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PEDIATRICS Vol. 111 No. 4 April 2003, pp. 864-870

The Role of Meat to Improve the Critical Iron Balance During Weaning

Leif Hallberg, MD, PhD, Michael Hoppe, MSci, Maria Andersson, MSci and Lena Hulthén, MDrSc

From the Department of Clinical Nutrition, Institute of Internal Medicine, Sahlgrenska Academy at Göteborg University, Göteborg, Sweden

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   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background. Iron requirements during the weaning period are the highest per unit body weight during human life, and diet is often insufficient to cover iron needs. For the first time in infant nutrition the absorption of both nonheme and heme iron from a typical weaning gruel after addition of meat with and without ascorbic acid (AA) to improve bioavailability was studied.

Methods. Nonheme and heme iron absorption from gruel was measured in 33 adults using 2 radioiron isotopes—an inorganic iron salt to label nonheme iron, the other biosynthetically labeled rabbit hemoglobin to label heme iron. Iron absorption was measured from the basal gruel (based on milkpowder and cereals) and from basal gruel added 20 g red powdered meat, alone and together with 20 mg AA in 4 different trials.

Results. Nonheme iron absorption from the basal meal was 0.33 mg/1000 kcal and the increase from added 20 mg AA was 39%, whereas addition of red meat increased nonheme iron absorption by 85%. This latter increase was unexpectedly high. Total iron absorption was further increased by heme iron absorption of 0.23 mgFe/1000 kcal. When adding both meat and AA, total iron absorption amounted to 1.08 mg iron/1000 kcal, ie, exceeding 1 mg/1000 kcal, a level estimated to correspond with daily iron requirements in 95% of infants aged 12 months.

Conclusions. Addition of powdered red meat to weaning gruels markedly increased total iron absorption. A weaning diet with added powdered meat and AA may serve as a viable option to satisfy the body’s high iron requirements during this critical period.

Key Words: weaning foods • heme and nonheme iron absorption • meat • ascorbic acid

Abbreviations: AA, ascorbic acid • SD, standard deviation • SEM, standard error of the mean


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Iron requirements during the weaning period are among the highest per unit body weight during the human life.1 The supply of iron to the full-term infant is secured during the first 4 to 6 months of life by the ingenious mechanisms during pregnancy that provide the infant with iron stores that cover the high iron requirements for growth during this first period of life. When these stores are exhausted, the iron balance situation becomes critical. The growing infant then enters the weaning period with continued high iron requirements that cannot be covered by continued lactation, which provides little iron. Therefore, weaning food with high bioavailable iron has to be given to the child during this critical period. Several reports have underlined the critical iron situation for weaning infants, in both developing countries as well as industrialized countries, strongly indicating that current weaning practices may not be sufficient to cover the needs of growing infants.1–10 Indeed, most family foods and commercial infant foods, in high use today by most populations, have low iron bioavailability.11 Current weaning diets are mainly based on cereals, milk products, fruits, and vegetables and have, because of the high content of inhibitors of iron absorption, a low iron bioavailability. Despite efforts by the food industry to improve bioavailability of iron in commercially produced weaning products, the weaning diet may not supply sufficient bioavailable iron. This could lead to an increased risk of iron deficiency with its negative and potentially irreversible impairments of mental and motor development.12–14 Significant prevalence of iron deficiency have been observed in most countries.1,2,4–7

In early man it is assumed, like in primitive societies today and among animals, that mothers prechewed the foods to the infants/offspring. By doing this their infants were secured a weaning diet with high iron bioavailability following its meat content. Moreover, the balance of evidence strongly suggests that the diet of early man had a higher nutrient density for nutrients such as iron and zinc.15

To find ways of improving the iron balance during the weaning period, the balance between different dietary factors in the weaning foods influencing bioavailability of iron need to be examined. Recent studies have shown that an increased intake of meat is associated with a better iron nutrition in the weaning period.3,16,17 The remaining problem has been how to provide the infant with meat in sufficient amounts and in a form that accounts for the infant’s inability to chew. We have experience using freeze-drying to homogenize food samples for analyses. This technique was used in the present study. The aim was to examine both the separate effect of a fine particle meat powder, and the combined effect of meat powder and ascorbic acid (AA), on iron absorption when added to an infant cereal-milk-based gruel.

Using 2 radioactive iron indicators we measured separately, and for the first time, the absorption of heme and nonheme iron from these meals. Thus, the total effect of adding meat on iron balance could be separately measured in the same individual. In another series of trials we examined the additive effect of AA.

The present trials were conducted in adults because recent studies clearly indicate that results in adults can be used to assess the influence of enhancers and inhibitors of Fe absorption in infants.18 If the study had been done in infants percent absorption values probably would have been higher. However, by using adults more sensitive and precise measurements of iron absorption using radioactive indicators could be applied in the present study.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Study Design
The absorption studies were performed in adults to examine the effect on iron absorption from a basal weaning meal, whole wheat gruel, by adding freeze-dried and pulverized red meat powder or meat powder together with AA.

The study comprised 4 trials. In trial 1 the effect on nonheme iron absorption by adding meat powder, corresponding to 20 g red meat, to the basal gruel was examined. The 2 meals, A (basal meal with added meat) and B (basal meal only), were labeled with the 2 radioiron isotopes 55Fe and 59Fe, respectively, and served on alternative days for 4 days in the order ABBA or BAAB.

In trial 2 the total iron absorption (nonheme and heme iron) from gruel containing meat powder was measured. The meal, labeled with both of the radioiron isotopes 59Fe and 55Fe, was served twice on 2 consecutive mornings. Nonheme iron in the meal was homogeneously labeled with an extrinsic 59Fe tracer. Heme iron in the same gruel was extrinsically labeled in the same way by using biosynthetically 55Fe-labeled rabbit hemoglobin.

In trial 3 the combined effect on nonheme iron absorption by adding meat powder and AA was examined. Two meals, A (basal meal with added meat and AA) and B (basal meal only), were labeled with 2 radioiron isotopes, 55Fe and 59Fe, respectively. The meals were served on alternative days for 4 days in the order ABBA or BAAB.

Trial 4 measured the total iron absorption, nonheme and heme iron, from gruel containing meat powder and AA. The meal was labeled with the 2 radioiron isotopes 59Fe and 55Fe. Heme and nonheme labeling of the meal was made in the same way as in trial 2. The meal was served twice on 2 consecutive mornings after an overnight fast.

Water (150 mL) was taken with all the meals in the 4 trials. No food or drinks were allowed for 3 hours after the meals.

The study was approved by the Ethics Committee of the Göteborg University.

Subjects
Forty-two adult healthy subjects, 23 women and 19 men aged 19 to 57 years volunteered to participate in the study. Twelve of the men and 2 of the women had served as blood donors (BDs) within the last year. None of the subjects reported any infections during the 4 weeks preceding the study. All subjects were informed in detail both in written form and orally about the purpose and procedures of the study. In most of our studies on factors influencing iron absorption over the years we have found that sample sizes between 6 and 10 subjects are suitable to detect differences of importance. With the design used based on the bioavailability of 2 radioiron isotopes, each subject serves as his own control. Subjects who had iron absorption values below 1% were excluded from the analyses because the values were too close to the isotopic background values to be reliable in the calculations of absorption. The number of remaining subjects in the 4 trials were thus 7, 8, 9, and 9 respectively, in total 33 subjects as shown in Tables 1 to 4. The iron status of each subject is described by hemoglobin concentration, serum ferritin concentration, and reference dose absorption.


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  		TABLE 1. Effect of Meat on Absorption of Nonheme Iron From a Whole-Wheat Gruel

 

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  		TABLE 4. Absorption of Nonheme and Heme Iron From a Whole-Wheat Gruel Containing Meat and AA

 
Test Meals
The basal gruel served were especially prepared by Nestlé Sweden AB (Ltd). They consisted of whole-wheat flour and milkpowder with no addition of iron or AA. Before serving, 48 g gruel powder was added to 175 mL boiling water. The native iron content in each portion was 0.8 mg. In addition, each portion was fortified before serving with ferrous sulfate to reach a final total content of nonheme iron of 2 mg iron per portion. Energy content per portion was 200 kcal, the calcium content was 224 mg, and phytate-phosphorus 40 mg per portion. Assuming a daily intake of 5 portions of basal gruel for an infant the estimated total daily energy intake would be 1000 kcal and the total daily nonheme iron intake 10 mg. The meat powder added to some of the portions was corresponding to 20 g lean meat per portion. The additional iron content from the added powdered meat was 0.32 mg heme iron and 0.32 mg nonheme iron per meal. The iron content in the meat powder added was indirect analyzed as previously described.19,20

Radioiron Labeling of the Meals and Radioisotope Measurements
Nonheme Iron
The nonheme iron was labeled with 55Fe or 59Fe as high specific activity ferric chloride. Each gruel portion was labeled just before serving with the radioiron solutions pipetted into the gruel.

Heme Iron
The heme iron in the meals was labeled with 55Fe-labeled hemoglobin prepared by intravenous administration of radioiron, 55Fe, in rabbits as described previously.19,21

Two weeks after serving the meals a whole body counting of retained 59Fe was made. At the same time a blood sample was drawn to measure the ratio of 55Fe and 59Fe in red cells to calculate the total retention in the body also of 55Fe as described previously.19 After measurement of 59Fe in the whole-body counter a reference dose of 3 mg iron labeled with 59Fe was given fasting on 2 consecutive mornings. Two weeks later a new whole body counting was made to calculate the basal iron absorption from the reference doses in each individual. This is the same procedure as used in previous studies and was first proposed by Layrisse et al.22 An informal agreement has been used to express absorption corresponding to a 40% reference dose absorption.23

Each subject received a total of 74 kBq of 55Fe and 100 kBq of 59Fe.

Statistics
Ordinary statistical methods were used to calculate means, standard deviations (SDs) and standard error of means (SEMs). Mean values were compared using the Student’s t test and analysis of variance test.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The results from the 4 trials are shown in Tables 1 to 4. Iron absorption is presented as fractional nonheme and heme iron absorption, absorption ratio heme/nonheme iron, adjusted to a 40% absorption from the reference dose and after adjustment to a total daily intake of 1000 kcal.

In trial 1 (Table 1) the nonheme iron absorption increased in all subjects when meat powder was added to the basal gruel. The average individual absorption increased by 81%. The mean calculated absorption per 1000 kcal increased from 0.29 mg ± 0.05 mg (mean ± SEM) to 0.49 mg ± 0.08 mg (P < .01).

In trial 2 (Table 2) the total average absorption of nonheme and heme iron was 0.99 mg ± 0.12 mg iron/1000 kcal. The percentage of heme iron absorption was on average close to 3 times higher than the nonheme iron absorption (ratio = 2.98).


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  		TABLE 2. Absorption of Nonheme and Heme Iron From a Whole-Wheat Gruel Containing Meat

 
In trial 3 (Table 3) the mean nonheme iron absorption increased when powdered meat and AA was added to the basal gruel. The average ratio with/without meat and AA was 2.59. The mean calculated nonheme iron absorption per 1000 kcal increased from 0.37 mg ± 0.07 mg from the basal weaning meal to 1.03 mg ± 0.25 mg.


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  		TABLE 3. Effect of Meat and AA on Nonheme Iron Absorption From a Whole-Wheat Gruel

 
In trial 4 (Table 4) the total absorption of nonheme and heme iron was 0.87 mg ± 0.15 mg/1000 kcal. The absorption ratio heme/nonheme was 2.86.

It is possible to pool results from the 4 different trials. Nonheme iron absorption from the basal meal was measured in trial 1 and in trial 3. The pooled mean nonheme iron absorption per 1000 kcal was 0.33 mg ± 0.05 mg (mean ± SEM; n = 16). The mean effect of meat given alone on nonheme iron absorption in trials 1 and 2 was 0.61 mg ± 0.07 mg/1000 kcal (n = 15). This means that there was a nearby doubling, ie, 85%, of nonheme iron absorption by the addition of 20 g meat to the basal meal (P < .01). When also AA was added to the meal in trials 3 and 4 the mean nonheme iron absorption was 0.85 mg ± 0.15 mg/1000 kcal (n = 18). This allows a calculation of the effect of AA on nonheme iron absorption by comparing this mean value with the one obtained in trials 1 and 2 above (0.61 mg). An increase of 39% of nonheme iron absorption was assignable to the effect of 20 mg AA (0.85/0.61 {Rightarrow} 39%). Heme iron was responsible for an absorption of 0.23 mg ± 0.02 mg iron as obtained by pooling the results in trials 2 and 4 (0.27 and 0.20). The total iron absorption heme and nonheme from the gruel was 0.99 mg ± 0.12 mg (trial 2) and 0.87 mg ± 0.15 mg (trial 4). This difference was not statistically different. When pooling the results of nonheme iron absorption from a gruel containing meat and AA 0.85 mg ± 0.15 mg (trials 3 and 4) and adding the absorption of pooled heme iron absorption 0.23 mg ± 0.02 mg, the total absorption was 1.08 mg/1000 kcal (Fig 1).



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  		Fig 1. The relative importance of adding meat and/or AA on the absorption of nonheme and heme iron from a typical whole grain weaning food. To a portion containing 200 kcal was added AA 20 mg which improved nonheme iron absorption by 39%; meat, 20 g, nearly doubled the absorption of nonheme iron, combination of meat and AA increased nonheme iron absorption by 2.6 times. For a total diet of 5 meals/day (1000 kcal), the heme iron present in meat further increased the absorption by 0.23 mg giving a total daily iron absorption of 1.08 mg iron per 1000 kcal (4.184 kJ)/day, thus more than tripling the total iron absorption. The total daily iron requirements of weaning infants at 12 months (1 mg/day) would thus be well-covered by the combined addition of meat and AA.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
The present results clearly indicate that the addition of meat powder to a weaning food has a marked enhancing effect on the absorption of iron. This is in agreement with an earlier study in eight infants where the effect on nonheme iron absorption of adding 25 g meat as lean beef to a home-prepared vegetable puréed meal was examined.17 In that study an absorption increase by 50% was noted.

The enhancing effect of meat on iron absorption was first noted by Layrisse24 and has later on been confirmed in several studies.25–28 The cause of the "meat effect" is not established despite many studies over several years.29 It is quite evident that meat has a counteracting effect on the inhibition of nonheme iron absorption by iron-binding polyphenols and phytates.30,31 However, this may not be the only and main effect of meat since meat has an absorption-promoting effect on both heme and nonheme iron despite the fact that these 2 kinds of iron have different mechanisms for absorption.25 In the present study the pooled effect of meat on nonheme iron absorption from trials 1 and 2 showed an absorption increase by 85%, from 0.33 mg ± 0.05 mg to 0.61 mg ± 0.07 mg/1000 kcal. This effect is significantly higher than anticipated from earlier studies on the effect of meat on iron absorption. Based on results from 15 studies by different authors in 135 subjects reviewed in a paper describing an algorithm to predict iron absorption from the composition of meals, the effect expected of meat in the present study would have been around 50%.31 It cannot be excluded that the more marked effect of powdered meat observed in the present study (85%) might be related to an effect of the more finely pulverized particles of the powdered freeze-dried meat used, making a local effect of meat on the intestinal surface more pronounced than when meat in ordinary meals is present in larger pieces.

Two methods were used to analyze the present data. To facilitate comparisons between measurements, individuals and groups, the absorption measurements obtained were adjusted to a certain iron status. This was achieved by measuring the absorption of iron from a small dose of an inorganic ferrous iron salt (3 mg Fe), the so-called reference dose, given to each subject, thus allowing all results in different subjects to be adjusted to the same iron status.

The second measure used to facilitate comparisons in the present paper was to express iron absorption in relation to iron requirements in weaning infants around 1 year of age. This was done by expressing the absorption results per unit energy. Assuming the daily energy requirements to be ~1000 kcal, at this age, the observed absorption could be related to these daily iron needs.32,33 The basal weaning gruel was fortified with iron to reach the final nonheme iron content of 2 mg per meal. For this the highly bioavailable fortificant, ferrous sulfate was used to obtain ultimate absorption and to get complete isotope exchange with the radioiron labeling method. However, it is known that ferrous sulfate causes organoleptic changes to dry-packed cereal products and may not be the optimal fortificant for dry-packed weaning food. But under experimental conditions it can be used to facilitate meaningful comparative trials.

The observed iron absorption from the basal gruel used in the present study was far below the iron requirements calculated for 1-year-old infants which has been estimated at around 1 mg/d.32,33 This was true despite the fact that the iron added to the gruel had a high bioavailability (ferrous sulfate), which may not always be the case with the iron compounds used by most producers of weaning foods. The nonheme iron absorption was only 0.33 mg—a pooled mean value of 0.29 and 0.37 mg iron/per 1000 kcal in 2 of the trials, 1 and 3.

By comparing nonheme iron absorption in trials 1 and 2 with trials 3 and 4 it was evident that addition of AA together with meat further increased the iron absorption. The absorption promoting effect of AA on nonheme iron absorption is well-known.31,34–36 The absolute enhancing effect depends on several factors such as the amount of AA present and the balance between different ligands present in the meal-enhancing or -inhibiting nonheme iron absorption. In the present study, no direct trial was made on the effect of AA on nonheme iron absorption. Indirectly, however, the effect of AA could be estimated from the mean values of nonheme iron absorption obtained when AA was present (trials 3 and 4) or not (trials 1 and 2; +39%). This is in agreement with calculated absorption ratio using the algorithm.31 Using this algorithm and calculating on adding 20 mg ascorbic to the basal gruel, the expected absorption ratio would be 1.41.

The present trials were made by adding red powdered beef meat. Studies by us and others clearly indicate that other kinds of meat, such as pork or chicken and fish, also have a promoting effect on iron absorption.26,37–39 These facts are of special importance when applying the present observations to populations in developing countries. However, when adding chicken or fish to stimulate nonheme iron absorption, the contribution of heme iron will be negligible. When adding pork meat, for example, the contribution of heme iron is only approximately one fourth to one fifth of the heme iron content of red meat.31

The relative importance of changing the composition of a weaning gruel is shown in Fig 1. We found that meat had higher promoting effect of iron absorption than AA. The importance of the heme iron in meat in weaning foods was clearly demonstrated in this paper, which is the first study where the marked contribution to total amount of iron absorbed made by heme iron in meat, was measured and demonstrated. However, it should be emphasized that giving heme iron alone, for example, as blood products, has no enhancing effect on nonheme iron absorption.25,40

An extensive cross-sectional study in 18-month-old infants in Britain showed a strong relation between poor iron status, expressed as lower serum ferritin and hemoglobin levels, and high intakes of milk and dairy products.8 Reduction of the amount of calcium, which acts as a iron absorption inhibitor, by lowering the amount of milk products in the weaning meals toward the actual calcium recommendations may be favorable and may further increase the bioavailability of its iron.41,42 This should also be favorable when adding meat to the weaning meals and still keeping the protein content constant. On the other hand, there are no data indicating that a protein intake 3 to 4 times above the requirements has any adverse effect.43

Prolonged breastfeeding in the weaning period is generally recommended.44 This will provide little iron but has other advantages. Therefore, it may be beneficial to use higher amounts of meat-iron in single weaning meals since fewer daily meals containing meat are then provided. The present paper is not a systematic study on optimal composition of complementary foods over the whole weaning period or the relative role of gruel. However, the results indicate a marked positive effect of adding meat on iron nutrition. Increased meat consumption also has additional beneficial effects as increased zinc intake.6,45,46 Thus, there are several measures to consider by the producers of foods aimed at this important age of life.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
It is evident from the present study that the addition of meat to weaning foods, especially in the finely ground form, is expected to have a very marked and favorable effect on iron balance of the weaning infant. It might be considered to be a readaptation of weaning diets presently used with regard to the infant weaning diet of early man.


   ACKNOWLEDGMENTS
 
The Danone International Prize of Nutrition (1999), which was given to the co-author Leif Hallberg, supported the study. The technical assistance performed by Elisabeth Gramatkovski is gratefully acknowledged.


   FOOTNOTES
 
Received for publication Jul 8, 2002; Accepted Nov 25, 2002.

Address correspondence to Lena Hulthén, MDrSc, Department of Clinical Nutrition, Institute of Internal Medicine, Sahlgrenska Academy at Göteborg University, S-405 30, Göteborg, Sweden. Email: lena.hulthen{at}medfak.gu.se


   REFERENCES
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 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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PEDIATRICS (ISSN 1098-4275). ©2003 by the American Academy of Pediatrics



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