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SEAMEO-TROPMED Regional Center for Community Nutrition, University of Indonesia, Jakarta, Indonesia
4To whom correspondence should be addressed. E-mail: ekaryadi{at}dr.com.
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • infants • iron • vitamin A • zinc • multiple micronutrient supplement
Micronutrient malnutrition is an important problem among preschool children in most developing countries, including those in Southeast Asia (1). A recent study in Indonesian infants showed that the prevalence of marginal vitamin A deficiency was 54%, iron deficiency anemia was >50% and zinc deficiency was 17% (2).
The consequences of micronutrient deficiencies during childhood are considerable. Iron deficiency has a negative effect on the motor and mental development of young children (3) and causes anemia. In addition to its adverse effect on vision, vitamin A deficiency increases the risk of mortality (4). Zinc deficiency negatively influences growth (5–7) and increases the risk of diarrhea and respiratory infections (8–10).
Because multiple deficiencies coexist, there has been increased interest in the potential benefits of multiple micronutrient supplements. Combining multiple micronutrients in a single delivery mechanism may be a cost-effective way to achieve multiple benefits (11,12). Supplementation of young children with multiple micronutrients may be of special benefit, because of the practical difficulties encountered in improving the nutritional adequacy of traditional complementary foods. It is difficult to meet nutrient needs of infants with foods, especially those whose consumption of animal source foods is low. However, with large-scale supplementation programs, factors such as cost, availability, poor distribution of supplements, and low compliance often reduce program effectiveness, as experienced with iron supplementation programs for pregnant women (13). Some have questioned the effectiveness of multimicronutrients combined within a supplement, because of possible adverse interactions among the nutrients or interference with their absorption (14,15). Supplementation on a weekly basis, instead of daily, is cheaper (16) and may be easier to manage. Program compliance may also be better (17). A previous study in young Vietnamese children showed that weekly supplementation with multiple micronutrients was as effective as daily supplementation for improving hemoglobin, serum zinc, and retinol concentrations (17).
The present study compared the efficacy of weekly and of daily multiple micronutrient supplementation and daily iron (DI)6 supplementation, for improving anemia and micronutrient status. Furthermore, the effect of supplementation on growth and morbidity was investigated.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Study design and randomization
The study was conducted in the subdistricts of Salam and Ngluwar, in the district of Magelang, province of Central Java, Indonesia. The area was selected based on the nutritional situation of the <5 y old children, according to the requirements of the IRIS study protocol. Prerequisite criteria were a >30% prevalence of anemia among infants and children under five (hemoglobin < 110 g/L) and >30% prevalence of vitamin A deficiency (serum retinol < 20 µg/L). The prevalence of anemia among children <5 y old in the selected area was 54.3%, the prevalence of underweight was 34.8% (18), and of marginal vitamin A deficiency, about 54% (2).
The study started in June 2000 with a baseline survey, with supplementation from July 2000 through December 2000 for a period of 23 wk. This period was 2 wk shorter than the original plan of 25 wk, due to a Muslim festival celebrated by the majority of the subjects studied. Inclusion criteria of subjects in the selected area were as follows: age 6–12 mo, willingness to participate, normal birth history, and apparently healthy. Exclusion criteria were severe wasting [< –3 weight-for-length Z score (WLZ)], fever (>39°C), severe anemia (hemoglobin < 80 g/L), premature birth of the child (<37 wk), low birth weight (<2500 g), and presence of congenital defects and chronic illness.
The study was a randomized, double-blind, placebo-controlled trial. The sample size was calculated for the 4 country sites combined, based on the comparison of a decline in standardized weight for age from –0.65 to –0.95 for the intervention groups compared with a decline from –0.65 to –1.20 in the placebo (P) group. For a two-group, repeated measures ANOVA with 7 levels (mo 0 to 6) a sample size of 256 per group would provide the analysis with 80% power when the significance level is 5%. The aim was to include at least 70 infants per group (65 + 5 dropouts) in each country. At the beginning of the study, 284 infants aged 6 to 12 mo were randomly selected from a list of infants in the selected area. They were then randomly allocated to 4 different groups of treatment. If one family had more than one child that fulfilled the study requirements, all children were included and were treated individually but in the same intervention group. Group 1 received the multiple micronutrient supplement on a daily basis (DMM group). The second group received a multiple micronutrient supplement on one day of the week plus a daily placebo for the other 6 d (WMM group). The third group received an iron supplement on a daily basis (DI group), and the fourth group received a placebo daily (P group).
Interventions
To have a uniform product, the micronutrient supplement and placebo treatments were developed and produced centrally, and were distributed to each country site. The supplements developed were chewable tablets or foodlets, with the same color and flavor that would be attractive for toddlers (Roche Laboratories). The foodlets were packaged in identical-looking coded blister packs, each with 7 doses, one for each day of the week, as has been described previously (18). The DMM supplement contained 15 micronutrients, including iron, zinc, copper, and iodine, and vitamins A, D, E, K, C, and B at the daily adequate intake level for young children (19). The WMM supplement had twice the daily adequate intake amounts of the same micronutrients but was only given on one day of the week; the P supplement was given the other days. The DI supplement contained 10 mg of iron as ferrous sulfate and was given daily. The P supplement contained no nutrients. In all groups, the foodlets were administered for 23 wk for 7 d/wk, of which 6 d/wk foodlets were given directly to the infants at their homes by trained field assistants under the supervision of the research team, with compliance recorded. On day 7, the mother gave the supplement to her infant. The authors, the health staff, and the patients were unaware of the treatment codes until the study was completed. Number codes (1, 2, 3, and 4) were kept by UNICEF (United Nations Children’s Fund) and were not broken prior to statistical analyses.
Data collection and measurements
Socioeconomic data were collected by a questionnaire after the guidelines for nutrition baseline surveys in communities, followed by all IRIS studies (20). Weight was recorded to the nearest 0.1 kg, with the child minimally clothed, using an electronic weighing scale (SECA 770). Length was recorded to the nearest 0.1 cm, with the child lying down, using the WHO recommended length-measuring board for infants (Ahrtag). The body weight and the height of the mothers were measured at the beginning of the study. Subjects were weighed without shoes, using an electronic platform model weighing scale (SECA 770 alpha; SECA) to the nearest 0.1 kg, and height was recorded to the nearest 0.1 cm using a microtoise (21).
Child morbidity was measured in various ways during the 6-mo supplementation period. Whether the mother reported that the child had diarrhea (more than 4 runny stools), acute respiratory infection (cough, runny nose), or fever the day before was recorded. The mother was also asked about frequency of visits to health service to treat sickness of the child during the previous week.
Blood samples were collected at baseline and at the end of the study for biochemical analysis. Venous blood was collected using 2-mL vacuette heparin tubes with butterfly and luer adapters (Greiner). The tubes were immediately put in a cooled Styrofoam (Pt. Garinda) box and within 6 h were centrifuged at 
5000 x g for 5 min. Blood hemoglobin concentration was determined locally using the cyanomethemoglobin method (22), in which 20 µL whole fresh blood from the vacuettes was mixed with 5 mL of Drabkin solution and measured by a standard photometer. The plasma was transferred into two 500 µL Eppendorf Safe Lock cups (at least 400 µL in the first one). Plasma was stored at –70°C until transportation on dry ice to the Micronutrient Laboratory, University of Hohenheim, Germany. All procedures were done as quickly as possible and were protected from direct light. To avoid the risk of zinc contamination, all tubes and tips were trace-element free and were handled very carefully to avoid contact with dust. To reduce variation, all supplies for blood collection and storage were from the same batch and were provided by the Micronutrient Laboratory. Plasma ferritin was measured by a standard ELISA procedure (DAKO). Plasma retinol and 
-tocopherol were analyzed by HPLC according to Erhardt et al. (23). Plasma zinc concentrations were analyzed by electrothermal atomic absorption spectrophotometry according to the manufacturer’s instructions (Perkin Elmer). Riboflavin status was assessed by calculating the activation coefficient of the erythrocyte glutathione reductase (EGRAC), with and without added riboflavin (24). Plasma homocysteine levels were measured by HPLC (25). Plasma C-reactive protein (CRP), as an indicator of current infection, was assessed using the ELISA procedure (DAKO). Cutoff values for deficiency were <10 g/L for hemoglobin, <0.7 µmol/L for plasma retinol, <12 µg/L for plasma ferritin, and <0.7 µmol/L for plasma zinc.
Ethical considerations
The guidelines on ethics for biomedical research involving human subjects of the Council for International Organizations of Medical Sciences were followed (26). Before the study, mothers of the selected infants were informed by the investigators about the purpose and the protocol of the study. Assurance was given that participation was voluntary and that no negative consequences would result for those who decided not to participate in the study. The Ethical Committee for Study in Human from the Faculty of Medicine, University of Indonesia, Jakarta, Indonesia, approved the study protocol prior to implementation. At the end of the supplementation trial, the placebo group was supplemented with the WMM supplement for 3 mo.
Statistical analysis
Data were analyzed using SPSS windows version 10.0 (SPSS). Each dependent variable was tested for homogeneity of its variance using the Kolmogorov-Smirnov test. Data are reported as mean and SD or SEM for the normally distributed variables and as median and range for the non-normally distributed variables. Differences in prevalence were tested with a Pearson chi-square test. Differences among groups were examined using ANOVA for parametric variables, and the Mann-Whitney test or the Kruskal-Wallis test for nonparametric variables. A paired t test was used to evaluate the changes over time within each group for parametric variables, and the Wilcoxon’s test for nonparametric variables. The McNemar’s test was applied to measure the differences in the number of subjects within the groups after supplementation. Values of P < 0.05 were considered to be significant. Infants with plasma CRP concentrations > 12 mg/L were excluded from statistical analyses of plasma ferritin, zinc, and retinol concentrations, because these are altered by the acute infection or inflammatory process.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Even though the prevalence of iron deficiency anemia at baseline was >50%, and the severity of anemia of most of the infants was mild, the supplements still did not eliminate anemia. The DMM supplement and DI supplement significantly increased hemoglobin and plasma ferritin concentrations. This finding indicates that a small daily supplementation of iron during 23 wk of infancy, either alone or in combination with other micronutrients, is sufficient to increase the iron stores so that only 4% of children were iron deficient posttreatment. Despite this apparent iron repletion, anemia still persisted, with a third of subjects in the DMM group still anemic posttreatment. When the data were pooled, the benefit in terms of increased hemoglobin was greatest in those that were initially anemic, which is as one would expect. However, the greatest increase in hemoglobin levels in anemic infants was found in the DMM supplemented group, suggesting that the other micronutrients in DMM supplements have a beneficial effect on hemoglobin over and above that of just iron. Why the supplement, although it corrected iron deficiency, did not eliminate anemia is not clear. It may be because of infections and or other micronutrient deficiencies not covered by the supplement.
The change in plasma zinc concentration with supplementation was significantly different among treatment and P groups. Plasma zinc concentrations fell in all groups, except in the DMM group, so that, whereas there was little or no zinc deficiency in the DMM group at the end of the study, the other groups had 10 to 30% prevalence of deficiency. Considering that almost all (97%) of the infants were being fed rice-based complementary food starting from 6 mo of age, the natural zinc in these foods may have been poorly absorbed when consumed with the high phytate in the diets (29). However, the level of zinc in the DMM supplement seems to be sufficient to overcome this. The highest prevalence of zinc deficiency was found in the DI supplemented group after 23 wk of supplementation, probably due to the interactions between zinc and iron, and/or between these micronutrients and other components present in the food matrix during the process of absorption (30).
All groups showed a significant increase in plasma retinol, but the increment was not significantly different among groups. It is likely that the vitamin A supplement distribution program in the area affected the plasma retinol in all groups. More than 60% of infants had a mega-dose of vitamin A within the last 6 mo of the study period, as part of the national public health program. The vitamin A distribution scheme was twice a year with a dose of 100,000 IU vitamin A targeted to infants aged 6–12 mo, and 200,000 IU to those above 12 mo of age. Although 21.3% of the infants initially had serum retinol <0.70 µmol/L, only 0.4% of them had serum retinol <0.35 µmol/L, which indicated that the level of deficiency was marginal. Also, almost 95% of the infants were still breast-fed, and breast milk might have been an important source of their vitamin A (2).
The effect of the DMM supplement on riboflavin, tocopherol, and homocysteine concentrations further confirms the initial hypothesis that infants who suffer from anemia in Indonesia suffer from multiple micronutrient deficiencies. That these concentrations of tocopherol and riboflavin showed significantly greater change compared with baseline only in the DMM group suggests that the infants in the other groups did not have optimal concentrations of these nutrients. The effect of the DMM supplement on plasma homocysteine levels could be due either to improved folate and/or vitamin B-12 status. No other studies have looked at these micronutrient concentrations in infants in Indonesia.
There was no significant difference in the number of days with illness between the micronutrient supplemented groups and the P group. The lack of effect of multimicronutrients and iron supplementation on morbidity differs from that in some other studies, in which supplementation with iron (31), zinc (8,9,32,33), or vitamin A (4,34) did reduce morbidity. Possibly, the doses of the micronutrients supplemented were not sufficient to reduce infant morbidity. However, some studies showed no effect of micronutrient supplementation on morbidity (10,35). Moreover, the immunocompetence of the infants in this study might be relatively good, because most of them were still breast-fed and the presence of acute infection was an exclusion criterion at the beginning of the study. It is also possible that the regular visits and questions on morbidity by the field assistants influenced the mothers’ child-care practices so they cared better for their infants and/or sought treatment earlier for their sick infants.
In conclusion, although both DMM and DI supplementations were effective in correcting iron deficiency during infancy, the DMM supplement was the most efficacious for a number of other outcomes. These included improving hemoglobin levels and preventing zinc deficiency and improving levels of other micronutrients, including riboflavin and vitamin E. Plasma homocysteine concentrations were also most improved in the DMM group, indicating better B vitamin status. The DI supplement had a negative impact on zinc status. Despite improving micronutrient status for many nutrients, the DMM supplement had no impact on the growth and the morbidity of the infants. From this study, we conclude that daily supplementation with an adequate daily intake of multiple micronutrients is the best of the strategies tested for improving anemia and micronutrient status of infants in developing countries.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Supported by UNICEF, as part of the Multi-Center International Research on Infant Supplementation (IRIS study).
3 Present address: World Bank, Jakarta, Indonesia.
5 Present address: UNICEF, 3 UN Plaza, New York, NY.
6 Abbreviations used: CRP, C-reactive protein; DI, daily iron; DMM, daily multiple micronutrient supplement; EGRAC, erythrocyte glycine reductase activity coefficient; LAZ, length-for-age Z-score; P, placebo; WAZ, weight-for-age Z-score; WLZ, weight-for-length Z-score; WMM, weekly multiple micronutrient supplement.
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LITERATURE CITED |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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