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Post Graduate Program in Public Nutrition, Universidad La Molina, Lima, Peru and * Nutrition Section, Program Division, UNICEF, New York, NY
3To whom correspondence should be addressed. E-mail: gromana{at}lamolina.edu.pe.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • micronutrient supplementation • iron • zinc • anemia • growth faltering • Peru • infants
Micronutrient deficiencies are one of the most prevalent nutritional problems in the world and are currently the most prominent nutritional problem in Peru and other Latin American countries (1). In Peru, there is evidence that, in low socioeconomic groups, multiple micronutrient deficiencies are common throughout the life span but especially in small children (2). In recent years, poor urban populations in Peru, as in other developing countries, have been undergoing the so-called nutrition transition phenomenon, characterized by decreasing rates of stunting and wasting, together with increasing rates of overweight and micronutrient deficiencies (3).
One-third of the Peruvian population lives in Lima and 
50% of the country’s population lives in poor urban communities surrounding the major cities of the dry coastal region. Although the gross national income of Peru is about $2000 per capita per year, 15% of the population of 26 million still earns less than 1 dollar a day (4). Over the last 5 y, the rates of stunting in children aged <5 y have fallen from 37% to 25%, whereas the rate of wasting has remained at 1%. Despite this improvement in child growth, the prevalence of anemia has remained at 50% for children <5 y old and 30% for women of fertile age (2,5). Furthermore, the prevalence of vitamin A deficiency in children <5 y old is 22% (6). Although the prevalence of iron and vitamin A deficiencies is higher in the rural areas of the country, the total number of affected persons is higher in urban areas.
The Peruvian Ministry of Health carries out most of its micronutrient intervention programs using a single micronutrient approach. These programs provide iron supplements and megadoses of vitamin A, mostly to women, but the coverage of these interventions is not very high. The exception is a large salt iodization program that has almost eradicated this deficiency in the country.
In the past decade, several micronutrient supplementation schemes have emerged in the literature. Apart from the traditional regimen of a daily single dose of iron, several studies have shown the benefits of adding other micronutrients to iron supplements, such as vitamin C (7), vitamin A (8), folic acid (9), or multiple micronutrients (7,10). A recent report based on 22 studies of intermittent iron supplementation shows that daily supplementation is more efficacious than weekly supplementation (11). On the other hand, several studies show that weekly iron supplements are as, or more, effective than daily supplementation in improving iron status and/or growth of children (10,12–14). Most of these studies have been conducted in schoolchildren, adolescents, or adults, but there is little information about the efficacy of multiple micronutrient supplementation in infants, the age group in which these deficiencies start and progress with potentially severe consequences. Therefore, the objective of the present study was to determine the most efficacious scheme of 3 micronutrient supplementation schemes compared with a placebo control, to reduce the occurrence of anemia, micronutrient deficiencies, growth failure, and morbidity during infancy in Peru.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The area was chosen because of previous experience and existing information on the prevalence of iron-deficiency anemia and vitamin A deficiency in the communities. The study was carried out in peri-urban communities of 2 cities in the department of Lambayeque (Lambayeque and Chiclayo), located 600 km north of Lima, the capital of Peru. An extensive evaluation conducted 2 y ago in the study area found that 26.5% of children under 3 y of age were stunted, 72% had anemia, 25% were vitamin A deficient, 72% had acute respiratory infections, and 27% suffered from diarrheal diseases. Furthermore, the prevalence of underweight and overweight in the adults of this area was 1.5% and 20%, respectively, making these communities good candidates for our study.
Subject selection
A total of 313 infants, aged 6 to 12 mo, were randomly chosen from the study population following the methodology described by Gross et al. (15). The sample size was calculated for the 4 International Research on Infant Supplementation (IRIS)4 country sites combined, based on the comparison of a drop in standardized weight-for-age from –0.65 to –0.95 Z for the daily dose of multiple micronutrients (DMM) group compared with –0.65 to –1.20 in the P group. For a two-group repeated measures ANOVA with 7 levels (mo 0 to 6), a sample size of 256 per group will 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. During enrollment, the following exclusion criteria were used: lack of signed informed consent, premature birth of the child, low birth weight (<2500 g), congenital defects, chronic infection, severe wasting (Z-score weight-for-height <–3 SD), fever (>39°C) and severe anemia (Hb <80 g/L). Only 2 children were excluded from the study (one due to prematurity and the other due to congenital birth defects). Before the inclusion of the child into the study, the mother received an explanation of possible risks and benefits, and a signed consent was obtained.
Treatments
Infants were randomly assigned to receive 1 of 4 treatments, a daily placebo (P), a daily dose of 10 mg of iron as ferrous fumarate (DI), a DMM, or a weekly dose of multiple micronutrients (WMM). The daily supplement contained 15 micronutrients as follows: vitamin A (375 µg), vitamin D (5 µg), vitamin E (6 mg), vitamin K (10 µg), vitamin C (35 mg), vitamin B-1 (0.5 mg), vitamin B-2 (0.5 mg), vitamin B-6 (0.5 mg), vitamin B-12 (0.9 µg), niacin (6 mg), folic acid (150 µg), iron as ferrous fumarate (10 mg), zinc as gluconate (5 mg), copper as gluconate (0.6 mg), and iodine (50 µg). For the WMM study group, these amounts were doubled for consumption on one day of the week. The multiple micronutrient supplement was designed to provide the recommended daily intakes of children aged 1 to 2 y, with the exception of zinc, for reasons which are described elsewhere (16). Supplements were manufactured as chewable, easy to break and to dissolve tablets in weekly coded blister packs. Three of the groups (P, DI, and DMM) had blister packs with 7 tablets of the same composition. The 4th group (WMM) had blister packs that included 6 placebo tablets, and 1 tablet with micronutrients, which was always in the same position in the blister packs. The supplements were administered at home on a daily basis, 7 d/wk. On 6 of the days, a trained field worker, under the supervision of the research team, gave the tablet directly to the infant and on 7th day, the mother gave the supplement to the infant. Mothers of younger infants (6 to 8 mo), preferred to dissolve the tablets with a small amount of water in a teaspoon. For the older infants (8 to 12 mo), the preferred method was to divide the tablets into small pieces and to offer them to the children directly. The manufacturing laboratory (Hersil SA) assigned the codes to the different treatments and sent them to UNICEF (United Nations Children’s Fund), where they were kept until the end of the field study. The treatments were randomly assigned to the selected screened children in the field using a random number generator. The codes were broken during data analysis by the Medical Research Council in South Africa.
Procedures
Before the supplementation trial, a baseline survey was carried out in all participating families after obtaining signed informed consent. A socioeconomic questionnaire and anthropometric measurements were obtained at the household level. Upon completion of the survey, all participating infants began receiving the supplements, which were administered at home on a daily basis. During the daily household visit, information was collected and coded on the acceptability of the supplement and infant morbidity on the previous day. All morbidity information was collected based on the mother’s perception of presence or absence of symptoms. Diarrhea was defined as 
4 watery stools; upper respiratory infection was defined as presence of cough, runny nose, earache, or sore throat the previous day; and fever was defined as present or absent on the day of the visit. The information was summarized on a weekly and monthly basis.
Heparinized venous blood samples (10 mL) were collected at the beginning and the end of the trial at the nearest health post, for biochemical assessment of micronutrients. Hemoglobin (Hb) concentrations were analyzed locally using the cyanomethemoglobin method (17). Blood samples were stored immediately after collection in a precooled Styrofoam box (Productos Quimicos Pervanos) and were centrifuged within 6 h. Duplicate plasma and erythrocytes samples were transferred into 500-µL Eppendorf tubes and 500-µL Eppendorf Safe Lock cups, respectively. All plasma and erythrocyte samples were stored at –70 C until their transportation in containers on dry ice to Germany, where they were analyzed at the Micronutrient Laboratory of the Institute of Biological Chemistry and Nutrition at the University of Hohenheim. Plasma ferritin was measured by a standard sandwich ELISA procedure from the provider of the antibodies (DAKO). Plasma zinc concentrations were analyzed by flame atomic absorption spectrophotometer according to the description of the manufacturer (Perkin Elmer). Plasma retinol and tocopherol levels were analyzed according to Erhardt et al. (18). Plasma homocysteine levels were measured by HPLC (19), and riboflavin status was assessed by calculating the activation coefficient of the erythrocyte glutathione reductase (EGRAC) with and without added riboflavin (20). C-reactive protein (CRP) was measured as an indicator of short infection, by means of a Sandwich ELISA (DAKO).
Anthropometric evaluations were carried out at the beginning and the end of the study in the nearest health post and on a monthly basis in the households. Infant’s weight was measured and recorded to the nearest 0.1 kg with an electronic weighing scale (SECA) and with the infants minimally clothed. Length was recorded to the nearest 0.1 cm using the WHO recommended length-measuring board for infants (Ahrtag). Weight-for-age Z-score (WAZ), weight-for-height Z-score (WHZ), and height-for-age Z-score (HAZ) were calculated with EpiInfo 6.0 (Centers for Disease Control). Stunting and wasting were defined as <–2 Z-scores for height-for-age and weight-for-height, respectively, compared with international reference values; underweight and overweight were defined as <–2 Z scores of weight for age and >2 Z scores of weight for height, respectively (21).
Statistical analyses
Data collected was transferred to 4 spreadsheets (anthropometry, baseline demographics, weekly morbidity, and laboratory) using SPSS windows version 10.0 (SPSS) and sent to the Medical Research Council in South Africa were the statistical analysis for continuous variables was carried out. The data tested for normality and ferritin concentrations were log transformed. Height and weight gains were calculated per week, and the changes in the Z-scores were calculated per month. Descriptive statistics on the change from baseline to postintervention were obtained. Analysis of variance was conducted on continuous variables with normal distributions to test whether there were significant group differences (F-test) using Dunnett’s t test to specifically test whether each of the 3 supplementation groups differed significantly from the P group. Cases with elevated plasma CRP (>12 mg/L) were excluded from the statistical analysis for plasma ferritin, retinol, and zinc. The difference in the prevalence of anemia and specific micronutrient deficiencies between groups at baseline and at the end of the study were measured using the chi-square test with Yates continuity correction (22). Cutoff values for deficiency were 110 g/L for Hb and 12 µg/L for ferritin, 10.7 µmol/L for zinc, 0.7 µmol/L for retinol, EGRAC > 1.4 for riboflavin. P values < 0.05 were considered statistically significant.
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The weight and the height gain of the study children was similar in all 4 groups, and no form of supplement was able to control growth faltering. Similar results were found in a study of the growth of Vietnamese infants, which compared the effect of a daily with a weekly multiple micronutrient supplement (23). In Mexico, on the other hand, Rivera et al. (24) found significantly greater length gains in young children who received multiple micronutrient supplementation compared with a control group but only in those initially aged <12 mo. The Vietnamese trial and this Peruvian IRIS trial excluded low birth babies, which the Mexican trial did not. The Vietnamese trial used a supplement containing only 4 micronutrients (retinol, iron, zinc, and vitamin C), whereas the Mexican trial supplement contained 19 micronutrients, with higher doses of several micronutrients, including zinc. These trials thus are not strictly comparable, because of differences in exclusion criteria and in the doses and the numbers of micronutrients in the supplements.
The lack of effects of the micronutrient supplements on morbidity was both surprising and difficult to interpret. The significant improvement in the prevalence of acute respiratory symptoms at the end of the study was present in all groups, and it is likely that this was a reflection of seasonal variation. There was no effect of any form of supplement on the prevalence of diarrhea of these children. The absence of an effect these morbidities is surprising considering that the benefits of prophylactic zinc supplements for preventing both diarrheal diseases and pneumonia in preschool children has been amply demonstrated by pooled analysis of randomized control trials, with reductions in diarrhea (18% less) and pneumonia (41% less) (25). It may be that the dose of zinc in the supplement was too small, because even in the DMM group with the highest weekly dose of zinc, 20% of children still had low plasma zinc after 6 mo of supplementation. Another trial comparing the effects of zinc vs. multiple micronutrient supplements in Peruvian toddlers also found no effects on growth but reported that morbidity was greater in the multiple micronutrient than in the zinc supplemented group (26). These results are not strictly comparable, however, because the subjects were children suffering from persistent diarrhea, i.e., it was not a population-based trial of preventive supplementation but a trial of therapeutic supplements in the treatment of sick children. Furthermore, the doses of micronutrients used in the supplements were larger than in the IRIS supplements.
Anemia levels improved in all intervention groups and the control group, but the greatest effect was seen in groups receiving iron daily. Although all groups show a significant increase in mean Hb concentrations during the 6 mo of the trial, those receiving iron daily (DI and DMM) had significantly greater increases than those receiving weekly or no iron (P and WMM). The prevalence of anemia at the end of the intervention was significantly lower in those receiving iron daily (DI and DMM) compared with those receiving no iron or iron weekly (WMM and P). The reduction in anemia levels was 78%, 67%, and 43% of initial values in the DMM, DI, and WMM groups, respectively, compared with just 23% in the P control. The existing evidence is inconsistent regarding the effect or the possible benefit of different schemes of iron supplementation on anemia. Several studies show that weekly iron supplementation, either alone or with other micronutrients, is as effective as daily iron supplementation in reducing anemia in children (12,14,23,27), and adolescent girls (28–30). Other studies have shown that daily iron supplementation is more efficient (31–32). The present results are in line with the findings of the Beaton and McCabe (11) meta-analysis, which concluded that, whereas weekly iron supplements were as efficacious as daily iron supplements in many situations, during periods of rapid growth, e.g., pregnancy, and when pregnant mothers were already anemic, daily supplementation is needed. Levels of anemia were certainly high in these infants, with 40% still anemic at the end of the trial in both the P and the weekly iron groups, compared with 15% in the DMM and 23% in the DI groups.
Based on the other indicators used to measure micronutrient status, the DMM appears to be the best intervention. Although mean ferritin levels improved over 6 mo in both groups receiving iron daily (DI and DMM), prevalence of iron deficiency was significantly lower only in the DMM group compared with the no iron or weekly iron groups (P and WMM) but not with the DI group. Even then, half of the DMM group was still iron deficient. This may mean that the dose of iron was too small as iron deficiency (ferritin <20 µg/L) still affected at least half of those receiving iron daily (DMM and DI) and 90% of those receiving iron either weekly (WMM) or no iron (P). However, increasing the iron content of the supplements may not be appropriate, because the DI alone group had significantly more zinc deficiency at the end of the trial than the daily and weekly multiple micronutrient intervention groups, and increasing the iron dose is likely to exacerbate the zinc deficiency even more. It may be that levels of infection were high enough to inhibit proper utilization of the iron available, as has been suggested by other authors (33), and future interventions should consider infection control as part of the intervention. The lack of effect of any of the interventions compared with placebo on levels of homocysteine, riboflavin, retinol, and tocopherol suggests that the intake of these micronutrients, and possibly B-12 and folate, is adequate in these Peruvian infants.
In conclusion, we consider that the DMM intervention gave the best result in terms of anemia, and iron and zinc status. However, none of the treatments tested prevented growth faltering or common morbidities of young children. We believe that the results are insufficient to make a recommendation to Peruvian government authorities with regard to which supplementation scheme is the most appropriate to treat anemia and multiple micronutrient deficiencies during infancy. Although the daily multiple micronutrient supplementation was the most efficacious one for preventing anemia, iron, and zinc deficiencies during infancy, we believe that the results are inconclusive, because even in the DMM group, the most effective intervention, 15%, 20%, and 50% still remained anemic, zinc deficient, and iron deficient, respectively, at the end of the study. We recommend that further research be done to investigate whether higher doses of iron and zinc are needed to control these deficiencies, and/or whether simultaneous infection control procedures should also be considered.
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FOOTNOTES |
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2 Supported financially by UNICEF.
4 Abbreviations used: CRP, C-reactive protein; DI, daily iron supplement; DMM, daily multiple micronutrient supplement; EGRAC, erythrocyte glutathione reductase activity coefficient; HAZ, height-for-age Z-score; Hb, hemoglobin; IRIS, International Research on Infant Supplementation; P, placebo; WAZ, weight-for-age Z-score; WHZ, weight-for-height Z-score; WMM, weekly multiple micronutrient supplement.
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LITERATURE CITED |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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