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Journal of the American College of Nutrition, Vol. 25, No. 1, 20-25 (2006)
Published by the American College of Nutrition

Cooking and Fe Fortification Have Different Effects on Fe Bioavailability of Bread and Tortillas

Miguel Hernández, MSc, Virginia Sousa, BChem, Salvador Villalpando, MD, PhD, Ambar Moreno, BChem, Irene Montalvo, BChem and Mardya López-Alarcón, MD, PhD

Unit of Research in Medical Nutrition, National Medical Center "Siglo XXI" (M.H., V.S., I.M., M.L.-A.)
School of Chemical Sciences (M.H., A.M., I.M.)
La Salle University, and National Institute of Public Health (S.V.), Mexico City, MEXICO

Address reprint requests to: Mardya López-Alarcón, MD, PhD, Unidad de Investigación Médica en Nutrición, Centro Médico Nacional Siglo XXI., Apartado Postal C-029 C.S.P.I. "Coahuila". Coahuila #5, Col. Roma, México D.F., 06703, MEXICO. E-mail: marsau2{at}prodigy.net.mx


   ABSTRACT
TOP
 FOOTNOTES
 ABSTRACT
INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
 REFERENCES
 
Objective: To identify iron sources for wheat- (WF) and corn-flour (CF) fortification taking into account the effect of cooking.

Methods: Sixty-six Fe-depleted rats were replete with various Fe sources. Fe bioavailability and utilization in wheat bread (WB) and corn tortillas (CT) fortified with various Fe sources was assessed after the depletion and repletion periods.

Results: Baking decreased the phytates content of WF by 97%. Improvements in Hb and FeHb were greater in rats fed unfortified WB than in those fed unfortified WF. Fe fortification had no benefit. In contrast, phytates content was unchanged by tortilla preparation, but fortification improved iron availability. Iron bioavailability indicators were best in rats fed CT fortified with ferrous sulfate and NaFe(III)EDTA than in those fed unfortified CT or CT plus reduced Fe.

Conclusion: We concluded that baking WF bread improved the bioavailability of native Fe with no further effect of fortification. Pan-cooking of lime-treated CF did not improve Fe bioavailability, but addition of Ferrous sulfate or NaFe(III)EDTA did it, despite the high phytate and calcium content of tortillas.

Key words: bioavailability, Fe, wheat bread, corn tortillas, phytates


   INTRODUCTION
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
MATERIAL AND METHODS
 RESULTS
 REFERENCES
 
Fe deficiency is a widespread phenomenon in developing countries, and anemia, its most frequent consequence, is a worldwide health problem. The primary cause of Fe deficiency is the poor bioavailability of Fe contained in grains and legumes because of their high phytic acid content [1]. Consequently, several countries have established programs to fortify flour with Fe derived from various sources. For instance, the Chilean program for fortification of wheat flour uses ferrous sulfate [2], and the Venezuelan program uses ferrous fumarate [3]. The impact of these programs has been evaluated; in Chile, for instance, the prevalence of anemia in preschool children and adolescents is less than 2%. In Venezuela, the frequency of anemia decreased from 37% to 15% in preschool children and from 19% to 10% in adolescents within two years of initiating the fortification program. In Mexico, a program for fortification of wheat and corn flour with reduced Fe was begun in 1998, but the prevalence of anemia has yet to decrease. In Mexico, the prevalence of anemia was 30% in preschool children, 23% in school children and 23% in women of reproductive age [4].

The most common source of Fe used to fortify wheat flour worldwide is reduced Fe, which has poor bioavailability [5]. Because high concentrations of reduced Fe make bread less palatable, it is unfeasible to increase concentrations further. Therefore, other Fe sources have been used. We recently demonstrated that the addition of reduced Fe to wheat or corn flour did not improve Fe status in anemic rats [6]. In contrast, Fe from other sources such as citrate, fumarate, and sulfate improved the Fe status of anemic rats when added to wheat flour, but not when added to corn flour.

Phytic acid (myo-inositol-1,2,3,4,5,6-hexakisphosphate) is the main inhibitor of Fe absorption [7]. White flour has a lower phytate content than integral flour because phytic acid is abundant in the external layer of wheat [8]. In addition, the baking process destroys phytic acid further improving Fe bioavailability [9]. The phytic acid content of tortillas does not decrease during its preparation from lime-treated corn flour. Because phytates are found in the germ portion of the grain [8], the process of nixtamalization (lime treatment) does not destroy phytates [10, 11]. In addition, calcium, which inhibits Fe absorption, is increased by nixtamalization [12–14].

Thus, it seems plausible that fortification of wheat flour with an adequate source of Fe may improve the Fe status of populations. However, in populations that are high consumers of corn tortillas (CT), alternative sources of Fe must be found in order to decrease the prevalence of Fe deficiency anemia.

The purpose of this study was to assess the effect of baking bread made of wheat flour fortified with reduced iron, ferrous sulfate, ferrous fumarate, Fe ammonium citrate, and pan-cooking tortillas made of lime-treated corn flour fortified with reduced iron, ferrous sulfate and NaFe(III)EDTA on Fe bioavailability.


   MATERIAL AND METHODS
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
RESULTS
 REFERENCES
 
Diet Composition
Wheat bread (WB) and CT were prepared from commercially available wheat flour (WF) and lime-treated corn flour (CF), respectively, either fortified or unfortified with hydrogen-reduced Fe (325 mesh). WB was also prepared from WF fortified with 20 mg/kg Fe as ferrous sulfate, ferrous fumarate, or Fe ammonium citrate. CT was also prepared from CF fortified with 30 mg/kg as reduced iron, ferrous sulfate or NaFe(III)EDTA. The amount of iron added to both types of flours was in accordance to recommendations for fortification of commercial wheat and corn flours in Mexico [15]. WB was prepared using 1 kg all-purpose WF, 60 g sugar, 24 g iodized salt, 10 g compressed yeast, and 624 mL water. Ingredients were poured into an electric oven (Bread Box, Toastmaster, model 408528, USA). The bread-making process included two steps of dough preparation, three periods of fermentation lasting 90 min in total, and baking at 190°C for 50 min. The entire process took 140 min to complete. After cooling, one portion of bread was used for measurement of water content and the other was divided into small pieces, dried at 40°C, and milled through a #40 mesh. The resulting powder was used to determine the content of phytate, calcium, and Fe bioavailability. To prepare tortillas, water was added to CF to form dough (masa flour), each tortilla was then cooked in a thin pan for 2 min. After cooling, humidity was determined and tortillas were dried, milled and analyzed as for WB.

Diet composition is presented in Table 1. Vitamin-free casein (Sigma, St Louis, MO) was used as a protein source for the low-Fe diet. Diets were prepared with either 95% CT or 85% WF (70–72% extraction) and bread, which had protein contents of 8% and 9%, respectively. AOAC methods were used to analyze the proximate composition of flour [16]. Diet samples were ashed by calcination before determination of Fe and Ca content using atomic absorption spectrometry (Perkin Elmer Analyst 300, Norwalk Connecticut). Ashes were solubilized with lanthanum chloride and deionized water to determine Ca and Fe respectively. Phytates content was analyzed using the method described by Frubbeck, Alonso, Marzo & Santidrian [17]. All experimental procedures involving laboratory animals were performed in accordance with the Mexican Official Regulations NOM-062-Z0-1999, which are similar to NIH Guidelines for experimentation in rats.


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  		Table 1. Composition (g/kg) of Low-Fe casein, Wheat flour, Wheat Bread, and Corn Tortilla Diets

 
Experimental Design
The hemoglobin (Hb) depletion-repletion method was used to determine Fe bioavailability and utilization [6]. Briefly, two separate lots of male and female Sprague-Dawley rats, 21–23 d old, were selected and placed in individual stainless-steel cages with metal-grid floors. The rats were fed a low-Fe casein diet (protein: 9%; Fe: 1.4 mg/100 g) ad libitum for 10 d. Deionized water was provided ad libitum during the experimental period. After the depletion phase, the rats were weighed, and blood samples were obtained from the tail vein for measurement of Hb concentration (initial Hb) using a portable photometer (Hemo Cue, Angel Holm, Sweden). Anemic rats of the first lot were allocated to six groups of wheat diet treatments (six rats per group), and the second lot to four groups of corn diet treatments (10 rats per group). Animals from each lot were stratified across treatments according to Hb concentrations. In the repletion period, rats consumed diets based on WF, unfortified WB, or WB fortified with 20 mg/kg of iron as either reduced Fe, ferric citrate, ferrous fumarate or ferrous sulfate for 14 d. Similarly, rats were fed unfortified CT or CT fortified with 30 mg/kg of iron as either reduced Fe, ferrous sulfate or NaFe(III)EDTA for 14 d. Groups consuming WF, unfortified WB and unfortified CT were regarded as controls for the respective treatments. During this period, weight and food intake (discounted for food spills) were recorded daily. At the end of the repletion period, a second blood sample was obtained as described previously to determine Hb concentration (final Hb).

Indices of Fe Bioavailability and Utilization
Hb and Fe variables were calculated using formulas described previously [18, 19]. Fe bioavailability was calculated from the percentage of Hb regeneration efficiency (%HRE) (Equation 1). The content of Fe in Hb (FeHb) was estimated assuming a total blood volume of 6.7% of body weight and an average Fe content of 0.335 for Hb (Equation 2). The formula for Fe utilization is shown in Equation 3.


Formula 1(Equation 1:)


Formula 2(Equation 2:)


Formula 3(Equation 3:)

Statistical Analysis
Data were assessed using The Minitab statistical software package (Minitab 14, State College, PA). Data are presented as means ± SD for each group. One-way (1 x 6 and 1 x 4) analyses of variance plus Bonferroni post hoc tests were used to compare wheat and corn diets, respectively. Pearson correlation analysis was performed to analyze associations between Fe content of diets and Fe bioavailability. A p-value < 0.05 was considered statistically significant.


   RESULTS
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
REFERENCES
 
The chemical compositions of unfortified WF, WB, and CT are presented in Table 2, and the chemical compositions of repletion diets in Table 3. The Fe content of fortified diets used in the repletion period was approximately double that of WF and unfortified bread or tortillas. The latter was the result of summing the native iron content of wheat (~26.0 mg/kg) and of corn diets (~30.5 mg/kg) to the intended fortification levels for both wheat (20 mg/kg) and corn (30 mg/kg) diets, in compliance with local regulations [15]. Phytic acid content was much higher in corn than in wheat diets. After baking, the phytate content of WB decreased significantly, but that of CT did not. The calcium content of all CT diets was significantly higher than that of wheat diets.


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  		Table 2. Chemical Composition of Wheat Flour, Dry Wheat Bread, and Dry Corn Tortillas1,2

 

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  		Table 3. Protein, Ca, Fe and Phytate Content of WF, WB and CT Diets Used during Fe Repletion of Anemic Rats

 
Tables 4 and 5 present the weights and Hb concentrations and FeHb of rats after the depletion and repletion periods for the wheat and corn diets. The improvement in Hb concentration was higher in rats fed unfortified WB than in those fed WF (85.0% vs. 47.5%, p < 0.05). Fe fortification did not confer any further benefit on Hb after baking. FeHb also improved after baking (71.6% vs. 114.0% for WF and unfortified WB, respectively, p < 0.05), but fortification did not increase FeHb further (Table 4). Baking increased %HRE for WB, but fortification decreased Fe bioavailability. In contrast, Fe utilization improved after baking and fortification with all Fe sources except citrate (Table 6).


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  		Table 4. Body Weight, Hemoglobin (Hb), and Hemoglobin Fe Content of Anemic Rats during the Repletion period; Rats Were Fed Diets Based on Wheat Flour and Bread Unfortified or Fortified with Fe from Different Compounds1

 

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  		Table 5. Body Weight, Hemoglobin (Hb) Concentration, and Hemoglobin Fe Content in Anemic Rats Fed Diets Based on Corn Tortillas Unfortified or Fortified with Different Fe Sources during the Repletion Period1

 

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  		Table 6. Hb Regeneration Efficiency (%HRE), and Fe Utilization in Anemic Rats Fed Diets Based on Unfortified WF, WB, and CT, or WB or CT Fortified with Fe from Different Sources during the Repletion Period1

 
For CT, Hb concentration improved to a greater extent in rats receiving diets fortified with NaFeEDTA (78%) or ferrous sulfate (96%) than in rats that consumed unfortified tortillas (63%) or CT plus reduced Fe (59%). However, differences for the NaFeEDTA fortified diet did not attain statistical significance. Similar results were observed for FeHb: concentrations increased by 128% in rats fed CT plus ferrous sulfate, by 90% in rats fed unfortified CT, and by 92% in rats fed CT plus reduced Fe (p < 0.05). Concentrations increased by 120% in rats fed CT fortified with NaFeEDTA, but the difference was not significant (p = 0.11) (Table 5). Fe bioavailability was lower in rats fed fortified CT than in those fed unfortified tortillas. However, Fe utilization improved in rats that consumed the diet containing ferrous sulfate (Table 6).


   DISCUSSION
 
In this study, we found that baking improved the utilization and availability of Fe in WF as efficiently as fortification with reduced Fe. We also identified ferrous sulfate as an adequate source of Fe for fortification of lime-treated corn flour, as its addition improved Fe utilization and bioavailability.

The Fe bioavailability improvement in rats fed WB seems to be related to baking (phytates destruction) and not to fortification. This effect was evident from the comparison between Hb increase in rats fed unfortified bread and those that consumed only wheat flour. This was supported by the finding that none of the various sources of Fe improved Hb over that resulting from the unfortified WB diet. In addition, bioavailability (%HRE) improved after baking, but was not improved further by fortification. A low-protein diet can affect the Fe content of Hb and the growth of rats, our results can not rule out such an effect. However, since the unfortified group presented an average weight gain that was comparable to that of groups fed fortified diets, it seems that the differential effects of increments in the iron content of Hb are still valid. A negative association between Fe concentration in the diet and Fe bioavailability has been reported previously [6, 20,21]. Likewise, in this study, the correlation coefficient between Fe concentration and %HRE was –0.914.

When analyzing Fe bioavailability it is important to begin with low values of Hb, as this condition results in a more pronounced response to Fe ingestion [22, 23]. In the present study the initial Hb concentration of rats fed wheat diets was around 80 g/L, and 72 g/L in rats fed corn diets, well below the norm of 120 g/L, assuring an appropriate low level to expect an adequate response. The CT ferrous sulfate and NaFeEDTA groups responded with increments in Hb greater than 55 g/L while the reduced Fe group did not enhance Hb concentration more than unfortified CT. This finding is in accordance with studies reporting that the utilization of Fe in ferrous sulfate and NaFeEDTA is higher than that of elemental Fe in the presence of inhibitors such as phytic acid and Ca [24].

In this study, bioavailability and utilization of Fe from WF were improved by baking. This was most likely because of the reduction of phytates (97%) resulted by the conditions used for baking such as fermentation, acidity, pH, heat, etc. The reduction in phytate may explain the similar Fe utilization response in fortified diets, as phytate destruction improved Fe utilization from bread with a low Fe content. This is in agreement with others who reported that the absorption of native Fe in WF (ferric monophytate) by the gastrointestinal tract is good in the absence of inhibitors such as phytic acid [25, 26].

In contrast, the content of phytates in CF was not modified by the process of tortilla preparation. This lack of effect of cooking on tortillas may be explained because tortilla preparation does not require fermentation and corn masa is exposed to heat only for short periods of time (2 min per tortilla). Therefore, phytates were not exposed to the phytases produced by fermentation, neither to high temperatures for a time period long enough to destroy phytates.

In the present study, we found that the amount of Fe in corn diets was variable. This high variability and phytate content indicates that a Fe fortification method that avoids the binding of Fe and phytate is required. NaFeEDTA is a potential candidate, which has been studied extensively. It has been reported that NaFeEDTA increases dietary Fe availability in the gastrointestinal tract and may improve absorption [14, 27,28]. In fact, a number of studies have reported improved Fe absorption when diets are fortified with NaFeEDTA [29–32]. However, our results demonstrated that Fe bioavailability in rats receiving NaFeEDTA-fortified CT was not improved compared with rats receiving unfortified CT. This may be because nixtamalization increases Ca content, which inhibits Fe absorption by the gastrointestinal tract, affecting nonheme and heme Fe blood concentrations [13]. However, the amount of Ca required to inhibit Fe absorption is not known, although values in the range of 80–600 mg Ca have been proposed [13,33–35]. In Mexico, the consumption of 3–4 tortillas (a normal diet) is equivalent to an intake of approximately 150 mg of Ca, which could potentially antagonize NaFeEDTA absorption.

Another important factor to consider when analyzing Fe bioavailability and utilization is the presence of enhancers in the diet. It has been reported that acids such as ascorbic acid inhibit the effect of phytate and Ca on Fe absorption [8, 36]. We tested Fe citrate, an acidic compound, because it resulted in good Fe utilization when added to wheat flour in a previous study [6]. However, when tortillas were prepared from corn flour plus Fe citrate, they acquired a green color that made them unattractive as a food item and it was therefore not used.

In summary, baking WF bread improved the bioavailability of native Fe with no further effect of fortification. Pan-cooking of lime-treated CF did not improve Fe bioavailability, but addition of Ferrous sulfate or NaFe(III)EDTA did it, despite the high phytates and calcium content of tortillas. However, it is necessary to evaluate the effect of shelf life and storage conditions on corn flour enriched with ferrous sulfate.


   FOOTNOTES
TOP
 FOOTNOTES
ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
 REFERENCES
 
Supported by grant 31033-M from CONACYT Mexico.

Received May 30, 2005. Accepted December 21, 2005.


   REFERENCES
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
 REFERENCES
 

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