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Effect of Beef and Soy Proteins on the Absorption of Non-Heme Iron and Inorganic Zinc in Children

USDA/ARS Children’s Nutrition research Center (P.E., K.M.H., L.K.L., S.A.A., I.J.G.)
Section of Neonatology (S.A.A., I.J.G.), Department of Pediatrics, Baylor College of Medicine, Houston, Texas

Address reprint requests to: Ian J. Griffin, MD, USDA/ARS Children’s Nutrition Research Center, Baylor College of Medicine, 1100 Bates Street, Houston TX 77030. E-mail:igriffin{at}bcm.tmc.edu

	ABSTRACT

TOP FOOTNOTES ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS ACKNOWLEDGMENTS REFERENCES

 
Background: Iron and zinc deficiency remain substantial problems in small children in both developed and developing nations. Optimizing mineral absorption is an important strategy in minimizing this problem.

Objectives: To assess the effects of beef and soy proteins on the bioavailability of non-heme iron and zinc in children.

Methods: We measured iron (n = 26) and zinc (n = 36) absorption in 4–8 y old children from meals differing only in protein source (beef or a low-phytate soy protein concentrate). Iron and zinc absorption were measured using multi-tracer stable isotope techniques. Iron absorption was calculated from the red blood cell iron incorporation measured after 14 days and zinc absorption from the ratio of the oral and intravenous excretion of the zinc tracers 48 hours after dosing.

Results: Iron absorption from the beef meal was significantly greater (geometric mean, 7.6%) than from the soy meal (3.5%, p = 0.0015). Zinc absorption from the beef meal was greater (mean ± SD, 13.7 ± 6.0%) than from the soy meal (10.1 ± 4.1%, p = 0.047).

Conclusion: These findings indicate that beef protein increases both non-heme iron and zinc absorption compared to soy protein. The effect of protein source on non-heme iron and inorganic zinc absorption should be one of the factors taken into account when designing diets for children. The inhibitory effect of the soy based meal on iron and zinc absorption could be overcome by fortifying the soy protein with these minerals during the production process.

Key words: beef protein, iron absorption, soy protein, stable isotopes, zinc absorption

	INTRODUCTION

TOP FOOTNOTES ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS ACKNOWLEDGMENTS REFERENCES

 
Twenty five percent of the world’s population may be iron deficient and approximately 500 million people suffer from iron deficiency anemia [1]. Iron deficiency is decreasing in prevalence in the general US population [2, 3] although high risk groups in the US, and infants and small children in developing countries, remain at unacceptably high risk of iron deficiency [4]. This is of concern as there is evidence that iron deficiency in early life may lead to developmental delays that are unresponsive to subsequent iron therapy [5, 6].

In developing countries, zinc deficiency is increasingly recognized as an important health concern. Due to difficulties in assessing zinc status, the incidence of sub-optimal zinc status in developed countries is less clear. Zinc deficiency is most likely to occur in individuals with low intakes of meat or whose primary zinc sources are poorly bioavailable [7].

Beef may have a beneficial effect on iron and zinc status, not only by providing highly bioavailable sources of minerals, but possibly by increasing zinc and iron absorption from other dietary components. Several studies have suggested that the consumption of beef protein increases non-heme iron absorption from aqueous solutions [8], vegetable purées [9] or meals with high phytate content [8]. There are conflicting data on the effect of beef protein on zinc absorption. One study in adults showed no benefit of beef intake on zinc absorption from a semi-synthetic diet [10] whereas another reported a beneficial effect [11].

Soy protein has been reported to decrease iron absorption [12–15] although this effect is partly reversed by phytate reduction [14, 15]. There is little information on the effect of soy protein on zinc absorption. One study has suggested that soy protein decreases zinc absorption [10] but this may simply be due to a decrease in the zinc load of the meals [16].

To the best of our knowledge, there are no data on the relative effects of beef and soy protein on iron and zinc absorption in children.

Recently, public policy guidelines have been developed which remove previously existing limits on soy protein that can be used in programs such as the school lunch program. Formerly, soy protein could account for no more than 30% of the meat and meat alternative servings [17]. Increasing the amount of soy protein allowed in programs such as the school lunch program could be problematic if it leads to decreases in bioavailable iron and zinc in the diet of vulnerable populations. Therefore, we sought to assess the effect of beef and soy proteins on the bioavailability of non-heme iron and inorganic zinc directly in children using typical meals containing these proteins. We hypothesized that non-heme iron absorption and inorganic zinc absorption would be significantly higher in meals containing beef, rather than soy protein.

	SUBJECTS AND METHODS

TOP FOOTNOTES ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS ACKNOWLEDGMENTS REFERENCES

 
Study Subjects
Thirty-eight children age 4–8 y were recruited from the Houston metropolitan area by public advertising. Subjects were eligible for the study if they were healthy, did not suffer from any food allergies, and were not taking daily medications or herbal supplements. Eight of the recruited children were taking multivitamins, but these were discontinued at least two weeks before the start of the study. The Institutional Review Board for Baylor College of Medicine and Affiliated Hospitals (IRB) approved the protocol. Informed written consent was obtained from the parents, and verbal assent from the children.

Experimental Design
On day 1 of the study, children were admitted to the General Clinical Research Center (GCRC) at Texas Children’s Hospital. Their height and weight were measured using a stadiometer and calibrated scale, and a local anesthetic cream (Ela-Max®, Ferndale Laboratories, Inc, Ferndale, MI) was applied over a subcutaneous vein in the antecubital fossa.

Children were given a test meal of chili extrinsically labeled with zinc-67 (2 mg) as aqueous zinc chloride, and iron-58 (1 mg) as aqueous ferrous sulfate. Children were randomized to receive either the chili meal made with beef protein or with soy protein (see below). Following the consumption of the meal, the children received zinc-70 (0.5 mg) as aqueous zinc chloride intravenously. The parents of the children were given coolers containing a cup and oral and written instructions on the methods of collecting a urine sample 48 h later. Two weeks later, children returned and blood was collected for hemoglobin, ferritin, transferrin receptors and iron isotope enrichment.

Test Meal
The test meal given to the children was chili made with either beef or soy protein (Table 1). Both chilies contained the same amount of protein (11.4 g), non-heme iron (3.3 mg) and zinc (4.75 mg). The beef chili consisted of 40 g of 10% fat roast beef that was previously ground and blended to make it homogenous. The soy chili consisted of 52 g of soy crumbles from soy protein concentrate (Smart Ground^TM Original, Lightlife Foods, Turner Falls, MA). The beef and soy meals were kept frozen until the day of the study, when they were thawed and weighed. Seasoned tomato sauce was stirred into the mixture and heated in the microwave for 15 s. The subjects ate the chili with corn chips (Fritos® Scoops!® Corn Chips, Frito-Lay) and grated mild cheddar cheese.

The children were observed as they ate the test meals to ensure that all the food was consumed. Actual intakes were assessed by weighing the bowls containing the chilies before and after the meal.

Isotope Preparation
Zinc-67 (88.6% enrichment by mass), zinc-70 (95.6% enrichment by mass) and iron-58 (90.5% enrichment by mass) were purchased as the metal from Trace Sciences Inc (Ontario, Canada). Zinc isotopes were converted to aqueous solutions of zinc chloride, and iron-58 was converted to an aqueous solution of iron sulfate as previously described [18, 19]. Solutions for intravenous use were tested for sterility and pyrogenicity before use.

Sample Preparation and Analysis
Zinc was purified from the urine sample using ion exchange chromatography. Isotope enrichments were measured by magnetic sector thermal ionization mass spectrometry. Isotope ratios were expressed with respect to the non-administered isotope, zinc-66, and corrected for differences in fractionation using the zinc-64/zinc-66 ratio [19]. The tracer:tracee ratio (TTR) was calculated mathematically from the zinc-67/zinc-66 and zinc-70/zinc-66 ratios in the sample. The calculation takes into account the known distribution of isotopes in nature and in the isotopically enriched tracers. The TTR is the stable-isotope equivalent of the specific activity (used for radioactive isotopes) and represents the amount of zinc (or iron) in the sample derived from the enriched tracer, divided by the amount of zinc (or iron) present in the sample that derived from tracee present in the body prior to administration of the isotopically enriched tracers.

Iron absorption was calculated from incorporation of iron-58 into red blood cells. Isotope ratios were also measured by thermal ionization magnetic sector mass spectrometry (Finnigan MAT 261, Bremen, Germany) [18]. Ratios were expressed relative to the non-administered isotope, iron-56, and corrected for temperature specific differences in fractionation using the ratio of iron-54 to iron-56. Iron isotope ratios were converted to tracer:tracee ratios [20] from the iron-58/iron-56 and iron-57/iron-56 ratios, as described above for zinc.

Serum ferritin was measured with an electrochemiluminescence immunoassay (Elecsys 1010/2010, Roche Diagnostics Corporation, Indianapolis, IN) which consists of a double antibody sandwich method which upon application of voltage, chemiluminescence is emitted and measured by a photomultiplier. Serum transferrin receptors were determined using an enzyme immunoassay test kit (Ramco TfR test kit, Ramco Laboratories Inc., Stafford, TX).

Zinc and Iron Absorption Measurements
Zinc and iron absorption were measured as previously described [20, 21]. Briefly, zinc absorption was calculated from the fractional excretion of the oral and intravenous isotope in the 48 h urine sample [21] from the equation,

where TTR is the tracer:tracee ratio.

Red blood cell incorporation of the oral iron isotope was given by the equation

where Fe_Circ is the total amount of iron circulating as hemoglobin and is given by,

Iron absorption was then estimated by assuming that 90% of absorbed iron was incorporated into red blood cells.

Statistics and Sample Size Calculation
The sample size was designed to detect a significant effect on zinc absorption. We expected zinc absorption to average 30% (SD 6%) from the beef meal [22]. Assuming the smallest clinically significant change was a relative decrease of 20% in the soy meal (to 24%, SD 6%), two groups of 16 were required for 80% power and 0.05 type I error. Iron absorption was expected to be about 8% (SD 4%) from the beef meal [23]. Two groups of 16 would have an 80% power to detect a decrease of 4% in iron absorption from the soy meal.

Data analysis carried out after the planned number of subjects had been studied revealed a potentially clinically meaningful difference in zinc absorption between the groups that was not statistically significant (p = 0.06). Six additional subjects were recruited (with IRB approval) in order to clarify this result. These six subjects followed an identical protocol, but did not have iron absorption measured.

Iron and zinc absorption from the two meals were compared using a 2-sided t-test. In the case of iron absorption, data was also analyzed using analysis of covariance (ANCOVA) with markers of iron status as covariates (serum ferritin concentration, serum transferrin receptor concentration, and the ratio of the two). The relationship between iron absorption and iron status (as measured by the serum ferritin or serum transferrin receptor concentration) were assessed by linear regression analysis. Serum ferritin concentrations and iron absorption were log₁₀ transformed due to lack of normality.

Differences in zinc or iron absorption from the two meals were expressed as mean (95% confidence interval).

Sample size was estimated using DSTPLAN for Macintosh (MD Anderson Cancer Center, Houston, TX). Statistical analysis was carried out using StatView 5.0.1 for Macintosh (SAS Institute, Cary, NC).

Definitions of Anemia and Iron Deficiency
Anemia was defined as a hemoglobin concentration less than 11.5 g/dL as recommended by the Centers for Disease Control and Prevention [2]. A serum ferritin of less than or equal to 12 ng/ml was used as a marker of iron deficiency [2].

	RESULTS

TOP FOOTNOTES ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS ACKNOWLEDGMENTS REFERENCES

 
Subject Demographics
Thirty-eight children, 15 male and 23 female were recruited. Blood was successfully drawn for iron isotope ratios (and iron absorption measurement) from 26 children (81%), of whom 23 had sufficient serum for determination of serum ferritin, and 24 had sufficient serum for determination of serum transferrin receptor concentration. Zinc isotopes were successfully infused, and urine samples collected in 31 of the first 32 children studied, and in 5 of the 6 subsequent children studied (95% overall).

The age, weight, and heights of the subjects were not different between the two groups (Table 2).

Iron absorption was significantly negatively correlated with log₁₀ (serum ferritin) from the soy meal (r = –0.64, p = 0.019) but not from the beef meal (r = –0.10, p = 0.77) (Fig. 1). There were no significant correlations between iron absorption from either meal and the serum transferrin receptor concentration or the serum ferritin to transferrin receptor ratio.

View larger version (18K): [in this window] [in a new window]   Fig. 1. Relationship between the percent iron absorption and the log serum ferritin in the soy (upper panel) and beef (lower panel) chili meal groups.

	DISCUSSION

 
In children, consumption of meals based on beef protein led to significantly greater absorption of iron and zinc than identical meals made with soy protein. Iron absorption from the beef meal was approximately double that from the soy meal. For zinc absorption the relative increase was 35%.

The enhancing effect of meat on non-heme iron absorption has been attributed to cysteine-rich-peptides [24, 25], and to amino acids, such as histidine [26] and cysteine and peptides like glutathione [27], released during digestion [28]. The meat factor effect has also been attributed to a stimulation of gastric acid secretion, probably by the compounds, accompanied by a lowering of gastric pH that keeps the iron in a more soluble form [29]. However, this last mechanism would not explain the enhanced iron uptake which has been repeatedly shown in in vitro experiments [30–32].

Few studies have been published on the effect of beef on zinc absorption, especially in children. It appears, however, that zinc in meat products is better utilized than in plant-based sources [33–35].

Soy products contain a number of potential inhibitors of mineral absorption including phytic acid [36], particularly the inositol pentakis- and hexakis phosphates [37], and digestion products of one of the constitutive protein fractions in soybeans, conglycinin, which may inhibit iron absorption [15]. The effect of soy on iron absorption might depend on the type of soy product used, i.e. whether it is soy concentrate, soy isolate or soy flour [38, 39]. Phytic acid, on the other hand, seems to play the most important role in inhibiting zinc absorption. Phytate-zinc, phytate-zinc-calcium and phytate-zinc-calcium-amino acid complexes could apparently form during the processing of soy protein products or during the digestion process in the gastrointestinal tract. These complexes are poorly soluble and presumably, therefore, poorly absorbed which may account for the low bioavailability of zinc from soy containing products [40]. The differences we observed between the beef and soy meals probably reflect the presence of inhibitors of absorption in the soy meal as well as enhancers of absorption in the beef meal, as addition of meat to soy meals appears to improve iron [41] and zinc [42] absorption.

The phytate content of the beef meal and the soy meal (without the soy crumbles component) were 135 mg each (Nutrition Data System software, Nutrition Coordinating Center, Minneapolis, MN). Since the software program did not contain the phytate amount of soy crumbles, we measured it by the method described by Latta and Eskin [43]. The phytate content was very low: 9.2 ± 0.02 mg per 52 g of soy crumbles used in the preparation of the meal. The beef and the soy meal, therefore, contained 135 and 144 mg phytate, respectively. While considerable scientific literature indicates that phytate can decrease the uptake of minerals, the small increase (6.8%) in phytate content relative to the beef meal is unlikely to explain the lower iron and zinc bioavailability obtained from the soy meal. Instead, as mentioned previously, the differences in iron and zinc absorption that we observed between the beef and soy meals most likely reflects the presence of enhancers and other inhibitors of mineral absorption in the meals. Our results show that even low-phytate soy protein content has an adverse effect on non-heme iron and zinc bioavailability, compared to beef protein.

Zinc absorption from the beef meal was lower than expected, presumably as a result of the high levels of phytate in the both of the test meals.

The meals were designed to contain equal amounts of protein, however this lead to differences in the amount of inorganic zinc and non-heme iron present in the meals. As these differences in iron and zinc load could lead to differences in fractional absorption, independent of the effect of protein source, inorganic zinc was added to the soy meal and non-heme iron was added to the beef meal. Using this design we were able to isolate the effect of protein source on iron and zinc absorption, in meals containing equal amounts of protein, non-heme iron and inorganic zinc.

We added iron to the beef chili and zinc to the soy chili to ensure similar mineral contents between the meals. Although studies have shown that intrinsic and extrinsic labeling techniques produce similar assessments of iron [44] and zinc [45] bioavailability, we are aware that a limitation of this study might be the possible differences in mixing of the added isotope with the intrinsic metals that could explain the absorption values obtained. In the case of non-heme iron this is unlikely. If the non-heme iron intrinsic to the meals were very poorly available, addition of extra iron would be expected to "dilute" the iron isotope to a greater extent in the beef meal than in the soy meal. Therefore, we would have expected lower measured iron absorption from the beef group than from the soy group. However, we obtained a higher iron absorption value from the beef meal than from the soy meal.

This however does not apply to zinc as the labeled zinc is more diluted in the soy meal and we obtained lower zinc absorption from the soy meal than from the beef meal. However, we believe it was important to compare meals with similar iron and zinc contents to test the effect of protein on absorption, without the confounding effects of having different iron and zinc doses in the two meals. Previous studies have confirmed that extrinsic labeling is a valid method for measuring zinc absorption from foods such beef [45] and milk-based infant formulas [46], and gives results comparable to intrinsic labeling.

We noted a significant inverse relationship between iron absorption from the diet and serum ferritin in the soy group, but not the beef group. We have identified similar findings previously where iron absorption from orange juice (which contains the enhancer of iron absorption ascorbic acid) was not related to serum ferritin, but iron absorption from apple juice (which does not contain ascorbic acid) was inversely related to serum ferritin [47].

Iron absorption from the soy meal increased as iron status worsened, but no such effect was seen for the beef meal. The difference in absorption between the soy and beef meals, therefore, became less as iron status worsens. As none of our subjects was iron deficient we cannot say whether this effect continues as iron deficiency becomes apparent.

We have shown that non-heme iron and inorganic zinc absorption is lower from low-phytate soy protein based meal than from beef based meal. Clearly, this could be overcome by increasing the iron and zinc content of the soy protein through fortification during the production process. Our results suggest that nonheme iron content of soy based meal would need to be at least double that of the beef meal, and the inorganic zinc content at approximately 50% greater, to overcome the relative inhibitory effect of the soy protein.

We conclude that substitution of soy protein for beef protein reduced non-heme iron and zinc absorption. The effect is not explained by different non-heme iron or zinc loads in the different meals, but appears to be specifically related to the protein source. These effects should be one of the factors taken into account when designing diets for children.

	ACKNOWLEDGMENTS

TOP FOOTNOTES ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS ACKNOWLEDGMENTS REFERENCES

 
We would like to thank Dr E. O’Brian Smith for his statistical advice; and the nursing staff of the Metabolic Research Unit at the Children Nutrition Research Center, and the Children’s Nutrition Research Center, Texas Children’s Hospital, Baylor College of Medicine, Houston Texas for their help during the study. For assistance with the sample preparation, we thank Penni Davila-Hicks and Yana Kriseman. There was no conflict of interest. Dr. Etcheverry was responsible for the conduct of the study and Dr. Griffin was responsible for patient care and the overall interpretation of study results. Ms. Hawthorne was involved in the dietary aspects of the study, Ms. Liang was in charge of the sample analysis and data interpretation and Dr. Abrams was responsible for the overall interpretation of mass spectrometric data. All of the authors contributed to the study design, development and manuscript preparation.

	FOOTNOTES

TOP FOOTNOTES ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS ACKNOWLEDGMENTS REFERENCES

 
This work is a publication of the U.S. Department of Agriculture (USDA)/Agricultural Research Service (ARS) Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine and Texas Children’s Hospital, Houston, Texas. This project has been funded with federal funds from the USDA/ARS under Cooperative Agreement number 58-6250-6-001 and in part by beef and veal producers and importers through their $1-per-head check-off through the National Cattleman’s Beef Association (NCBA). Contents of this publication do not necessarily reflect the views or policies of the USDA, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. government.

Received March 1, 2005. Accepted December 22, 2005.

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TOP FOOTNOTES ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS ACKNOWLEDGMENTS REFERENCES

 

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