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* Human Nutrition Laboratory, Institute of Food Science and Nutrition, ETH Zurich, Switzerland; Centre Suisse de Recherches Scientifiques, Abidjan, Côte d'Ivoire; and ** Programme National de Nutrition, Abidjan, Côte d'Ivoire
2 To whom correspondence should be addressed. E-mail: michael.zimmermann{at}ilw.agrl.ethz.ch.
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • iron • ferric pyrophosphate • salt • iodine • Africa
In regions of West Africa, 20–38% of school children may suffer from both iron (Fe) and iodine deficiencies (1). In countries in which existing food supplies and/or limited access fail to provide adequate levels of these nutrients in the diet, food fortification is a promising approach. However, there have been no published successful trials of food fortification with Fe in tropical Africa possibly due to other concurrent micronutrient deficiencies and the high prevalence of infection, which can reduce Fe absorption and decrease Fe mobilization from stores (2,3). Salt is one of very few food items consumed daily by rural African populations even in poor remote areas of subsistence farming (4). Salt has been iodized effectively in many African countries, and it would be advantageous to use the existing infrastructure for iodization to also fortify salt with Fe. An additional benefit of adding Fe to iodized salt, beyond the positive effect of Fe on cognitive development, school performance, immune function and work capacity (5), is that iron deficiency anemia (IDA)3 impairs thyroid metabolism and reduces the efficacy of iodine prophylaxis in areas of endemic goiter (1,6).
However, when ferrous Fe is added to low-grade iodized salt in developing countries, it causes unacceptable color changes and iodine losses (7,8). One approach is to place a barrier around ferrous Fe by encapsulation. In Morocco, a dual-fortified salt (DFS) containing ferrous sulfate encapsulated with hydrogenated oil showed good efficacy, but the salt discolored when the moisture content was high (9). Micronized ground ferric pyrophosphate (FePP) is a promising fortificant for salt (8). It has a white color and although insoluble, FePP with a mean particle size (MPS) of 2.5 µm has a relative bioavailability value (RBV) of 69% that of ferrous sulfate in rats (10). In Morocco, iodized salt (IS) fortified with micronized ground FePP (MPS of 2.5 µm) showed high efficacy in reducing IDA in children (11). However, conditions are more challenging in tropical Africa, where the ambient temperature and humidity are high, salt is typically low grade, and parasitic infections and nutrient deficiencies are common and may blunt the response to Fe interventions (12).
We fortified local, low-grade iodized salt in Côte d'Ivoire with micronized FePP and tested its stability, organoleptic qualities in traditional meals, and acceptability. We measured the efficacy of the DFS to improve iron status in a 6-mo intervention trial in iron-deficient school children in rural Côte d'Ivoire. IS was used as a control.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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27°C and a relative humidity 80% much of the year. During the 
6-mo rainy season, the village experiences daily drenching rains. Most of the foods consumed are produced locally, and the staple food is cassava. Plantain, rice, yams and dried, smoked fish are eaten regularly. Measurements of food and nutrient intake and calculation of dietary iron bioavailability. To establish the optimal fortification level for Fe in the salt, 3-d weighed food records were conducted in 24 randomly selected village households according to Hess et al. (13). In the village, family meals are traditionally eaten from shared bowls. To estimate individual food intake with greater accuracy, families ate from individual bowls during the 3 d of records.
Nutrient intakes (Fe, vitamin C, phytic acid, polyphenols, vitamin A, riboflavin) were calculated using food composition tables (4,14–17) and food analysis software EBISpro (University of Hohenheim/Stuttgart). Vitamin A intakes were calculated as retinol activity equivalents (RAEs) using a conversion factor of 12 µg ß-carotene to 1 µg retinol for a mixed diet (18,19). For ß-carotene from palm oil, the standard equivalent of 6 µg for 1 µg of RAE was used based on the presence of fat and the absence of a plant matrix (18). Dietary Fe bioavailability was estimated using the algorithms of Tseng et al. (20) and Reddy et al. (21) and adjusted for body iron stores (22). The percentage heme Fe in cooked animal products was estimated to be 60% for beef (23–26), 40% for pork (25,26), 30% for chicken (24–26), 25% for fish (25),and 10% for shrimp (25). Estimated iron bioavailability was calculated for a mean meal size consumed by children 6–15 y containing 28% sauce and 72% staple.
Salt fortification.
Iodized salt from Namibia imported by the major Abidjan salt producer (Sagid Salt) was used for the study. This salt has a slight beige color, a range of a particle size from 0.2 to 2 mm, and a NaCl content of 97%. To produce the DFS, 300 g food-grade micronized FePP (art. no. 3046449,25% Fe, mean particle size 2.5 µm, Dr. Paul Lohmann, GmbH KG), produced from regular FePP by grinding, was added to 25 kg of salt (3 mg Fe / g salt) and premixed by hand with a plastic spoon. The premix was then fed in 1 pass through a 2-m long, screw-ribbon blender set up by UNICEF at Sagid Salt for iodization. Homogeneity tests showed a homogenous mixing of the Fe into the salt after 1 pass with no further improvement with additional passes; the Fe concentration was 3.2 ± 0.2 mg Fe/g salt (n = 30) after 1 pass through the mixer. From each mixing for the DFS and from each prepackaged 25 kg bag for the IS, a sample of 30 g was collected and stored until analyzed for color, iodine, and Fe (DFS only) according to Wegmuller et al. (8).
The fortification level of 3 mg Fe/g salt was chosen on the basis of a mean per capita salt intake of 3.5 g/d in school children, an estimated iron bioavailability of 14% from the diet (see analysis of the 3-d records in the Results section), a RBV of 70% of the micronized ground FePP compared with Fe sulfate in rats (10), and the recommended level of daily Fe absorption (27).
Stability testing. DFS and IS were stored as 10- and 5-kg portions in loosely woven, high-density polyethylene bags typically used to package salt at the production site and as two 300-g portions in transparent low-density polyethylene bags typically used at the retail level and in markets. Storage conditions and the sampling procedure at mixing and after storage for 1, 2, 3, 4, 5, and 6 mo were according to a earlier publication (8). Samples were frozen at –25°C until color, iodine, and Fe (DFS only) were measured. The mean temperature and relative humidity, measured daily during the 6-mo storage period, were 27.5 ± 2.1°C and 79.3 ± 9.9%.
Organoleptic testing. For the evaluation of sensory changes of local foods, IS and DFS were added to meals prepared by local women using traditional recipes. Two equal amounts of each of the common staples (rice, yam, cassava, and plantain) were prepared in 2 pots and the same quantity of IS or DFS added. Four common sauces (tomato, eggplant, okra, and palm nut) were prepared without salt, divided into 2 equal parts, and equal amounts of IS or DFS added. The color, odor, and flavor of these foods were compared by an untrained panel of 18–21 (per session) local adults (mean age 38 y; 20% female) using triangle tests (28). In each session, 1 staple and 1 sauce were evaluated.
Efficacy study.
The subjects were 5- to15-y-old children from 4 primary schools. Informed written consent was obtained from the chief medical officer and informed oral consent from the school directors and the parents of the children. The Swiss Federal Institute of Technology in Zurich, Switzerland, and the Ministry of Health of Côte d'Ivoire gave ethical approval for the study. Oral assent was obtained from participating children. All children at the 4 schools (n = 605) were screened. Height and weight were measured, a spot urine sample was collected for measurement of urinary iodine, and blood was collected by venipuncture for the determination of hemoglobin (Hb) and serum ferritin (SF), transferrin receptor (TfR), and C-reactive protein (CRP) concentrations. Children with iron deficiency with or without anemia were invited to join the intervention trial. Anemia was defined as Hb <120 g/L in children aged 12 y, and Hb <115 g/L in children aged 5–12 y (29). Iron deficiency was indicated by serum TfR > 8.5 mg/L (30), or SF <30 µg/L (31). Two children with Hb <80 g/L were excluded and treated with oral Fe. The remaining children were divided into 2 groups: all children from 2 schools at one end of the village received the IS (n = 63); the children from 2 schools at the other end of the village received the DFS (n = 60). Both the investigators and schools were unaware of the group assignment. Each participating child was given a monthly 2.5-kg salt portion (based on a mean per capita salt intake of 4 g/d and an mean household size of 12 persons) distributed at school to be used in their household. In a village meeting at the beginning of the study and at each of the monthly salt distribution, it was emphasized that the distributed salt should be used for all cooking and food preparation, as well as at the table. At the baseline screening and again at 4 mo, all children received an oral dose of 400 mg albendazole (BELTAPHARM SPA and SmithKline Beecham Pharmaceuticals). At 6 mo, all baseline measures were repeated. To determine the prevalence of parasitic infections and micronutrient deficiencies that may influence response to the iron fortification, blood, spot urine, and stool samples were taken from subsamples of randomly selected children from all of the screened children of the 4 schools. In a first subsample, parasitic infections [malaria (n = 142), schistosomiasis (n = 144), soil transmitted helminths (n = 107)] were measured 12 mo after the intervention, and in 2 other separate random subsamples (n = 152 and 182), vitamin A (measured only in children with normal CRP) and riboflavin status were determined at the 6-mo measures.
Acceptability testing and compliance. To judge DFS and IS acceptability, household interviews were conducted after 1 and 6 mo of salt use. The head of the household answered questions on patterns of salt use, acceptability, and health benefits. Households were selected randomly including 68 IS and 75 DFS households corresponding to a total of 35% of participating households. To estimate compliance, salt remaining in the household at the end of the month was weighed and the amount of salt consumed per day during the period since the last distribution calculated. This amount was divided by the number of people in the household and compared with the mean per capita salt intake from the 3-d weighed food records.
Laboratory analysis.
Salt samples were stored at –25°C until analysis. Color was determined by colorimetry (Chroma-Meter CR-310, Minolta AG) as described in an earlier publication (8) using the Hunter Scale. The color of the DFS and IS at each time point was compared with IS at baseline and color lightness (L-value) and color difference (
E) were calculated. Salt iodine concentration was measured with a validated modified Sandell-Kolthoff method (8,32,33). The fortification level of Fe in the salt was verified by the standard addition method using flame atomic absorption spectroscopy (SpectrAA-400, Varian) according to (8).
Aliquots of serum and urine samples were frozen at –25°C until analysis. Hemoglobin was measured using an AcT8 Counter (Beckman Coulter). SF was measured using an automated chemiluminescent immunoassay system (IMMULITE, Diagnostic Products Corporation). Serum TfR was measured using an ELISA (RAMCO). Serum CRP was measured using nephelometry (TURBOX, Orion Diagnostics). CRP concentrations <10 mg/L were defined as normal (34). Body iron stores were calculated from the TfR:SF ratio (35). Only children with normal CRP concentrations at both time points, baseline and 6 mo, were included in the calculation of body iron stores. Serum retinol (SR) was measured by HPLC (Merck-Hitachi) according to Tanumihardjo et al. (36) in children with normal CRP values; vitamin A deficiency was defined as a SR <0.70 µmol/L (37). Riboflavin was measured by the erythrocyte glutathione reductase activation coefficient assay using a modification of the method of Dror et al. (38). Riboflavin deficiency was determined as activation coefficients >1.2 (39). Urinary iodine was measured using the Sandell-Kolthoff reaction as modified by Pino et al. (32). Whole blood was used to prepare a thick and a thin smear for malaria parasites by the Giemsa coloration technique from which parasites/µL of blood were determined (40). The presence of blood in urine, an indication for schistosomas, was analyzed by Dip Sticks (Roche Diagnostics). Schistosoma heamatobium infection was measured by counting eggs under the microscope in filtered spot urine samples (41). From the stool samples, a thick smear was prepared using the Kato-Katz method (42). The slides were examined using light microscopy for the presence of eggs of soil-transmitted helminths (Ascaris lumbricoides, hookworm, and Trichuris trichiura).
Statistical analysis.
Data processing and statistical analysis were done using SPSS 12.0 and Excel (XP 2002; Microsoft). Normally distributed data were expressed as means ± SD and were compared by Student's t test. Values in the text are means ± SD unless stated otherwise. Parameters not normally distributed were expressed as medians and ranges, and were compared by Mann-Whitney and Wilcoxon tests or log transformed and compared by t test. A 2-factor ANOVA was done to compare effects of time and group and time-by-group interaction for Hb, indices of Fe status, salt iodine, and salt color (lightness). T tests between groups and paired t tests within groups were done if the interaction effect was significant. The time effect for the binary variables of anemia, IDA, and iron deficiency was tested by the McNemar test and the group effect by Pearson's 
2 test. Significance was set at P < 0.05.
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RESULTS |
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Color and iodine stability.
There was no difference in color lightness between the two salts. The color difference E of 11 at 6 mo was due to the slight difference in color between the DFS (light beige) and the IS (white). Iodine loss at 6 mo was 50% for the IS and 70% for the DFS when stored in low-density polyethylene bags and close to 100% for both salts when stored in high-density polyethylene bags. The iron concentrations of the DFS at mixing and after 6 mo of storage was 3.28 ± 0.17 and 2.99 ± 0.24 mg Fe/g salt, respectively.
Organoleptic testing. In the triangle testing comparing DFS and IS, there was no detectable difference in color, odor, or taste in either the traditional staples (rice, cassava, yam, plantain) or the sauces (tomato, eggplant, okra, palm nut).
Efficacy trial. The iodine concentrations of the monthly salt aliquots (14/mo and type of salt) taken during mixing of the salt were 71.5 ± 18.6 and 53.8 ± 18.2 µg/g salt in the IS and the DFS, respectively. The iron concentration in the DFS at the monthly mixings (3–7 aliquots/mo) was 3.21 ± 0.21 mg/g salt.
The results of the screening showed that although nearly half of the children screened were anemic, the prevalence of IDA was only 12%, with another 11% of children iron deficient without anemia (Table 2). The median urinary iodine concentration was 358 µg/L (2.8 µmol/L) with a range from 19 to 1027 µg/L (0.2–8.1 µmol/L), indicating excessive iodine intake (43). The serum retinol concentration was 1.22 ± 0.38 µmol/L (measured only in children with normal CRP), and 7% of children had an SR <0.7 µmol/L, indicating very little vitamin A deficiency. The erythrocyte glutathione reductase activation coefficient (EGRAC) value was 1.26 ± 0.12, and 66% of children had a value >1.2, indicating extensive riboflavin deficiency. Overall malaria prevalence was 55%: 50 and 5% of the children were infected with Plasmodium falciparum and P. malariae, respectively. However, the parasite load was low (<10,000/µL blood) in 98% of the infected children. The prevalence of soil-transmitted helminths was only 14%, probably due to deworming 8 mo before measurement. Only 11% of the screened children had a CRP >10 mg/L.
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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FePP is a white colored, insoluble, organoleptically inert iron compound. It can be fortified into even low-grade salt without causing color changes (8). Moreover, ferric iron is more stable than ferrous iron when used in a DFS together with iodine in the form of KIO3, the form of iodine recommended for salt fortification in developing countries (43). However, the lower relative bioavailability of FePP compared with ferrous sulfate has presumably limited its use in food fortification (10,46). However, Zimmermann et al. (11) recently showed that increasing the fortification level of an iron compound can compensate for its lower bioavailability. Regular FePP (MPS 10 µm) was reported to be 20–70% the RBV of ferrous sulfate (10,46). Reducing the particle size to 0.5 µm was reported to increase RBV of FePP in milk products (47). However, we have no evidence that the micronized ground FePP (MPS of 2.5 µm) has a higher bioavailability than the regular FePP. In the present study, based on the change in body iron after 6 mo of DFS, considering the mean salt intake in school children of 3.4 g/d and the fortification level of 3 mg Fe/g salt, 3–3.5% of the fortification iron was absorbed during the study period.
An advantage to the approach to salt fortification used in this study was the achievement of a homogenous mixture of the iron into the salt with 1 pass through the local ribbon screw mixer installed by UNICEF and in place for salt iodization in many countries. Consequently, the only additional costs would be the iron compound and installation of a dry-mixing device to dose the iron into the upper basket of the screw mixer.
This study was similar to a previous study conducted in Morocco in which a DFS-containing micronized FePP decreased the prevalence of IDA in children from 31 to 3% after 10 mo (11). There are several possible explanations for the blunted response seen in Côte d'Ivoire. The present study length was 6 mo compared with 10 mo in Morocco, and the daily iron dose given here was 10 mg/d, compared with 20 mg/d in Morocco. Another difference between the 2 study sites was the food vehicle. Although in Morocco, salt was baked mainly into bread, it was primarily added to sauces in Côte d'Ivoire; thus, some FePP may have been lost in the cooking pot because it is insoluble. Along with iron deficiency, anemia in children in developing countries may be due to concurrent micronutrient deficiencies, malaria, hookworm, and hemoglobinopathies (2,48). Malaria is endemic in Côte d'Ivoire (49,50), whereas there is no malaria in northern Morocco. Although the malaria prevalence was determined in the dry season, during which malaria is less common, 55% of children had low-level parasitemia. Studies of DFS efficacy in India also reported no effect on Hb, possibly due to a high prevalence of malaria in the study population (51). Because of parasites in Côte d'Ivoire, we treated with albendazole at baseline and 4 mo. This could explain the impressive decrease in IDA in the control IS group. Hookworm and amoebae infection are common in rural Côte d'Ivoire; with studies reporting infection rates of 35–45% and 42% of hookworm and Entamoeba histolytica/E. dispar (4,49). Blood loss due to hookworm infection can contribute to iron deficiency and anemia (52) and several studies have shown a strong association between intensity of infection and anemia (53,54).
Another comorbidity that may have blunted the response to iron fortification was the poor riboflavin status in Ivorian children. Riboflavin deficiency may produce alterations in iron metabolism and Hb synthesis (2), and studies have shown the positive effect of riboflavin on iron utilization (55,56). The high prevalence of riboflavin deficiency in children in Côte d'Ivoire may have contributed to the lack of a Hb response despite an increase in body iron.
A similar pattern of response was reported in previous Fe repletion trials in tropical countries. In preschool children in Zanzibar, iron supplementation had no effect on Hb concentration or mild or moderate anemia but improved SF and erythrocyte protoporphyrin, likely due to endemic infections and concurrent nutrient deficiencies (3). Our findings indicate that a DFS-containing micronized ground FePP can increase body iron stores in children in Côte d'Ivoire, but does not increase hemoglobin. These data suggest that iron fortification programs may not be successful in reducing anemia in tropical West Africa without concurrent control of endemic parasitoses.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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3 Abbreviations used: CRP, C-reactive protein; DFS, dual-fortified salt; EAR, Estimated Average Requirement; EGRAC, erythrocyte glutathione reductase activation coefficient; FePP, ferric pyrophosphate; Hb, hemoglobin; IDA, iron deficiency anemia; IS, iodized salt; MFP, meat, fish, and poultry; MPS, mean particle size; RAE, retinol activity equivalents; RBV, relative bioavailability value; SF, serum ferritin; TfR, transferrin receptor.
Manuscript received 12 December 2005. Initial review completed 26 December 2005. Revision accepted 12 April 2006.
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