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U.S. Department of Agriculture, Agricultural Research Service, Grand Forks Human Nutrition Research Center, Grand Forks, ND
2To whom correspondence should be addressed. E-mail: jhunt{at}gfhnrc.ars.usda.gov.
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • iron absorption • elemental iron powder • food fortification • iron bioavailability • hemoglobin repletion • rats
Iron fortification of staple foods is considered to be a cost-effective, long-term strategy for reducing iron deficiency and its associated anemia, the most common nutrient deficiency in the world (1). Previously, elemental iron powders were thought to be advantageous because they do not cause unacceptable sensory changes in the fortified food and are relatively low cost. However, there has been little or no verification concerning the efficacy of elemental iron powders used widely as commercial food fortificants (2). Because production methods differ among suppliers, elemental iron powders differ physicochemically (3) and evidence suggests that these physicochemical differences substantially influence their bioavailability (4,5). More information is required on the nutritional efficacy of these powders and how efficacy relates to measurable physicochemical properties of the different elemental iron powders currently used to fortify foods (2,6).
On the basis of a review of animal (4–12) and human studies (6,13–21), an expert panel recently concluded that incomplete and inconsistent information exists on the food-grade elemental iron powders previously investigated and on iron powders currently used by the food industry (22). In most cases, the inconsistent findings may reflect the following: 1) the practice of testing elemental iron powders that were prepared experimentally and thus, are different from their commercially produced counterparts; 2) nonspecific identification of the elemental iron powders that were investigated; and 3) methodological differences (22). By the 1980s, elemental iron powders accounted for most of the iron used for food fortification in the United States (23), and the pattern of use was changing rapidly as the total iron content of the U.S. food supply continued to increase dramatically through the 1990s (24). To make specific qualitative and quantitative recommendations, more information is required on the bioavailability and physicochemistry of the current, commercially available elemental iron powders (2,22).
The specific objectives of the present investigation were as follows: 1) to determine the bioavailability of six different elemental iron powders, relative to ferrous sulfate, assessed by measuring change in hemoglobin concentration and total hemoglobin iron in rats; 2) to assess each elemental iron powder physicochemically; and 3) to determine the extent that physicochemistry predicts the bioavailability of the elemental iron powders. In addition to evaluating products recently on the market, this assessment uniquely compares an established electrolytic iron powder produced in the United States to one produced in India and includes a newer reduced iron powder from Canada that has been commonly used in cereal fortification in North America.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The six elemental iron powders [Carbonyl (Ferronyl, U.S.), Electrolytic (A-131, U.S.), Electrolytic (Electrolytic Iron, India), H-reduced (AC-325, U.S.), Reduced (ATOMET 95SP, Canada), and CO-reduced (RSI-325, Sweden)] and bakery-grade ferrous sulfate (FeSO4 · H2O)2 used in the present study were obtained from commercial suppliers in 2001 by SUSTAIN.3 The iron powders were chosen because they are currently used extensively for food fortification throughout the world. Because of proprietary constraints, specific statistics on the use of elemental iron powders found in the food supply are difficult to obtain. However, carbonyl iron powder is generally used in vitamins and pharmaceuticals, but less in foods except previously by some Northern European countries and the U.S. military. Electrolytic iron powder is used commonly to fortify infant cereals. Reduced forms of elemental iron powder are prominent in cereal flours and ready-to-eat breakfast cereals.
Descriptions of the specific elemental iron powders (e.g., carbonyl, electrolytic, reduced) generally reflect the method of production rather than the final chemical form or compound (3), which is relatively pure elemental iron (>98% iron; zero oxidation state) with >97% of the particle sizes <45 µm diameter. Once received, the elemental iron powders and ferrous sulfate were stored in a desicator under vacuum at room temperature until use.
Hemoglobin repletion tests in rats.
The relative biological value (RBV) of the six elemental iron powders was determined by a hemoglobin repletion/slope ratio method, based on the rat hemoglobin repletion bioassay of the AOAC (25), in 220 weanling (100 ± 9 g), male Sprague-Dawley rats (Charles River/SASCO, Wilmington, MA). Rats were housed individually in wire-bottomed stainless steel mesh cages under a 12-h light:dark cycle. After a 24-d depletion period with an iron-deficient diet (
1.5 mg iron/kg AIN-93G diet), the 214 rats with hemoglobin values between 30 and 60 g/L (mean ± SD of 43 ± 5 g/L; range 31 to 58 g/L) were randomly assigned by blocking on hemoglobin to one of 23 different repletion period diet groups. Rats consumed a repletion period diet (AIN-93G diet) for 14 d, fortified with one of six elemental iron powders (each 12, 24, or 36 mg iron/kg diet), bakery-grade ferrous sulfate (FeSO4 · H2O; 6, 12, 18 or 24 mg iron/kg diet), or no added iron (1.5 mg iron/kg diet); n = 9–10/diet. For bioavailability measurements, ferrous sulfate was selected as the reference standard because of its known and high bioavailability. During the repletion period, daily food consumption measurements included adjustments for food spilled. All diets and deionized, distilled water were consumed ad libitum. All experimental procedures conformed to U.S. National Institutes of Health, Public Health Service and Animal Welfare Act guidelines for the ethical treatment of laboratory animals.
Hemoglobin and hemoglobin iron determination.
At the beginning of the repletion period, rats were anesthetized with ethyl ether and blood was collected from the orbital socket. After repletion, the rats were anesthetized with ethyl ether, killed by injection with ketamine/xylazine and blood was collected from the descending vena cava. At both times, a modified methemoglobin method was used for the colorimetric determination of hemoglobin (CELL-DYN 3500 System; Abbott Diagnostics Division, Abbott Park, IL). Hemoglobin iron was determined on the basis of 3.35 mg iron/g hemoglobin and 0.075 L blood/kg body weight (26).
Animal diets.
All elemental iron powders or ferrous sulfate were incorporated into an AIN-93G (27) diet modified to lower iron contamination by using vitamin-free casein (Harlan Teklad, Madison, WI), a reagent grade calcium carbonate (J.T. Baker, Phillipsburg, NJ) and a high purity cellulose fiber source, Alphacel (ICN Biomedicals, Irvine, CA). Without added iron, the diet contained 1.6 mg iron/kg diet by analysis and contained (g/kg): 315 cornstarch, 200 vitamin-free casein, 314.5 sucrose, 70 soybean oil, 50 cellulose, 35 iron-free mineral mix (AIN-93G mineral mix omitting ferric citrate), 10 vitamin mix (AIN-93VX; Harlan Teklad, Madison, WI), 3 L-cystine, and 2.5 choline bitartrate.
Special care was taken when mixing each elemental iron powder into the experimental diets to ensure that the iron particles were not subjected to abrasive force with additional grinding or breaking, preserving the particle structure and the physicochemical characteristics of the elemental iron powders in their original commercial form. Before addition to the rest of the diet, each elemental iron powder, or ferrous sulfate, was combined with a 500-g portion of sucrose and mixed for 15 min using a nonchopping mixer (Model KSMC50 commercial mixer; KitchenAid, St. Joseph, MI) with an open-blade, plastic-covered stainless steel paddle (27). The sucrose/iron powder mixture was then added to the other dry diet ingredients and mixed (D330 mixer; Hobart, Troy, OH) for 30 min. Oil was then added and the diet was mixed for an additional 30 min.
To determine iron content, each diet (n = 6) was ashed by alternating dry heat (500°C) with reflux in concentrated nitric acid (J.T. Baker), then dissolving in 6 mol/L hydrochloric acid (J.T. Baker). Samples were analyzed by inductively coupled plasma-atomic emission spectrophotometry (ICP-AES; Optima 3100 XL; Perkin Elmer, Norwalk, CT).
Scanning electron microscopy.
Standard aluminum sample stubs were covered with double-stick cellophane tape (3M, St. Paul, MN) to receive the powders onto the exposed adhesive surface, distributed uniformly with a stainless steel spatula. Compressed tetrafluoroethane (Dust-Pro, Peca Products, Janesville, WI) was directed at the sample surface to remove loose particles, taking care to avoid contamination. The stubs were coated with 10 nm of gold/palladium (50/50 electrode) using a sputter coater (Hummer V; Anatech, Alexandria, VA), before examining in a field emission electron microscope (Model S-4700; Hitachi Scientific Instruments, Pleasanton, CA) operated at 15.0 kV and recording images (Type 55 P/N film; Polaroid, Cambridge, MA).
Physicochemical determinations.
Nanopure, analytical grade, 18.0 
M-cm water (Barnstead/Thermolyne, Dubuque, IA) was used for the physicochemical determinations. Solubility was measured (n = 3) using a method similar to that described by Forbes et al. (6) by placing 20 mg iron powder in 250 mL dilute 0.1 and 0.02 mol/L hydrochloric acid (calculated pH of 1.0 and 1.7, respectively) with constant orbital shaking (ORS 200; Boekel Scientific, Feasterville, PA) at 150 rpm and 37°C. No glass beads or magnetic stir devices were used. Iron in solution was assayed at 15, 30, 45, 60, 90, 120, and 150 min time points. Each time, shaking was stopped and 1 mL of solution was quickly taken and centrifuged (BiofugePico; Heraeus Instruments, South Plainfield, NJ) at 11,600 x g for 5 min. Immediately after centrifugation, 500 µL of the supernatant was diluted to 5 mL with 0.02 mol/L hydrochloric acid and then analyzed by ICP-AES. Solubility values are expressed as the mean ± SEM of triplicate samples determined on different days in randomized order.
Surface area was determined (Flowsorb 2300; Micromeritics Instrument, Norcross, GA) by nitrogen gas adsorption (30:70 nitrogen to helium molar ratio), based on the method of Brunauer et al. (28). Surface area values are expressed as the mean ± SEM of six adsorption measures.
Slope-ratio modeling and statistical analyses.
Data on repletion of hemoglobin concentration and change in total hemoglobin iron relative to dietary iron concentration (analyzed; mg/kg) from each iron source as well as absolute iron intake (µg/d) were analyzed by the slope-ratio assay method, expressing bioavailability relative to ferrous sulfate (29). Linearity of the regression curves was ascertained for each source of iron separately. Then, a single multiple regression model was derived to determine the slope of the responses for each of the six dietary iron sources, with the "no added iron" group serving as the blank (30). Tests were conducted to determine whether the mean of the blank differed significantly from the common intercept for the six iron powder sources. CI for relative bioavailability were obtained using Fieller’s method (29). Solubility and surface area data were analyzed using one-way ANOVA; differences among the means were tested using Tukey’s multiple comparison tests with significance set at P 
0.05 and values expressed as means ± SEM (31).
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Based on the variation in subsequent diet iron analyses, it was more difficult to mix the H- and CO-reduced iron powders homogeneously into the low iron diet. Thus, the 24-mg iron/kg H-reduced diet and the 12- and 36-mg iron/kg CO-reduced diets were remixed for an additional 15 min to obtain more homogeneous diets. Although the final variability of iron in these diets was similar to that of the other iron sources, the H-reduced diet, which was designed to contain 36 mg iron/kg, was found by analysis to contain only 27.2 mg iron/kg; if this value was undermeasured, the RBV for H-reduced iron powder may somewhat overestimate true bioavailability.
Scanning electron microscopy showed that particle surface microstructure differed among the iron powders (Fig. 2a–f). The carbonyl iron powder particles appeared smaller and spherical with a smooth surface and were more homogeneous than the other iron powders. Particles of both electrolytic and the three reduced iron powders were highly irregular. The electrolytic and H-reduced and Reduced (ATOMET 95SP) iron powders had a coarse, flake-like appearance with apparent fissures, whereas particles of the CO-reduced iron powder were less coarse with grooved surfaces.
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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These results, demonstrating that the bioavailability of elemental iron powders varies up to three times among different commercial forms, are generally consistent with previous reports (4–12,33, 38). For each type of iron powder studied previously, our RBV values were within the range of those reported for powders of a similar mesh (sieve size) specification, but higher than those with a greater proportion of larger particles.
Others (4,5) have also found highly correlated positive associations (R2 = 0.89 at 30 min and 0.90 at 10 min, both at pH 1.2) between solubility and in vivo RBV in rats. Although solubility of the powders in the present study was reproducible with low batch-to-batch variation, the relative solubilities between different powders differed consistently with pH and time. Possible explanations for the differences in this rank order based on solubility may include the differences in internal and surface microstructure among forms. The present results demonstrate that both the pH and time at which solubility is tested influence comparative results and thus, how well solubility predicts iron bioavailability.
In this study, surface area was also positively associated with in vivo RBV (R2 = 0.80; Fig. 4b), but an additional related observation suggests that there may be an upper plateau in the relation between surface area and bioavailability. In addition to the electrolytic iron powder supplied by SUSTAIN for the present study, we measured the surface area of an electrolytic iron powder of the same description from the same supplier, but produced 6 y earlier (1994–1995). Although an irradiated sample of the earlier lot had 55% RBV in piglets (38), similar to the RBV observed with rats in the present study, the nonirradiated sample from the earlier lot had twice the surface area (784 ± 3 vs. 370 ± 3 m2/kg). Extrapolation of the relation described in Figure 4b to predict bioavailability from this greater surface area would suggest an RBV greater than that of ferrous sulfate, which seems unlikely on the basis of the piglet data (38) and the high solubility and bioavailability of the latter iron salt.
On the basis of information provided by the manufacturers for each of the elemental iron powders used in this study, >97% of the iron powder particles were <45 µm in diameter. The electron micrographs of the present study (Fig. 2) demonstrate differences in particle size, especially the smaller particle size of the carbonyl iron powder, which may explain in part the increased bioavailability of this product. A reduction in the mean particle size of an elemental iron powder has generally been shown to increase RBV (4,8,39,40). However, elemental iron powders of similar particle size, manufactured by different methods, have different in vivo RBV values (40), suggesting that particle size alone does not fully explain differences in bioavailability of the iron powders.
The present results indicate that as much as 4–5 times more of the reduced iron fortificant may be required to achieve the same iron availability as bakery-grade ferrous sulfate. During the past decade, iron intake in the United States increased from 19.4 to 23.1 mg/d per person (24). A substantial proportion of this increase is due to greater consumption of iron from enriched grains and fortified ready-to-eat breakfast cereals (24). Because much of this iron is from reduced iron powders (23), which are not as bioavailable as other forms of nonheme iron, this expansion in intake to 23.1 mg/d likely does not reflect a corresponding increase in bioavailable iron. Algorithms used to estimate the bioavailability of nonheme iron from meal composition (41) may overestimate bioavailable iron if some of the nonheme iron is from an elemental iron powder.
The cost of different elemental iron powders also varies, typically as much as sixfold among the forms of elemental iron powder tested in this study, with carbonyl iron powder being the most and the reduced forms the least expensive (42,43). Although differences in RBV exist among elemental iron powders, when cost is considered, it may still be reasonable to fortify foods using greater quantities of a less bioavailable form.
Our findings show that iron from the commercially produced elemental iron powders used in this study was only 21–64% as bioavailable as iron in the form of bakery-grade ferrous sulfate. Our data also suggest that solubility in dilute hydrochloric acid at pH 1.0 at 30 min and iron powder particle surface area were more predictive of iron bioavailability in rats than solubility at pH 1.7 at any time. Further study is recommended before relying solely on either of these physicochemical measures to predict iron bioavailability, but the present findings support the measure of iron solubility in dilute hydrochloric acid at pH 1.0 as a rapid, inexpensive estimate of iron bioavailability. Current guidelines (44) for iron fortification of foods with elemental iron powders consider the bioavailability data adequate only for electrolytic iron; with bioavailability 50% that of ferrous sulfate, twice as much iron is recommended when this source is used. The present findings, together with data in humans and information on commercial pricing of iron powders, can assist in the development of qualitative and quantitative recommendations for fortification of foods with elemental iron powders.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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3 Abbreviations used: FeSO4 · H2O, ferrous sulfate monohydrate, bakery-grade; ICP-AES, inductively coupled plasma-atomic emission spectrophotometry; RBV, relative biological value.
4 Elemental iron powders and ferrous sulfate used in the present study were obtained from commercial suppliers in 2001 by the SUSTAIN (Sharing U.S. Technology to Aid in the Improvement of Nutrition, Washington, D.C.) organization. This research was conducted collaboratively with SUSTAIN and its partners as part of its overall review of the bioavailability of elemental iron powders. Under our agreement with SUSTAIN, specific producer names have not been used, but this collection of samples reflects the products and production methods prominent on the market in 2001.
Manuscript received 2 May 2003. Initial review completed 11 June 2003. Revision accepted 27 August 2003.
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LITERATURE CITED |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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