effective fortification... Conclusions and recommendations LITERATURE CITED

 
Almost all of the studies described above demonstrated the effects of ascorbic acid on intrinsic food iron or fortification iron in the form of ferrous sulfate. Its effect on other iron compounds has only been measured in a few experiments. Derman et al. (53) reported a threefold increase in percentage of iron absorption when ascorbic acid was added to infant cereals fortified with ferrous sulfate, ferric pyrophosphate or ferric ammonium citrate at 1:1.5 mol/L ratio of ascorbic acid to iron. The chemical form of the iron compound used for fortification did not seem to influence the result. The proportional effect on the absorption of ferric orthophosphate was shown to be similar to that for ferrous sulfate, although the basal level of iron absorption from ferric orthophosphate was very low in that study (54). The quantitative increase in absorption was minimal.

Elemental iron powders and ferrous fumarate are frequently added to complementary foods. Only one study (54) directly addressed the effect of ascorbic acid on an elemental iron powder. Radioactive electrolytic iron with a high relative bioavailability with respect to ferrous sulfate was used. The proportional improvement in iron absorption after the addition of ascorbic acid was only slightly less than that seen with ferrous sulfate. One could infer that ascorbic acid improves iron absorption from elemental iron from another report. Walter et al. (55) demonstrated that the feeding of an infant cereal fortified with a high concentration of electrolytic iron (55 mg/100 g dry cereal) together with an infant formula containing ascorbic acid was effective in reducing the prevalence of iron deficiency in infants. There is, nevertheless, an urgent need for a clearer understanding of the factors that affect the absorption of elemental iron and the influence of ascorbic acid.

The effect of ascorbic acid on iron derived from ferrous fumarate has also not been evaluated rigorously. Ferrous fumarate is undoubtedly a bioavailable form of fortification iron (25) but it is not soluble in water. It requires exposure to stomach acid to become soluble and presumably to enter the nonheme common pool. The general assumption is that ferrous fumarate readily enters the common nonheme pool in the stomach. If so, the enhancing properties of ascorbic acid should be identical to those observed in meals fortified with ferrous sulfate.

Three reports provide some information about the potential effectiveness of ascorbic acid in promoting iron absorption from ferrous fumarate. In the first, ascorbic acid was added to a chocolate drink powder containing 4.2 mg of iron/25 g serving (56). Absorption was relatively high when the ferrous fumarate was added during the manufacture of the drink powder (5.27%) but the addition of 25 mg of ascorbic acid had no effect. The absorption of ferrous fumarate was also measured in a liquid formula meal containing egg white, hydrolyzed maize starch and maize oil. Absorption increased modestly after the addition of 100 mg of ascorbic acid (from 7.14 to 11.26%) but the difference was not statistically significant. In the second report, the same investigators found no improvement in absorption by infants aged 6–12 mo when the ascorbic acid content of a wheat and soy flour infant cereal containing 2.5 mg of iron as ferrous fumarate was doubled from 25 to 50 mg/meal (57). Finally, Davidsson et al. (58) reported that iron absorption was approximately four times greater from ferrous sulfate than from ferrous fumarate when a weaning cereal containing ascorbic acid (molar ratio of ascorbic acid to iron, 2:1) was eaten by children aged 2–5 y. Very similar results were obtained in children with Helicobacter pylori infections (before and after treatment for the infection) and in uninfected children. The difference in absorption from the two salts may therefore not be attributable to reduced hydrochloric acid secretion caused by H. pylori infection. A possible alternative explanation for the experimental findings is that ascorbic acid induced the enhancement of iron absorption from ferrous sulfate but not from ferrous fumarate.

The observations outlined above raise questions about the interaction between ascorbic acid and ferrous fumarate but do not permit any definite conclusions to be drawn. Additional research is needed to determine how effectively ferrous fumarate equilibrates with the common nonheme iron pool and whether ascorbic acid is an effective enhancer of iron absorption from this iron salt in all meals. It would be prudent to use ferrous sulfate as the iron source in complementary foods at the present time. The absorption of iron from ferrous fumarate may be suboptimal in all infants or in those suffering from chronic H. pylori infections, which may be common in some developing countries. Iron absorption from ferrous fumarate may also not be enhanced adequately by ascorbic acid.

	Effective fortification strategies in infancy

TOP ABSTRACT Enhancers of nonheme iron... Enhancing properties of ascorbic... Effect of ascorbic acid... Importance of the form... Effective fortification... Conclusions and recommendations LITERATURE CITED

 
The experimental observations outlined above provide a framework for recommendations for iron fortification of complementary foods. They indicate that it will be important to ensure adequate bioavailability of the fortification iron. The effectiveness of milk-based infant formulas containing ferrous sulfate and ascorbic acid for the delivery of iron to bottle-fed infants is well established (40–42). The iron is highly bioavailable. When fed to adult volunteers, mean absorption values as high as 13–19% were observed (42).

The most convincing evidence for the effectiveness of delivering iron in complementary foods is provided by a series of studies conducted in Chile in which ferrous sulfate and ascorbic acid were added to liquid or powdered cow’s milk (43,59–61). The use of ferrous sulfate alone was only partially successful. Recently, the Ministry of Health in Chile instituted a national program in which all children under age 18 mo receive 2 kg of powdered milk per month. The milk is fortified with ferrous sulfate (10 mg Fe/100 g) and ascorbic acid (70 mg/100 g) in addition to other micronutrients. If the children receive all the milk, it is expected to supply them with 7 mg iron and 50 mg ascorbic acid per day. As we indicated above, it will provide 116% of the calculated average requirement between ages 6 and 12 mo and 124% after 1 y if 10% of the iron is absorbed. The preliminary results from a recent survey indicate that the program has been very successful in reducing the prevalence of iron deficiency (45).

The effectiveness of iron fortification of infant cereal foods is far less certain (62,63). There are several reasons for this situation. It is more difficult to add ferrous sulfate to infant cereals because of alterations in the organoleptic properties of the food. The two iron fortification compounds most commonly added to infant cereals are elemental iron and ferrous fumarate. Some forms of elemental iron may be insoluble and unavailable for absorption. Most cereal foods are rich in factors that inhibit iron absorption. Ascorbic acid, added to improve bioavailability, is frequently oxidized and rendered ineffective during storage or cooking of infant cereals [baking, prolonged boiling and even protracted warming (64) leads to the loss of ascorbic acid]. An enhancing effect of ascorbic acid has not been clearly established for elemental iron or ferrous fumarate although, as described above, fortification was effective in one small trial in which a rice-based cereal was fortified with a large quantity of electrolytic iron (550 µg/g) and fed with infant formula containing ascorbic acid (55).

	Conclusions and recommendations

TOP ABSTRACT Enhancers of nonheme iron... Enhancing properties of ascorbic... Effect of ascorbic acid... Importance of the form... Effective fortification... Conclusions and recommendations LITERATURE CITED

 

An adequate intake of highly bioavailable iron is important for preventing developmental delays in infancy and future cognitive impairment.

Although the iron in human milk is very well absorbed, the quantity is insufficient to meet the needs of infants after age 6 mo.

Complementary foods are provided along with human milk as the child transitions to the consumption of family foods. They must therefore be designed to meet the infant’s additional needs without displacing human milk from the diet. This is particularly important for iron, which is a critical nutrient during this period.

Because the intake of complementary foods is limited, particularly when iron requirements are highest, providing the iron in a highly bioavailable form is essential.

When technically feasible, ascorbic acid should be added to all complementary foods that are fortified with iron to improve bioavailability.

Ascorbic acid is unstable when exposed to heat and oxygen during food storage and preparation. If the loss of ascorbic acid before consumption cannot be prevented, other methods of improving bioavailability should be considered.

There is very little direct experimental evidence indicating that the molar ratio is the critical factor. The absolute amount of ascorbic acid in the meal and the ratio between the concentration of ascorbic acid and important inhibitors, particularly phytates, may be more important. It is nevertheless convenient to base quantitative recommendations for ascorbic acid on the molar ratio of ascorbic acid to iron, which should be between 2:1 and 4:1 (70–140 mg/d in complementary foods designed to supply sufficient iron to meet the calculated average requirements of breast-fed infants). The lower concentrations are sufficient in powdered cow’s milk and cow’s milk–based foods and cereal weaning foods that either have a low native phytate content or have been subjected to phytate removal. In cereal foods with high phytate concentrations, cereal foods that contain polyphenols or weaning foods that have significant quantities of soybean flour or soybean protein products, a molar ratio of ascorbic acid to iron of 4:1 should be used.

Where possible, dried ferrous sulfate of small particle size is the recommended source of fortification iron. The quantitative effect of ascorbic acid on the bioavailability of other iron sources such as ferrous fumarate and elemental iron that are frequently used for food fortification has not been determined.

The quantity of fortification iron added to complementary foods should be sufficient to ensure that the infant’s diet (human milk plus complementary food) meets the current Dietary Reference Intake (DRI)² values for iron (2). Experimental evidence indicates that absorption values of 10% can be expected for cow’s milk and low phytate or dephytinized cereal foods if ascorbic acid and ferrous sulfate are added in an ascorbic acid to iron molar ratio of 2:1. As indicated above, a molar ratio of 4:1 would be required if more inhibitory foods such as soybeans with a native phytate content are used.

The quantity of iron absorbed from human milk is very small. It is therefore convenient to ignore the contribution from this source and to base recommendations for fortification levels for iron in complementary foods solely on the current DRI. As indicated above, the average requirement for absorbed iron in children aged 13–24 mo is not much less than that for infants aged 7–12 mo. However, the Estimated Average Requirement (EAR) and Recommended Dietary Allowance (RDA) values published recently by the Institute of Medicine are much lower (2). They are based on a predicted absorption of 18% for dietary iron after age 1 y. The iron in most complementary foods used in developing countries will be less bioavailable. Therefore, the EAR and RDA values for infants aged 7–12 mo (6.9 mg and 11.0 mg, respectively) should be used in choosing the iron fortification level in complementary foods for all children. The RDA level should be supplied where possible. There is no risk of exceeding the Tolerable Upper Intake Level (40 mg/d for all children (2)). For infants aged 7–12 mo (daily consumption, 40 g), fortification iron would be needed at a level of 170 µg/g to meet the EAR and 275 µg/g to meet the RDA. Corresponding levels for children aged 13–24 mo (daily consumption, 60 g) are 115 and 183 µg/g. The fortification of simple cereal flours with these amounts of iron may cause unacceptable organoleptic changes. However, it has been proven possible to incorporate relatively large quantities of iron in composite foods such as Incaparina and Bienestarina (65).

Further research is urgently needed to establish the efficacy with which ascorbic acid improves absorption from ferrous fumarate and the various forms of elemental iron. It will also be important to determine whether these forms of iron are absorbed adequately by infants and whether normal gastric acidity is necessary for their assimilation.

Where possible the inclusion of meat products should be considered; 1 mg of heme iron would be as effective as 3–5 mg of nonheme iron introduced as ferrous sulfate with ascorbic acid.

Further research is urgently needed to evaluate alternative methods for improving the bioavailability of complementary foods. The removal of phytate appears to be the most promising at this time. The potential value of lactic acid as a promoter of iron absorption in selected complementary foods should also be studied because fermented foods that contain increased quantities of lactic acid are traditional complementary foods in some African countries.

	FOOTNOTES

 
¹ Presented as part of the technical consultation "Nutrient Composition for Fortified Complementary Foods" held at the Pan American Health Organization, Washington, D.C., October 4–5, 2001. This conference was sponsored by the Pan American Health Organization and the World Health Organization. Guest editors for the supplement publication were Chessa K. Lutter, Pan American Health Organization, Washington, D.C.; Kathryn G. Dewey, University of California, Davis; and Jorge L. Rosado, School of Natural Sciences, University of Queretaro, Mexico.

³ Abbreviations used: DRI, Dietary Reference Intake; EAR, Estimated Average Requirement; RDA, Recommended Dietary Allowance.

	LITERATURE CITED

TOP ABSTRACT Enhancers of nonheme iron... Enhancing properties of ascorbic... Effect of ascorbic acid... Importance of the form... Effective fortification... Conclusions and recommendations LITERATURE CITED

 

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