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Nutrient Physiology, Metabolism, and Nutrient-Nutrient Interactions

Meat Consumption in a Varied Diet Marginally Influences Nonheme Iron Absorption in Normal Individuals

Manju B. Reddy^*,1, Richard F. Hurrell and James D. Cook^**

^* Department of Food Science and Human Nutrition, Iowa State University, Ames, IA 50011; Institute of Food Science and Nutrition, Swiss Federal Institute of Technology, Zurich, Switzerland; and ^** Department of Medicine, Kansas University Medical Center, Kansas City, KS 66160

¹ To whom correspondence should be addressed: E-mail: mbreddy{at}iastate.edu.

	ABSTRACT

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
It is widely recognized that the intake of animal foods is the most important dietary determinant of the iron status of a population. The primary reason is the high bioavailability of heme iron, but it is also known from radiolabeled single-meal feeding studies in humans that muscle tissue facilitates absorption of nonheme iron. In the present study, we examined the effect of meat intake on nonheme iron absorption from a whole diet. Iron absorption was measured during 3 separate dietary periods in 14 volunteers (7 men and 7 women) by having them ingest a radioiron-labeled wheat roll with every meal for 5 d. The diet was freely chosen for the first dietary period and altered to eliminate or maximally increase the intake of muscle foods during the second and third periods. Nonheme iron absorption did not differ for the 3 dietary periods although the geometric mean of 4.81% when subjects consumed a freely chosen diet increased by 35% to 6.47% with maximum meat consumption (P = 0.075). When nonheme absorption was adjusted to normalize for differences in iron status using serum ferritin correction and the 3 absorption periods were pooled, multiple regression analysis indicated no significant relation with heme or nonheme iron, vitamin C, calcium, phosphorus, fiber, or tea content of the diet with the exception of animal tissue (P = 0.013). We conclude that the higher iron status associated with the consumption of an omnivorous diet is due more to the intake of heme iron than to the enhancing effect on nonheme iron absorption.

KEY WORDS: • iron bioavailability • nonheme absorption • meat • muscle foods

Radioisotopic studies of food iron absorption in human subjects during the past 60 y have identified numerous dietary factors that inhibit or facilitate the assimilation of nonheme iron. Because of the numerous inhibiting foods that are consumed with a varied diet (1), it has been impractical to reduce the intake of such foods in an effort to improve food iron bioavailability. Attention has therefore focused on increasing the content of substances that enhance the assimilation of dietary iron. The only 2 factors that have been identified to date are ascorbic acid and muscle tissue from meat, fish, and poultry. The addition of ascorbic acid to single meals fed to fasting subjects has invariably produced a dramatic increase in the absorption of nonheme iron from the meal (2). However, when absorption from a self-selected diet was examined in a recent study, no significant difference in mean absorption was observed with a range of dietary ascorbic acid of 51–247 mg/d intake (3). These results are in keeping with other reports that showed a reduced influence of dietary determinants of iron absorption when evaluated in the context of a complete diet rather than with single meals (4–6).

The effect of muscle tissue on nonheme iron absorption has been studied less extensively than that of vitamin C. A low intake of meat and meat products contributes to a higher incidence of iron deficiency in some populations despite high intake (7,8). In several studies in which meat, fish, or poultry was added to vegetarian meals, an average 2.6-fold increase in nonheme iron absorption was observed (9). In a widely used model for estimating the availability of dietary iron, 30 g of muscle tissue is considered equivalent in potency to 25 mg of ascorbic acid (10). In addition, in our previous study on assessing iron bioavailability from meal composition, animal tissue was shown to have a stronger effect on nonheme iron absorption measured from single meals compared with other dietary factors (11). On the basis of the differences in the degree of effect of dietary factors on absorption from single meals and the whole diet, we designed the present study to reexamine the enhancing effect of muscle tissue on nonheme iron absorption using a varied complete diet rather than a single meal. Nonheme iron absorption was measured by feeding radiolabeled wheat rolls during 3 separate 5-d dietary periods in the same subjects using a freely chosen diet, a vegetarian diet, and a diet in which meat, fish and poultry were increased maximally.

	SUBJECTS AND METHODS

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
    Subjects. Multiple iron absorption measurements were performed in 14 volunteers (7 men and 7 women); their mean age was 27 y with a range from 19 to 38. The participants were screened carefully before their participation to establish their ability and willingness to keep accurate detailed records of their dietary intake during the absorption studies. Video instruction was used to demonstrate the methods for estimating and recording portion sizes. The subjects were all in good health, had no gastrointestinal disorders or recent illness, and agreed to discontinue all iron and vitamin supplements for the duration of the study. Three of the women had depleted iron stores as defined by a serum ferritin concentration < 12 µg/L. The investigation was approved by the Human Subjects Committee of the Kansas University Medical Center and written informed consent was obtained from all subjects before initiating the study.

    Study design. The protocol was similar to that used recently to evaluate the effect of vitamin C (3). Double radioactive iron labels were used sequentially to obtain 4 independent measurements of iron absorption, 3 from a complete diet and 1 from a standard hamburger meal that was used to facilitate comparisons with earlier studies (4). Iron absorption was measured from a complete diet by having the subjects eat a radiolabeled bread roll with each of 3 meals for 5 d. Snacks between meals were not allowed. For the initial freely chosen diet, termed the self-selected (SS) diet, no dietary restrictions were imposed. In the remaining 2 dietary periods, the subjects were required to either eat no meat, seafood, or poultry (NM diet) or to increase maximally the intake (227–340 g) of these foods (HM diet). During the HM diet period, subjects were instructed to keep the animal product intake distributed evenly among the 3 meals. To reduce differences in protein intakes in these modified dietary periods, a list of other protein foods was given to compensate for the increase or decrease in muscle foods. No medications or dietary supplements were allowed during the entire study period. Subjects were required to maintain detailed daily records of the foods consumed during each 5-d labeling period. The dietary records for each of these labeling periods were analyzed for nutritional content using the NUTRITIONIST IV program (N-squared Computing, First Data Bank Division, Hearst Corporation). Heme iron was calculated on the assumption that 40% of the iron in animal tissue is heme iron (10). Nonheme iron was calculated as the difference between total and heme iron intake. Tea consumption was estimated using black tea equivalents: 1 cup (240 mL) of black tea = 2 cups (480 mL) of ice tea and 1.5 cups (360 mL) of herbal tea or coffee.

    Iron absorption tests. Blood (30 mL) was drawn from each subject 2 d before the initial absorption test for measurement of background blood radioactivity, serum ferritin concentration (12), and packed cell volume. Additional blood was obtained for these measurements at the beginning of wk 5 and from a final sample 2 wk after the last absorption test.

Iron absorption was measured from the SS diet as one of the initial pair of tests. The subjects reported to the laboratory each weekday morning to allow the review of dietary records from the previous day and to receive bread rolls labeled with ⁵⁵Fe to be consumed with each of the next 3 meals. The wheat rolls for each dietary labeling period were tagged extrinsically by mixing 0.1 mg iron as FeCl₃ with either ⁵⁹FeCl₃ or ⁵⁵FeCl₃ (Du Pont) with the dough before baking (13). Each roll weighed 12–13 g and contained one-fifteenth of the total dose; hence, a total dose of 37 kBq for ⁵⁹Fe or 74 kBq for ⁵⁵Fe was given with each diet.

The following week, absorption was measured from the standard meal that was fed on 2 successive mornings to minimize day-to-day variations in iron absorption. The meals were eaten between 0700 and 0900 after a minimum 10-h fast. The standard meal contained 113 g ground beef, 53 g bun, 68 g French fries, and 148 g milk shake providing 4.8 mg iron. Each meal was tagged extrinsically by pipetting 1 mL of 0.01 mol HCl/L containing 0.1 mg iron and 18.5 kBq ⁵⁹FeCl₃ onto the hamburger bun. Two weeks later, 30 mL blood was drawn to measure ⁵⁹Fe and ⁵⁵Fe in blood.

During wk 5, the HM or NM diet was tagged for 5 d using the same protocol as for the SS diet. The alternate diet was tagged during the following week. Bread rolls labeled with ⁵⁵Fe were used for the first dietary period (HM or NM) and ⁵⁹Fe tagged rolls for the second. Half of the subjects consumed the HM diet first and the NM diet second while the order was reversed in the remaining subjects. Subjects were given instructions to consume radioactive rolls with 3 main meals of the day to avoid labeling meals with low iron content. Two weeks after the final dietary labeling period, 30 mL blood was drawn to measure the increase in ⁵⁵Fe and ⁵⁹Fe in blood.

Radioactivity was measured in duplicate 10-mL blood samples by a modification of the method of Eakins and Brown (14). The percentage absorption was calculated based on the total blood volume estimated from the height and weight of each subject (15,16). The red cell incorporation of absorbed radioactivity was assumed to be 80% in all subjects (17).

    Statistical analysis. The mean daily intakes of nutrients for the SS, NM and HM diets were compared by ANOVA followed by Duncan's new multiple-range test. Iron absorption percentages were transformed to logarithms for statistical comparisons and the results recovered as antilogarithms (18) for reporting as geometric means ± SE. The differences in absorption between dietary periods were compared using appropriate contrasts from a 2-way ANOVA. Diet and subjects were used as class variables to account for the crossover design. Based on the average SD of the ratios obtained between 2 diets in various combinations, this study design had an 80% chance of detecting a ratio of 1.6 with the HM diet with a significance level of 0.05. Pearson correlation coefficients between nutrient intake and log absorption data were calculated. Multiple regression analysis with stepwise selection was used to test the combined influence of dietary factors on absorption in the SS diet as well as combining all 3 diets. The variation within subjects was removed by forcing the subjects to be part of the regression model along with the dietary variables when all 3 diets were combined. The effect was to eliminate the correlation between observations on the same subject. All statistical analyses were performed with SAS 9.1 program (SAS Institute) and differences were considered significant at P 0.05.

	RESULTS

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Protein differed significantly among the 3 labeling periods due to a lower intake during the NM dietary period (P < 0.0001), and both heme iron (P < 0.0001) and animal tissue (P < 0.0001) intakes were significantly different among the 3 diets (Table 1). Compared with the SS diet, the intake of animal tissue increased from 136 to 222 g with the HM diet.

View larger version (9K): [in this window] [in a new window]   FIGURE 1  Effect of modifying meat intake on nonheme iron absorption in 7 men and 7 women who consumed the SS, HM, and NM diets. Absorption ratios are between pairs of diets. The horizontal bars represent limits of the geometric mean ± 1 SEM. Based on 2-way ANOVA with contrasting between diets, only SS:HM was marginally different (P = 0.075).

The relation between the nutrient composition of the diet and iron absorption was examined further by multiple regression using stepwise selection. Using log absorption values adjusted to a serum ferritin concentration of 30 µg/L as the dependent variable, the relation with the intake of nutrients that were reported to influence the absorption of nonheme iron (ascorbic acid, tea, animal tissue, heme and nonheme iron, calcium, phosphorus, and fiber) was examined. The dietary variables and iron absorption from the SS diet were not associated. However, when the relation was examined in all dietary periods and the subjects were forced in the model, only 10.5% of the total 79% variation (P < 0.001) was explained by vitamin C, nonheme iron, and animal tissue. However, only animal tissue intake affected nonheme iron absorption (6% P = 0.013).

	DISCUSSION

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The majority of epidemiologic studies demonstrated a close relation between the prevalence of iron deficiency and the dietary content of animal protein. In an early report, a strong inverse correlation was observed in a Finnish study between iron status and the regional intake of meat and liquid meat products (19). In later studies, iron status was reported to be more favorable in elite runners consuming a high-meat diet (20) and better iron status was reported in postmenopausal women consuming a high-meat diet compared with lactoovovegetarians (21). Australian male vegetarians were found to have lower iron status as measured by the serum ferritin concentration despite higher iron intakes than omnivores (22). In an extensive dietary assessment of iron stores in an elderly population, the intake of heme but not nonheme iron was an important predictor of iron stores (23).

Radioisotopic studies of iron absorption in humans have provided a solid basis on which to explain these epidemiologic findings. In a classical study, Layrisse and colleagues (24) injected radioiron into animals before killing and demonstrated much higher bioavailability compared with vegetarian foods fed to humans. The key role of heme as a source of dietary iron was established when analysis of the meat homogenates demonstrated that most of the radioactivity was present as hemoglobin or myoglobin (25). Subsequent work demonstrated that dietary iron is comprised of 2 separate pools of heme and nonheme iron that differ markedly in bioavailability. Although heme iron comprises only 5–15% of the iron in a typical Western diet, it can account for more than half of the iron absorbed from the diet (26).

The Venezuelan investigators were also among the first to demonstrate the facilitating effect of animal tissue on the absorption of nonheme dietary iron (24). In a detailed review of 12 such early studies using either biosynthetically or extrinsically labeled single vegetarian meals, an average relative increase of 2.6 was observed (range, 1.1–4.4) when meat, poultry, or fish was added to the meal (9). In a later study in which beef, pork, lamb, liver, chicken, or fish was substituted in a standard meal, extrinsic tagging of the meal showed no significant differences in absorption (27). When a meal of semipurified ingredients with egg albumen as the protein source was used, substitution of these tissue foods resulted in an average 3-fold increase (range, 2.1–3.9). These and other observations led to the inclusion of meat, poultry, and fish as the major determinants of nonheme iron absorption in a widely used model for estimating the bioavailability of dietary iron (10).

Information about the mechanism by which meat influences the absorption of nonheme iron is limited. In an important early experiment, a dramatic improvement in iron absorption from black bean was observed when it was mixed with 100 g fish before administration (28). When various amino acids were added in the same proportion as the fish, neither the basic, aromatic, or aliphatic amino acids affected absorption; of the sulfur amino acids, only cysteine had a stimulating effect. This observation was confirmed in a later study in which cysteine given in gelatin capsules increased iron absorption from black bean, soybean, and maize 2-fold, although no effect was seen when the amino acid was added to these foods before cooking (29). It was postulated by these authors that cysteine acts by forming a soluble chelate with nonheme iron. They then tested the possibility that cysteine-containing peptides were released in the gut lumen during digestion of animal foods to account for the enhancing effect on iron absorption. When peptic digestion extracts from 100 g of beef were fed with a maize meal, earlier oxidation of the extract produced a 2-fold reduction in iron absorption (30). They concluded that meat facilitates absorption of nonheme iron by virtue of cysteine-containing peptides such as glutathione.

In recent years, the uptake of iron by Caco-2 cell cultures was used to screen for dietary factors that influence food iron bioavailability (31–34). Swain and co-workers (35) used cooked beef homogenates that underwent simulated gastric digestion with pepsin and pancreatin followed by ultrafiltration to screen for meat fractions that promoted radioiron uptake. They found that low-molecular-weight peptides ranging from 1–7 kDa increased iron solubility at pH 6 and promoted Caco-2 uptake fractions and that this activity increased progressively with increased histidine content. More recently, Huh et al. (34) used the uptake of radiolabeled iron and the rate of ferritin synthesis by Caco-2 cell cultures to examine the enhancing effect of acidic digests of cooked fish prepared without digestive enzymes. They observed that the most active chromatographic fractions contained negligible amounts of proteins or amino acids but were highly enriched with carbohydrates believed to be oligosaccharides originating in the extracellular matrix of muscle tissue. The widely disparate conclusions about the nature of the meat factor reported in these 2 studies could be related to differences between the active components in fish and meat muscle, the manner in which the tissue digests were prepared, or differences in Caco-2 cell uptake methodology.

There has been mounting evidence in recent years that absorption measurements using a single meal tend to exaggerate the effect of dietary factors that influence nonheme iron absorption. When absorption was measured from a complete diet using the same protocol employed in the present report, the range in absorption between an enhancing and inhibiting diet was only 2.5-fold when measured with a complete diet compared with 5.9-fold range using single meals (4). Dietary labeling has since been widely used to evaluate food iron bioavailability in humans (36). We extended our original observations in which several dietary variables were altered simultaneously (4) to the examination of isolated dietary factors that affect nonheme iron absorption from a whole diet. Calcium was shown to inhibit iron absorption from single meals but when we reduced the calcium intake in a self-selected diet from 1281 to 280 mg/d, the increase in absorption from 4.7 to 5.8% was not significant (6). Similarly, when the intake of ascorbic acid was increased from 51 to 247 mg/d, the increase in absorption from a whole diet from 5.7 to 7.7% was not significant (3).

The methodological approaches for assessing nonheme absorption from a complete diet have differed among laboratories. Our approach has been to allow our participants to choose their diet freely except with respect to the dietary variable under study. In other laboratories, the diet has been defined by the investigator and fed under careful supervision (5,37–40). However, even when the diet has been defined by the investigator, the influence of dietary factors that alter nonheme iron absorption from single meals has not always been evident. In the case of calcium, no significant effect was demonstrated when a glass of milk was fed with every meal for 4 d (37). On the other hand, a significant reduction in absorption was observed when calcium was added to a defined 10-d diet (5). Our previous results with calcium and ascorbic acid are very similar to the relatively modest difference in absorption between the vegetarian and high-meat diet observed in the present study. Although it has been difficult to demonstrate the effect of modifying a single factor when using a self-selected diet, we believe that the use of a varied diet provides a more realistic evaluation of the nutritional effect of bioavailability on nonheme iron absorption.

The degree of enhancement of nonheme iron absorption from including meat in our study supports a previous controlled 5-d feeding study that reported a 49% enhancement of nonheme iron absorption by including Danish meat in a low available meal containing low vitamin C and high phytic acid (40). Considering that they used a controlled diet, the enhancement was significant but the 35% enhancement we observed in our study was only marginally significant due to the differences in variation as stated above. We acknowledge the variation in our study, but our objective was not to add further evidence of a meat effect but rather to evaluate the effect when examined with a highly varied diet chosen within certain guidelines by the subjects rather than the investigator.

The effect of animal tissue nonheme iron absorption in multiple regression agrees well with our previous studies (3,11). Animal tissue was reported to be a strong predictor based on the algorithms developed from meal composition single-meal absorption studies (11). In an earlier similar study (3), animal tissues made a significant contribution to explaining the variability of nonheme iron absorption. With a given variation in the self-selected diets, it was interesting to see consistent results between 2 studies that were designed to look at the effect of different factors; this underscores the importance of animal tissue for iron absorption in human diets. Although the enhancement of meat from the typical self-selected diet was marginal in our study, we believe this increase may be still biologically important to improve the iron status of populations consuming diets with low bioavailabity due to low vitamin C and high phytate contents.

Our results suggest that higher iron status from consumption of an omnivorous diet is due more to the increased intake of heme iron than from the promoting effect of nonheme iron on iron absorption. Nonheme iron absorption increased from 4.8 to 6.5% with a high-meat diet, representing an additional absorption of 0.2 mg/d from the daily intake of 14 mg nonheme iron. The intake of heme iron increased from 2.8 to 4.6 mg; based on an average absorption of 30% of heme iron in an iron-replete individual (26), heme iron absorption increased by 0.54 mg/d, a nearly 3-fold greater increase than nonheme iron absorption. These rough estimates will vary considerably with the iron status of the individual, the bioavailability of the diet, and the type of muscle tissue consumed.

The inability to demonstrate isolated factors that influence iron bioavailability from a Western diet in subjects with adequate iron status should not be construed as evidence that the diet is an unimportant determinant of iron status in humans. It is likely that the facilitating effect of muscle tissue is more apparent with a more monotonous vegetarian diet that is typical in regions in which iron deficiency is prevalent. The influence of the basal diet in human studies of food iron bioavailability is an important question in future studies.

	FOOTNOTES

 
² Abbreviations used: HM, high meat; LM, low meat; SS, self-selected.

Manuscript received 17 August 2005. Initial review completed 8 September 2005. Revision accepted 15 December 2005.

	LITERATURE CITED

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

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