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© 2004 The American Society for Nutritional Sciences J. Nutr. 134:3301-3304, December 2004

Nutrient Metabolism

Particle Size Reduction and Encapsulation Affect the Bioavailability of Ferric Pyrophosphate in Rats1

Rita Wegmüller2, Michael B. Zimmermann, Diego Moretti, Myrtha Arnold*, Wolfgang Langhans* and Richard F. Hurrell

Human Nutrition Laboratory, Institute of Food Science and Nutrition and * Physiology and Animal Husbandry, Institute of Animal Sciences, Swiss Federal Institute of Technology, Zürich, Switzerland

2To whom correspondence should be addressed. E-mail: rita.wegmueller{at}ilw.agrl.ethz.ch.


   ABSTRACT
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 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Particle size is an important determinant of Fe absorption from poorly soluble Fe compounds in foods. Decreasing the particle size of elemental iron powders increases their absorption. The effect of a reduction in particle size on the bioavailability of ferric pyrophosphate (FePP) is unclear. Encapsulation of iron compounds for food fortification may protect against adverse sensory changes, but at the same time may reduce bioavailability. The hemoglobin (Hb) repletion method in weanling Sprague-Dawley rats (n = 100) was used to compare the relative bioavailability (RBV) of 4 forms of FePP: 1) regular FePP [mean particle size (MPS) {approx} 21 µm]; 2) MPS {approx} 2.5 µm; 3) MPS {approx} 2.5 µm encapsulated in hydrogenated palm oil; and 4) MPS {approx} 0.5 µm with emulsifiers. The RBV compared with ferrous sulfate was calculated by the slope-ratio technique. The RBV was 43% for encapsulated MPS {approx} 2.5 µm, significantly lower than the other FePP compounds (P < 0.05), 59% for the regular FePP, and 69% for MPS {approx} 2.5 µm, not different from each other but significantly lower than ferrous sulfate (P < 0.05), and 95% for emulsified MPS {approx} 0.5 µm, comparable to ferrous sulfate. Encapsulation of FePP with hydrogenated palm oil at a capsule:substrate ratio of 60:40 decreased RBV. Particle size reduction increases the RBV of FePP and may make this compound more useful for food fortification.

KEY WORDS: • ferric pyrophosphate • iron • bioavailability • particle size • encapsulation

Iron (Fe) deficiency anemia (IDA)3 is a major global public health problem, affecting primarily young women, infants, and children (1). Although food fortification with Fe may be an effective strategy to control IDA, successful Fe fortification of foods remains a challenge (2). Water-soluble, highly bioavailable Fe compounds often cause adverse organoleptic changes in foods. Poorly soluble Fe compounds, although more stable in foods, tend to have low bioavailability. Ferric pyrophosphate (FePP) is a white-colored, poorly soluble iron compound that does not cause sensory changes in many difficult-to-fortify food vehicles, including salt (3). However, its low bioavailability, only 30–50% of ferrous sulfate, reduces its nutritional value (4).

Particle size can be an important determinant of Fe absorption from poorly soluble Fe compounds in foods. Decreasing the particle size of elemental iron powders by 50–60%, to a mean particle size (MPS) of 7–10 µm, increases Fe absorption by ~50% in rats (5,6). In a human study, Fe absorption from hydrogen-reduced elemental Fe with particle sizes between 5 and 10 µm was comparable to that from Fe sulfate (7). Similarly, reducing the particle size of FePP may increase its absorption. Conventional grinding can decrease the MPS of FePP to 2–3 µm. Further reduction in MPS to <1 µm is possible by generating FePP particles in aqueous solutions and adding emulsifiers to prevent agglomeration (8). In a human stable isotope study, the RBV of a dispersible FePP with a MPS of 0.5 µm was comparable to that of ferrous sulfate (9). In a recent intervention trial in Moroccan children with dual-fortified salt, FePP with a MPS of 2.5 µm demonstrated high bioavailability and efficacy (10).

Fe encapsulation has the potential to help overcome several major challenges in Fe fortification of foods. It may decrease unwanted sensory changes and reduce interactions of Fe with other food components (2). However, encapsulation can adversely affect Fe bioavailability. In rat studies, encapsulation of ferrous sulfate in hydrogenated soybean oil and ferric ammonium citrate in palm oil at a ratio of capsule:substrate ≥60:40 decreases Fe RBV by ~20% (11).

To determine the potential effects of particle size reduction and encapsulation on the bioavailability of FePP, we tested the RBV of 3 FePP compounds with varying particle sizes [regular (MPS {approx} 21 µm), {approx}2.5 µm, {approx}0.5 µm] and of one encapsulated FePP (60:40 capsule:substrate) using the hemoglobin (Hb) repletion assay in rats.


   MATERIALS AND METHODS
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 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
    Iron compounds. The iron compounds tested are shown in Table 1. The encapsulated FePP was produced in our laboratory at the Swiss Federal Institute of Technology Zurich by spray cooling. The capsule was made of hydrogenated palm oil (Nutriswiss) containing 1% lecithin (Loders Croklaan). The palm oil was heated to ~85°C and a suspension containing the FePP was made. This was then passed through a screw pump (Scheerle) into a stainless steel spraying tower, atomized using air as the second medium, and cooled with liquid nitrogen.


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  		TABLE 1 Iron compounds used to fortify repletion diets

 
    Animals and diets. The Veterinary Office of the Canton of Zurich, Switzerland, approved the study. The bioavailability of the Fe compounds was determined by the Hb repletion method (12–14). Two levels of dietary iron were used for each compound. Male weanling Sprague-Dawley rats (n = 100; Charles River) at 21 d of age were housed individually in plastic cages with grated stainless steel floors, and kept under controlled conditions with a daily 12-h light:dark cycle. Millipore water (Milli-Q UF Plus, Millipore) was provided for all rats ad libitum throughout the whole study. All of the rat diets used in the study were prepared by Dyets. Rats consumed an iron-deficient diet [~2 mg Fe/kg AIN-93G purified rodent diet (15)] ad libitum for 24 d. After this depletion period, the rats were weighed and blood was collected by tail incision (16) into EDTA-coated tubes for Hb determination. Rats with Hb values between 30 and 60 g/L (mean ± SD, 44 ± 5 g/L; range 33–57 g/L) were randomly assigned to 11 groups of 8 rats. The rats consumed the same Fe-deficient diet (AIN-93G diet), but fortified with 1 of the 4 FePP compounds (each at ~10 or 20 mg Fe/kg diet), ferrous sulfate (FeSO4 · H2O; at ~10 or 20 mg Fe/kg diet), or no added Fe (~2 mg Fe/kg diet) for 14 d ad libitum. Other than their Fe content, the diets were equivalent and conformed to the recommendations for AIN-93 purified diets (15). The Fe content of all diets was verified by atomic absorption spectroscopy (SpecrAA-300/400 with GTA-96 Graphite Tube Atomizer, Varian Techtron). Individual food consumption was recorded daily throughout the repletion period. After the repletion period, rats were weighed, blood was collected by tail incision for Hb determination, and the rats were killed.

    Laboratory analysis. Hb concentration was measured in triplicate in whole blood with a commercial kit (Hb MPR 3, ref 124729, Roche Diagnostics) using the cyanmethemoglobin method (17), and commercially available control material (Digitana AG).

    Slope-ratio modeling and statistical analysis. Data processing and statistics were done using SPSS 12.0. Using the slope-ratio method, the bioavailability of each test Fe source relative to FeSO4 was calculated by comparing the change in Hb [g/(L · 14 d)] with the following: 1) the Fe level in the diet; and 2) the absolute Fe intake (µg/d) (18,19). The slope of the responses for each dietary Fe source was calculated by using a common-intercept multiple linear regression model with the "no added Fe" group serving as the blank. Linearity of the regression curves was ascertained for each Fe source separately. Tests were conducted to determine whether the mean of the blank differed significantly from the common intercept for the 4 Fe compounds. Tukey’s method was applied to test whether the slopes of the Fe compounds were significantly different from that of FeSO4 and from each other (P < 0.05). Using Fieller’s method (18), 95% CIs for relative bioavailability were obtained. Fe intake, body weight gain, and Hb change during the repletion period were expressed as mean ± SEM, n = 8/Fe compound and fortification level.


   RESULTS
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 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Fortification level, fortification Fe intake, body weight gain, and Hb change during the 14-d repletion period are shown in Table 2. The RBVs calculated using dietary fortification Fe concentration (mg/kg) and Fe intake (µg/d) are shown in Table 3. In both models, the regression lines for the Fe compounds did not significantly depart from linearity and the mean of the blank was not different from the common intercept. R2 for the models using fortification iron and Fe intake were 0.89 and 0.88, respectively, and did not differ.


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  		TABLE 2 Fortification level, fortification iron intake, body weight gain, and change in Hb in depleted rats during the repletion period1

 

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  		TABLE 3 Relative bioavailability value (RBV) of ferric pyrophosphate compounds compared with ferrous sulfate1

 
The RBV of the FePP compounds did not differ using the 2 models. The RBV of the emulsified MPS {approx} 0.5 µm was higher than that of the other FePP compounds (P < 0.05), and was not different from ferrous sulfate. The RBV of the regular FePP and the MPS {approx} 2.5 µm was 59 and 69%, respectively, significantly lower than ferrous sulfate and not different from each other (P > 0.05). The RBV of the encapsulated MPS {approx} 2.5 µm was 43%, significantly lower than that of the MPS {approx} 2.5 µm in both models and, in addition, significantly lower than the regular FePP when the dietary fortification level model was applied (Table 3). The dose-response curves on the basis of Fe fortification level (mg Fe/kg diet) or Fe intake (µg/d) and on change in Hb concentration (g/L · 14 d) are shown in Figure 1.



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  		FIGURE 1 Dose-response curves for the Hb repletion assay in depleted rats consuming a Fe-deficient diet or the Fe-deficient diet fortified (10 and 20 mg Fe/kg diet) with ferrous sulfate (Fe sulfate), ferric pyrophosphate with different particle sizes (FePP, 0.5 µm; regular FePP, 21 µm; FePP, 2.5 µm) or with encapsulated 2.5 µm ferric pyrophosphate (FePP, 2.5 µm enc.) for 14 d. Regression lines were calculated (A) on the basis of Fe fortification level (mg/kg diet) or (B) Fe intake (µg/d) and on change in Hb concentration [g/(L · 14d)]. Values are mean daily Fe intake ± SD, n = 8 for panel B and mean change in Hb concentration ± SD, n = 8 for panels A and B. The variable "b" indicates the slope of the regression line.

 

   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Particle size can be an important determinant of Fe absorption from poorly soluble Fe compounds in foods. Decreasing the particle size of elemental Fe powders significantly increases their absorption in rats (5,6) and humans (7). In a recent rat study, the bioavailability of different elemental Fe powders was compared; carbonyl Fe, with a smaller particle size than the other tested compounds, had the highest RBV (20).

FePP has a low-to-medium bioavailability, due to its slow and incomplete dissolution in the gastric juice (4). Human stable isotope studies reported that the RBV of regular FePP is only 30–40% that of ferrous sulfate and ferrous fumarate (21,22). However, several recent studies suggested that decreasing the particle size of FePP may increase its absorption. In a human study, decreasing the MPS of FePP from 8.5 to 6.7 µm increased its RBV compared with Fe sulfate from 36 to 52%, although this was not significant (P = 0.08) (22). In a recent randomized, double-blind intervention study in Morocco, dual fortification of salt with iodine and FePP with a MPS {approx} 2.5 µm at a level of 2 mg Fe/g salt was highly efficacious in reducing the prevalence of IDA among schoolchildren (10). In a rat Hb repletion study, the RBV of commercial FePP and the dispersible MPS {approx} 0.5 µm FePP were found to be 56 and 104% compared with ferrous sulfate (23). In a human stable isotope study, the absorption of dispersible MPS {approx} 0.5 µm FePP fed in a fortified infant cereal and yogurt drink was comparable to that of ferrous sulfate (9). However, it is unclear whether the high RBV of this FePP compound is due only to its small particle size or whether the surrounding emulsifiers may also play a role.

We chose the modified AOAC hemoglobin repletion method in rats to evaluate the RBV of the FePP compounds in this study. This method was validated against clinical measurements of Fe absorption in human subjects using radiotracers (14). The findings of the present study are novel in that they suggest decreasing FePP particle size from a MPS {approx} 21 µm to 2.5 µm to 0.5 µm results in a step-wise increase in absorption. The RBV of the regular FePP compound was 59%, comparable to results obtained in other studies in rats (45–58%) and humans (21–74%) (2,23). Decreasing MPS to {approx}2.5 µm increased RBV 69%; decreasing MPS to {approx}0.5 µm significantly increased RBV to 95%, a value comparable to ferrous sulfate.

Our findings also demonstrate that encapsulation of Fe compounds may reduce their bioavailability. In the present study, encapsulation of MPS {approx} 2.5 µm FePP with hydrogenated palm fat at a capsule:substrate ratio of 60:40 reduced RBV from 69 to 43% (P < 0.05). In a series of rat Hb repletion tests, the RBV of encapsulated ferrous sulfate at a 40:60 capsule:substrate ratio was comparable to that of nonencapsulated ferrous sulfate (24,25). However, the RBV of ferrous sulfate was reduced 20% when encapsulated in hydrogenated soybean oil at a capsule:substrate ratio of 60:40 (11). Similarly, the RBV of ferric ammonium citrate was reduced 25% when encapsulated in hydrogenated palm oil at a 60:40 ratio of capsule:substrate. Our findings support the recent recommendation that the bioavailability of encapsulated Fe compounds should be tested in rat Hb repletion studies before being recommended for use in food fortification (11).

Reducing the particle size of FePP may increase Fe bioavailability and make this compound more useful for food fortification. However, several questions remain. Although particle size reduction to {approx}0.5 µm clearly increases the RBV of FePP, the commercially available compound is prohibitively expensive and patented. It is unclear whether reducing particle size of FePP to 2.5 µm is justified; in the present study, although RBV was increased, the difference was not significant (P = 0.31). Processing costs to reduce particle size are high and could be a major barrier to the use of small particle size FePP in fortification programs in developing countries. If these issues can be resolved, the promise of small particle size FePP is its combination of inert sensory characteristics with good bioavailability.


   ACKNOWLEDGMENTS
 
We thank Daniel Kiechl for technical assistance in spraying the encapsulated compound and Luciano Molinari (Children’s Hospital, Zürich, Switzerland) for statistical advice. We thank Taiyo Kagaku Company, Ltd. (Mie, Japan) for providing the MPS {approx} 0.5 FePP, and Dr. Paul Lohmann (Emmerthal, Germany) for providing the remaining Fe compound.


   FOOTNOTES
 
1 Supported by the Swiss Foundation for Nutrition Research and the Swiss Federal Institute of Technology in Zürich, Switzerland, and by Dr. Paul Lohmann GmbH KG, Emmerthal, Germany. Back

3 Abbreviations used: FePP, ferric pyrophosphate; Hb, hemoglobin; IDA, iron deficiency anemia; MPS, mean particle size; RBV, relative bioavailability value. Back

Manuscript received 9 June 2004. Initial review completed 30 June 2004. Revision accepted 7 September 2004.


   LITERATURE CITED
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

1. WHO/UNICEF/UNU (1998) IDA: Prevention, Assessment and Control 1998:1-9 World Health Organization Geneva, Switzerland. Report of a joint WHO/UNICEF/UNU consultation.

2. Hurrell, R. F. (2002) Fortification: overcoming technical and practical barriers. J. Nutr. 132:806S-812S.[Abstract/Free Full Text]

3. Wegmüller, R., Zimmermann, M. B. & Hurrell, R. F. (2003) Dual fortification of salt with iodine and encapsulated iron compounds: stability and acceptability testing in Morocco and Côte d’Ivoire. J. Food Sci. 68:2129-2135.

4. Hurrell, R. F. (2002) How to ensure adequate iron absorption from iron-fortified food. Nutr. Rev. 60:S7-S15.

5. Motzok, I., Pennell, M. D., Davies, M. I. & Ross, H. U. (1975) Effect of particle size on the bioavailability of reduced iron. J. Assoc. Off. Anal. Chem. 58:99-103.[Medline]

6. Verma, R. S., Motzok, I., Chen, S. S., Rasper, J. & Ross, H. U. (1977) Effect of storage in flour and of particle size on the bioavailability of elemental iron powders for rats and humans. J. Assoc. Off. Anal. Chem. 60:759-765.[Medline]

7. Cook, J. D., Minnich, V., Moore, C. V., Rasmussen, A., Bradley, W. B. & Finch, C. A. (1973) Absorption of fortification iron in bread. Am. J. Clin. Nutr. 26:861-872.[Abstract]

8. Nanbu, H., Nakata, K., Sakaguchi, N. & Yamazaki, Y. (1998) Mineral composition. European Patent EP 0870435A1 .

9. Fidler, M. C., Walczyk, T., Davidsson, L., Zeder, C., Sakaguchi, N., Juneja, L. R. & Hurrell, R. F. (2004) A micronized, dispersible ferric pyrophosphate with high relative bioavailability in man. Br. J. Nutr. 91:107-112.[Medline]

10. Zimmermann, M. B., Wegmueller, R., Zeder, C., Chaouki, N., Rohner, F., Saïssi, M., Torresani, T. & Hurrell, R. F. (2004) Dual fortification of salt with iodine and micronized ferric pyrophosphate: a randomized, double blind, controlled trial. Am. J. Clin. Nutr. 80:952-959.[Abstract/Free Full Text]

11. Zimmermann, M. B. (2004) The potential of encapsulated iron compounds in food fortification: a review. Int. J Vitam. Nutr. Res. (in press).

12. Association of Official Analytical Chemists (1984) Bioavailability of iron: rat hemoglobin repletion bioassay. Williams, S. eds. Official Methods of Analysis 14th ed. 1984 AOAC Washington, DC. .

13. Fritz, J. C., Pla, G. W., Harrison, B. N. & Clark, G. A. (1974) Collaborative study of the rat hemoglobin repletion test for bioavailability of iron. J. Assoc. Off. Anal. Chem. 57:513-517.[Medline]

14. Forbes, A. L., Adams, C. E., Arnaud, M. J., Chichester, C. O., Cook, J. D., Harrison, B. N., Hurrell, R. F., Kahn, S. G. & Morris, E. R., et al (1989) Comparison of in vitro, animal and clinical determinations of iron bioavailability: International Nutrition Anemia Consultative Group Task Force report on iron bioavailability. Am. J. Clin Nutr. 49:225-238.[Abstract/Free Full Text]

15. Reeves, P. G., Nielsen, F. H. & Fahey, G. C., Jr (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 123:1939-1951.

16. Fluttert, M., Dalm, S. & Oitzl, M. S. (2000) A refined method for sequential blood sampling by tail incision in rats. Lab. Anim. 34:372-378.[Abstract/Free Full Text]

17. Crosby, W. H. & Munn, S. I. (1954) Standardized method for clinical hemoglobinometry. U.S. Armed Forces Med. J. 51:693-703.

18. Finney, D. J. (1978) Statistical Method in Biological Assay 1978 Charles Griffin & Company London, UK.

19. Amine, E. K. & Hegsted, D. M. (1974) Biological assessment of available iron in food products. J. Agric. Food. Chem. 22:470-476.[Medline]

20. Swain, J. H., Newman, S. M. & Hunt, J. R. (2003) Bioavailability of elemental iron powders to rats is less than bakery-grade ferrous sulfate and predicted by iron solubility and particle surface area. J. Nutr. 133:3546-3552.[Abstract/Free Full Text]

21. Davidsson, L., Kastenmayer, P., Szajewska, H., Hurrell, R. F. & Barclay, D. (2000) Iron bioavailability in infants from an infant cereal fortified with ferric pyrophosphate or ferrous fumarate. Am. J. Clin. Nutr. 71:1597-1602.[Abstract/Free Full Text]

22. Fidler, M. C., Davidsson, L., Zeder, C., Walczyk, T., Marti, I. & Hurrell, R. F. (2004) Effect of ascorbic acid and particle size on iron absorption from ferric pyrophosphate in adult women. Int. J. Vitam. Nutr. Res. 74:301-307.[Medline]

23. Sakaguchi, N., Rao, T. P., Nakata, K., Nanbu, H. & Juneja, L. R. (2004) Iron absorption and bioavailability in rats of micronized dispersible ferric pyrophosphate. Int. J. Vitam. Nutr. Res. 74:3-9.[Medline]

24. Hurrell, R. F. (1985) Nonelemental sources. Iron Fortification of Foods 1985:39-53 Academic Press Orlando, FL.

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