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3 Department of Public Health Sciences, University of Toronto and Research Institute, the Hospital for Sick Children, Toronto, Canada M5G 1X8; 4 Research and Evaluation Division, Bangladesh Rural Advancement Committee, Dhaka, Bangladesh 1212; 5 The Manoff Group, Inc., Washington, DC, 20008; 6 Division of Clinical Nutrition, University of California, Davis, CA 95616; 7 Micronutrient Initiative, Ottawa, ON, Canada K2P 2K3; and 8 Snacks and Beverages Technology Division, Procter & Gamble Company, Cincinnati, OH, 45253
* To whom correspondence should be addressed. E-mail: ziauddin.hyder{at}sickkids.ca.
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ABSTRACT |
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 TOP ABSTRACT IntroductionMaterials and MethodsResultsDiscussionLITERATURE CITED |
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70 g/L) enrolled in a randomized, double-blind, placebo-controlled trial and were allocated to either a fortified or nonfortified beverage of similar taste and appearance. The beverage was provided at schools 6 d/wk for 12 mo. Concentrations of Hb and serum ferritin (sFt), retinol, zinc, and C-reactive protein were measured in venous blood samples at baseline, 6 mo, and 12 mo. In addition, weight, height, and mid-upper arm circumference (MUAC) measurements were taken. The fortified beverage increased the Hb and sFt and retinol concentrations at 6 mo (P < 0.01). Adolescent girls in the nonfortified beverage group were more likely to suffer from anemia (Hb <120 g/L), iron deficiency (sFt <12 µg/L), and low serum retinol concentrations (serum retinol <0.70 µmol/L) (OR = 2.04, 5.38, and 5.47, respectively; P < 0.01). The fortified beverage group had greater increases in weight, MUAC, and BMI over 6 mo (P < 0.01). Consuming the beverage for an additional 6 mo did not further improve the Hb concentration, but the sFt level continued to increase (P = 0.01). The use of multiple-micronutrient-fortified beverage can contribute to the reduction of anemia and improvement of micronutrient status and growth in adolescent girls in rural Bangladesh.
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Introduction |
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TOPABSTRACTIntroductionMaterials and MethodsResultsDiscussionLITERATURE CITED |
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The major micronutrient deficiencies include iron, vitamin A, and iodine in adolescent girls living in developing countries (5). In addition, deficiencies of the B vitamins (folic acid, vitamin B-12, vitamin B-6, riboflavin, and niacin), vitamin C, and zinc often coexist with the 3 major problem nutrients (6). In Bangladesh, a large proportion (11–56%) of adolescent girls suffer from subclinical vitamin A deficiency (7,8). Moreover, recent surveys show that 
30–40% of adolescent girls in Bangladesh are anemic (9–11). Because 34% of Bangladeshi adolescent girls get married before the age of 18 y (12) and 33% have their first pregnancy by ages 15–19 y (13), they are at increased risk of developing anemia during pregnancy, compromising their health as well as that of their offspring. It is therefore essential to ensure that adolescent girls enter pregnancy with an adequate nutritional status.
To date, the main public health strategies to control micronutrient deficiencies include food diversification, supplementation, and food fortification. Recently, a new diet-based strategy, which delivers multiple vitamins and minerals at physiological levels in a single vehicle (fortified, fruit-flavored powdered beverage) has been proposed (14). Community-based trials in multiple countries showed that the consumption of multiple-micronutrient-fortified beverage is efficacious in improving micronutrient status in school children in Tanzania (15), Botswana (16), and the Philippines (17) and in pregnant women in Tanzania (18,19). This study was conducted to assess the effect of a similar multiple-micronutrient-fortified beverage on hematological status and levels of vitamin A, iron, zinc, and growth status among adolescent girls in Bangladesh.
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Materials and Methods |
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TOPABSTRACTIntroductionMaterials and MethodsResultsDiscussionLITERATURE CITED |
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300 km northeast of Dhaka city. These schools were established for adolescent girls who have either withdrawn from the formal education system or never enrolled in school (20). A total of 54 NFPE schools were randomly selected from a list of 80 schools in Sherpur district. On average, each school had 30 pupils. The study area had similar geographical characteristics to the rest of the plain lands in Bangladesh, including high population density, fertile agricultural land, low risk of malaria, and minimal hookworm infection (21). No case of HIV was reported in the region among the study's age group (22). All adolescent girls from each selected school were screened for micronutrient and health status. Students suffering from either severe micronutrient deficiencies [severe anemia, i.e. hemoglobin (Hb) <70 g/L, n = 10; clinical signs of vitamin A deficiency, i.e. night blindness, n = 2; and clinical signs of iodine deficiency, i.e. visible goiter, n = 23] or acute infection (clinical signs of fever or reportedly suffer from any infectious disease, n = 9) were excluded and referred to the nearby health center for appropriate treatment.
The study protocol was approved by the Bangladesh Medical Research Council and Government of Bangladesh. Before the start of the study, meetings were held with parents at the selected schools to inform them about the study. Informed written consents were obtained from the students as well as from each of their parents or guardian.
Study design and protocol.
This study was a randomized, placebo-controlled, double-blind trial. Subjects from each school were randomly allocated to either a fortified or a nonfortified beverage group. Randomization was done by listing all selected children, assigning them with random numbers, and dividing the odd numbers from the even numbers to form the 2 groups. The test beverages were consumed 6 d/wk for 12 mo at the schools (no drink was provided during the school holidays, which totaled 20 d) under the direct supervision of the schoolteachers with the assistance of the BRAC community health workers (shastho shebikas). One shastho shebika was assigned per school to prepare and distribute the drink. Schoolteachers maintained daily attendance sheets for tracking beverage consumption. Adolescent boys attending the schools (30% of the students) were included in the randomization process and were provided the same beverages to avoid sharing. However, they were not included in any aspect of the data collection and analysis.
The fortified beverage was developed and produced by Procter & Gamble (14). It has been used earlier in clinical studies in school children (15,17) and pregnant women (18,19) with slight modification to meet the requirements of the study subjects. It is an orange-flavored powdered beverage, fortified with multiple-micronutrients and packaged in sachets (Table 1). Each sachet contained 45 g of powdered beverage. Procter & Gamble also provided an equal quantity of a nonfortified orange-flavored powdered beverage (identical to the fortified beverage in terms of weight, color, flavor, and appearance) as a control. The sachets containing the fortified and nonfortified beverage differed only in the sachet's color (blue or yellow). Researchers, schoolteachers, shastho shebikas, and students did not know whether the blue or yellow colored sachets contained the fortified beverage. The decoding was done only by the manufacturer after the study was completed and the data analyzed.
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Baseline information, including socioeconomic status and menstrual history, was collected by trained BRAC program organizers through house-to-house interviews using structured questionnaires. Baseline information also contained individual food consumption data collected by expert field nutritionists using a 24-h recall method. Venous blood samples (3 mL) were collected by trained laboratory technicians from subjects at baseline, 6 mo, and 12 mo to assess Hb and serum levels of ferritin, retinol, zinc, and C-reactive protein (CRP). Anthropometric measurements including height, weight, and mid-upper arm circumference (MUAC) were determined by trained BRAC program organizers at baseline, 6 mo, and 12 mo at the schools. Wooden height scales were used for the measurement of height to the nearest 1 cm. Uniscales developed by the SECA Company (http://seca.accurate-scale.com) were used for measurements of weight to the nearest 0.1 kg. BMI was derived from weight and height measurements (kg/m2) . Teaching-aids at Low Cost (http://www.talcuk.org) insertion tape was used to measure MUAC to the nearest 1 mm.
Laboratory analysis. Hb was measured by a trained technician using a portable photometer (HemoCue) immediately after the collection of blood (24). The HemoCue machine was standardized before each use for accuracy, using a standard microcuvette supplied by the manufacturer. Serum was separated at the field laboratory by centrifugation in a portable bench centrifuge (at 3600 x g; 15 min) before storage at –18 to –20°C. Frozen serum samples were then transported on dry ice and analyzed for ferritin, retinol, zinc, and CRP at the University of California Davis. Serum ferritin (sFt) was analyzed in duplicate by radioimmunoassay using a commercially validated kit (Diagnostic Products) and the interassay variation was <5%. Serum retinol was analyzed by HPLC and the interassay variation was <5%. Following acid digestion, zinc concentration in serum was determined by atomic absorption spectrophotometry relative to a standard curve (the National Institute of Standards and Technology) and the interassay variation was <10%. Serum CRP was analyzed by radial immunodiffusion (Nanorid; The Binding Site) and the concentration was determined relative to a calibration curve provided with the kit. For quality control, the laboratory used inter- and intra-assay variation (percent CV) of the standard curve and commercially available quality control samples.
Anemia was defined as Hb <120 g/L, depleted iron stores were defined as sFt <12 µg/L, and iron deficiency anemia (IDA) was defined by Hb <120 g/L and sFt <12 µg/L (25). Low serum retinol concentration was defined as serum retinol <0.70 µmol/L, low serum zinc was defined as serum zinc <10.7 µmol/L, and the presence of infection was defined as CRP >10 mg/L (26).
Sample size.
A total of 1268 adolescent girls, 634 in the fortified group and 634 in the nonfortified beverage group, were planned to be recruited in the study. The sample size was calculated to detect within and between group differences in mean Hb, prevalence of anemia (Hb <120 g/L), mean serum retinol, and low serum retinol concentrations (serum retinol <0.70 µmol/L) at a power of 0.80, 
= 0.05, and a lost-to-follow up of 25%.
Statistical methods. All forms were manually checked for completeness, consistency, and range. Data were coded, processed, and analyzed using SPSS for Windows (version 10.0) statistical software. When data were skewed, log transformation was used to perform statistical tests requiring normal distributions. Binary data were summarized with percentages. Paired t test was used for comparison of means within groups. Independent t test or general linear modeling was used for comparison of means and/or mean increment between groups. Wilcoxon's Signed Rank test was used for comparison of proportions between groups. Change in anemia prevalence within groups was assessed using McNemar's test. The OR for anemia, iron deficiency, IDA, and low serum retinol concentrations were computed using logistic regression. Differences were considered significant at P < 0.05.
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Results |
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TOPABSTRACTIntroductionMaterials and MethodsResultsDiscussionLITERATURE CITED |
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Prevalence of anemia, iron deficiency, and IDA. After the 6-mo intervention phase, the prevalence of anemia in the fortified beverage group decreased from 32.4 to 19.1% (P < 0.01), with no significant change during the second 6 mo. In the nonfortified beverage group, prevalence of anemia after 6 mo (32.1%) did not differ from that of the baseline (30.4%). Furthermore, the prevalence of anemia in this group continued to increase to 36.5% at the 12-mo follow-up assessment, which was higher than the baseline prevalence (P = 0.02).
After 6 mo, the prevalence of iron deficiency (defined as sFt <12 µg/L) decreased in both groups. In the fortified beverage group, iron deficiency decreased from 30.5 to 6.6% (P < 0.01). In the nonfortified beverage group, iron deficiency was reduced from 32.9 to 27.4% (P < 0.01). The reduction was greater in the fortified (22.9%) than in the nonfortified beverage group (6.6%) (P < 0.01). No further change was observed in the nonfortified beverage group between 6 and 12 mo. However, in the fortified beverage group, the prevalence of iron deficiency dropped further from 6.6 to 3.2% (P < 0.01).
After the 6-mo intervention phase, the prevalence of IDA (combination of anemia and iron deficiency) in the fortified beverage group decreased from 13.1 to 1.5% (P < 0.01), with no further change during the following 6 mo. In contrast, in the nonfortified beverage group, prevalence of IDA at 6 mo (14.0%) did not differ from the baseline (13.8%). No further change was observed during the following 6 mo. After 6 mo of the supplementation, the adolescent girls in the nonfortified beverage group were 2 times more likely to be anemic, 5 times more likely to be iron deficient, and 11 times more likely to suffer from IDA (Table 5).
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Among the nonanemic girls at baseline, anemia developed in 6.8% of the girls in the fortified beverage group compared with 11.6% of the girls in the nonfortified beverage group after 6 mo of the intervention. Therefore, the odds of becoming anemic were lower in the fortified beverage group compared with the nonfortified beverage group (OR = 0.56, 95% CI = 0.36–0.88; P < 0.01).
Vitamin A and zinc status. Baseline mean serum retinol and zinc concentrations did not differ between the groups and a similar proportion of girls in the 2 groups had low serum retinol (serum retinol <0.70 µmol/L) and low serum zinc values (serum zinc <10.7 µmol/L) (Table 4). After 6 mo, serum retinol and zinc concentrations increased significantly in both groups. The increased serum retinol was significantly higher in the fortified beverage group compared with the nonfortified beverage group (Table 4). Between 6 and 12 mo, serum retinol and zinc concentrations decreased in both groups (P < 0.01).
From baseline to 6 mo, prevalence of low serum retinol dropped from 11.2 to 1.2% in the fortified beverage group (P < 0.01) and from 10.3 to 6.3% in the nonfortified beverage group (P < 0.01). The change was higher in the fortified beverage group (P < 0.01). After 6 mo of supplementation, the nonfortified beverage group was 5 times more likely to have a low serum retinol concentration compared with the girls of the fortified beverage group (Table 5). After 6 mo, the prevalence of low serum zinc dropped from 60.9 to 25.6% in the fortified beverage group (P < 0.01) and from 55.3 to 25.9% in the nonfortified beverage group (P < 0.01). Between 6 and 12 mo, the serum zinc decreased in both groups (Table 4).
The prevalence of elevated CRP was low (<3%) in both groups at baseline, after 6 mo, and after 12 mo of intervention, and the groups did not differ (data not shown).
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Discussion |
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TOPABSTRACTIntroductionMaterials and MethodsResultsDiscussionLITERATURE CITED |
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In the group receiving the nonfortified beverage, mean Hb remained low and overall anemia prevalence continued to increase. This may be due to the increased need of iron for growth not being met. A higher proportion of girls in the nonfortified beverage group developed anemia during the study. The prevalence of iron deficiency and suboptimal vitamin A status was also significantly higher in the girls receiving the nonfortified beverage after 6 mo. Our findings thus are in agreement with previous studies using a similar multiple-micronutrient-fortified beverage that demonstrated significant improvements in iron and vitamin A status in school children and pregnant women (15–19).
Despite the high prevalence of low serum zinc at the start of the study, we did not observe a positive effect of the fortified beverage. The prevalence of low serum zinc decreased significantly and to a similar extent in both study groups within 6 mo. The lack of effect of the fortified beverage on zinc status compared with the nonfortified beverage could be due to the dose of zinc being too low or to a possible interaction between iron and zinc for absorption (28). Indeed, recent studies showed that iron inhibits zinc absorption (29) (and vice versa). However, iron has little effect on zinc absorption when zinc-iron ratios are 1:1, which is similar to the ratio in our study (30). Therefore, the interaction of iron and zinc from the fortified beverage should be further investigated and the dosage of zinc reevaluated.
In this study, girls who consumed the fortified beverage had a higher mean increase in weight, MUAC, and BMI over 6 mo compared with girls in the nonfortified beverage group. These results are consistent with those from the other studies that have used a similar multiple-micronutrient-fortified beverage in school children (15,16,31). In one of the previous reports (16), significantly increased weight and MUAC were obtained after 8 wk of fortified beverage consumption. In the other studies, significantly increased weight was shown after 6 mo (15) and 14 mo of supplementation (31). Similarly, a recent trial in adolescent girls in India reported increased weight gain with the use of iron supplements for a period of 3 mo (32). As speculated by others (15,33), the significantly greater weight and MUAC gains in the girls receiving the fortified beverage could be due to increased appetite. With our study design, however, it was not possible to determine whether these improvements in anthropometric measurements were due to a single vitamin or mineral (like iron) or to a combination of vitamins and minerals. Unlike that of the school children study in Tanzania (15), consumption of the fortified beverage did not significantly affect height gain during the duration of the trial. This inconsistency could be due to differences in age and gender. The mean age for the Tanzanian school children was 10 y (the subjects included boys and girls). In contrast, the mean age for the adolescent girls in this study was 12 y and boys were not included.
The results of the current study should be applied in the context of the following study limitation. Although strongly related to anemia, parasitic infection was not determined at baseline. Because BRAC does not provide deworming treatment for NFPE school students as a regular intervention, we opted not to test for it to create a situation that would be similar to that found in the current programmatic setting.
The advantages of using a fortified beverage in a school-based setting as reported here include: 1) the ability to address more than 1 micronutrient deficiency simultaneously; 2) the ability to provide the beverage isolated from meals containing inhibitors of mineral absorption such as phytate; and 3) the likelihood of higher adherence due to the supervision during beverage preparation and consumption and due to the pleasant fruit flavor of the beverage. We demonstrated that it is efficacious to provide a multiple-micronutrient-fortified beverage in a school-based setting to improve anemia and other vitamin and mineral status of vulnerable adolescent girls as well as to lead to improvements in anthropometric measurements. The fortified beverage studied not only treated but also prevented anemia from developing. The findings in this study may have further implication in terms of pregnancy outcomes, because there is a positive interaction between maternal BMI at conception and birth weight (27). Indeed, women with low BMI who fail to gain adequate weight during pregnancy are at a higher risk of having a low birth weight babies.
The results of this study could be generalized to the rest of the rural areas in the country, because the study population was typical for rural Bangladesh. Future studies should investigate a number of operational issues, including the optimum duration of the use of the fortified beverage and feasibility of distributing the product through different channels such as schools (as used in this study), adolescent clubs, and also through the private sector, using a social marketing approach. As a public health strategy, this intervention has the potential to improve adolescents' overall nutritional status, which would in turn improve pregnancy outcomes.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Author disclosures: S. M. Ziauddin Hyder, M. Khan, F. Haseen, T. Schaetzel, C. S. B. Jalal, M. Rahman, Bo Lönnerdal, V. Manner, and H. Mehansho, no conflicts of interest.
9 Abbreviations used: BRAC, Bangladesh Rural Advancement Committee; CRP, C-reactive protein; Hb, hemoglobin; IDA, iron deficiency anemia; MUAC, mid-upper arm circumference; NFPE, nonformal primary education; sFt, serum ferritin.
Manuscript received 19 March 2007. Initial review completed 23 May 2007. Revision accepted 24 June 2007.
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LITERATURE CITED |
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