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3 Department of Pediatrics, Washington University School of Medicine, St. Louis, MO 63110; 4 Department of Community Health, College of Medicine, University of Malawi Blantyre 3; 5 Children's Nutrition Research Center, Houston, TX 77030; 6 Institut de Recherche pour le Développement, 75003 Paris, France; 7 Department of Paediatrics, Tampere University Hospital, Finland FIN-33014; and 8 Department of International Health, University of Tampere Medical School, Finland FIN-33014
* To whom correspondence should be addressed. E-mail: manary{at}kids.wustl.edu.
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ABSTRACT |
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 TOP ABSTRACT IntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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Introduction |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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12 mo of age, thickened corn dough, the family staple food, is introduced (5). The growth faltering seen in Malawi is often attributed to these poor complementary feeding practices. Corn porridge is lacking in many micronutrients, particularly Zn, iron, and Se, and has a low-energy density (6). Interventions to improve corn porridge for infants include the addition of micronutrient sprinkles and tablets (7,8) and the addition of a legume or oil to the porridge (9). Although these strategies seem like logical ways to increase infant nutrient intake, evidence demonstrating improved growth from trials of such improved porridges is limited. These strategies are difficult to sustain in practice because of the intermittent availability of forticant premixes in Malawi and the inability or unwillingness of mothers to consistently add oils to their infant's porridge.
Malawian adults consume corn dough as a staple food, rather than porridge, which has 2.8 times the energy density of porridge. Corn dough has not traditionally been given to infants, because it is generally believed that infants are unable to safely swallow semisolid foods. However, infants in other settings have successfully consumed complementary food of a soft, semisolid consistency (10). A sustainable, successful complementary feeding might utilize thickened corn porridge to improve the energy density of the infant's food and the addition of a powdered micronutrient-rich food that is always available, such as small fish.
Fortified spread (FS)9 is a lipid paste with imbedded small dry food particles; peanut butter forms the basis for FS. FS does not require cooking, nor does it support the growth of bacteria because of its low water content (11). FS has 25 times the energy density as typical infant porridge. Ready-to-use therapeutic food is a FS that has been successfully used in large-scale operational programs treating moderate and severely malnourished children (12). In addition, FS can be prepared in rural villages by mothers without sophisticated food processing facilities. Healthy infants have successfully consumed adequate amounts of FS as complementary food for 12 wk in rural Malawi (13). FS is an attractive alternative when considering improved complementary foods in Malawi, because it has a high energy density and micronutrients can be imbedded into this lipid paste.
This study explores the use of 2 novel complementary foods in rural Malawi to promote better growth, a fish-fortified thickened maize porridge (FP) and a micronutrient fortified, soy/peanut FS, in children 6–18 mo old. Growth was assessed over 2 age intervals: 6–12 mo and 12–18 mo. The 2 age intervals were chosen for evaluation, rather than a single interval from 6–18 mo, because children typically consume different foods and are fed differently during these age intervals and the effect of complementary feeding interventions may also differ. The hypotheses tested were that children receiving FS will have greater weight and length gains than those children receiving FP during both of these intervals.
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Subjects and Methods |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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All children 5.5–6.5 mo of age residing in the villages without evidence of edema or severe chronic illness were eligible for the study. Prior to enrollment, health aides compiled a list of all appropriately aged children based on records from the village census and then notified the mothers about the study. Mothers were told to be present at a central meeting point for enrollment on a specified date and time if they were interested. Upon presentation, all children were screened for their eligibility based on the birth date listed in their government-issued health passport.
Written and oral informed consent was obtained from all of the children's caretakers before enrollment. The study was approved by the College of Medicine Research Ethics Committee, University of Malawi and the Human Studies Committee of Washington University School of Medicine in St. Louis, MO.
Study design. This was a prospective, randomized clinical effectiveness trial comparing FP and FS as complementary foods to prevent growth faltering in rural Malawi.
Upon enrollment, caretakers were questioned about demographic data, anthropometric indices were recorded, and blood was drawn to measure Zn and Se status. Children were then randomized to either FS or FP by selecting a card in a sealed, opaque envelope from a preprinted, randomly shuffled stack. The 2 food groups were then separated and instructed how to use the complementary foods in their local language by the study nurses. Twins were assigned to receive the same complementary food.
Both diets provided 836 kJ/d (200 kcal/d) and at the age of 9 mo, mothers were instructed to increase their feedings to give children 1254 kJ/d (300 kcal/d) in accordance with WHO recommendations (14). Children were then followed monthly for weight gain and fortnightly for symptoms of infection as evidenced by mothers reporting fever, cough, or diarrhea. Compliance was determined by the fortnightly home visits by the health aides, who visually ascertained if the appropriate amount of food had been consumed.
Length was measured every 3 mo using standard measure mats (SECA Model 210, precision 0.25 cm). Each length measurement was taken in triplicate and the mean value of the 3 measurements was used for the determination of anthropometric outcomes. Weight was measured monthly using a digital scale. After 6 mo of participation, when the child was 12 mo of age, blood was again drawn to measure changes in Zn and Se status.
The primary outcomes were rates of weight and length gain from 6–12 and from 12–18 mo of age. Secondary outcomes were the incidence of fever, cough, and diarrhea from 6–12 mo and 12–18 mo of age in the 2 groups as well as changes in Zn and Se plasma concentrations from 6–12 mo of age. A sample of size of 240 children was chosen to detect differences in weight gain of 100 g and length gain of 0.5 cm, with 95% sensitivity and 80% power, assuming that 15% of the children would not complete 12 mo of follow-up.
Complementary foods. The FS consisted of 20% soy flour, 35% sugar, 26% peanut paste, 17% soy oil, and 2% vitamin and mineral mix that included iron, Zn, and Se (Table 1; Chipalonga Prevention Mix, Nutriset). FS was produced using a hand-powered grinder/mixer by a team of villagers. Soybeans and peanuts were roasted over paraffin stoves and the soybeans were then taken to the local mill for grinding into flour. The soy flour, roasted peanuts, sugar, vitamin/mineral mix, and one-half of the oil were then combined and ground to make a dry, crumbly paste. The remaining oil was then mixed in separately with a spatula to create a smooth paste that was poured into clear plastic jars with screw-top lids.
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Caretaker instruction. Mothers of children receiving FP were shown a preprepared sample of porridge to demonstrate the appropriate consistency. Each mother then received identical cups and teaspoons and was shown how much to fill the cup to constitute 1 serving of porridge (70 g). Each mother also received a supply of powdered fish and was shown how many teaspoons (2.5) were to be mixed into the porridge. Each level teaspoon corresponded to 2 g of fish powder. They were then instructed to prepare the mixture using the sample porridge and to feed their own child under the direct observation of the study nurse. Mothers demonstrated that they understood the recommendations through an interactive cooking session. At 9 mo, they were instructed to feed their child the freshly prepared FP 3 times each day.
Mothers receiving FS were taught about the spread's ingredients and given identical spoons that contained 4 g of FS per level spoon. Mothers were shown how to first mix the FS within the jar using the spoon to homogenize the spread and then how to level the spoon against the edge of the spread's container. Mothers demonstrated their understanding by mixing the spread and feeding their child under the study nurse's observation. Mothers were told to feed their child 5 teaspoons 2 times each day and to feed their child 5 spoonfuls 3 times each day when their child reached 9 mo of age. No mention was made to mothers concerning the feeding of other foods to their children.
Biochemical analyses. Upon enrollment and at 12 mo of age, 1–3 mL of venous blood was drawn and placed in a Zn-free heparinized, plastic centrifuge tube and separated on-site using an electric microcentrifuge. Samples were promptly frozen and transported frozen to the Center for Human Nutrition, University of Colorado in Denver. Zn was measured by a standard atomic absorption spectrometry method and plasma Se was measured by inductively coupled plasma MS (15).
Data analyses. We calculated rates of change of weight and length from 6–12 mo and 12–18 mo of age. Comparisons were made using a Student's t test for continuous variables. Comparisons of rates of growth were not stratified by sex, because these rates do not differ for weight or length by sex in the international reference population (16) nor in the local Malawian population (4). A Wilcoxon's rank-sum test was used to compare the incidence of fever, cough, and diarrhea between the 2 groups.
Because acute inflammation is known to lower plasma Zn concentration without actually altering Zn status (17), comparison of plasma Zn concentration between complementary food groups was conducted using ANCOVA to control for the effects of initial Zn status and fever during the 14 d prior to Zn measurement.
Anthropometric indices were calculated using the WHO 2005 standards for the purpose of comparing child growth in this population to international standards (16). The results of the Zn and Se analyses were compared with normal values from reference populations; for Zn, a value of < 9.9 µmol/L was considered low and consistent with Zn deficiency (18); and for Se, a value < 0.51 µmol/L was considered low and consistent with Se deficiency (19). A P-value < 0.05 was considered significant.
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Results |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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Whereas infants receiving FS did gain more weight than those receiving FP, all 6- to12-mo-old infants gained less weight and length than the WHO international reference population; the mean change in weight-for-age Z-score was –0.3 ± 0.5 and in length-for-age Z-score (LAZ) was –0.3 ± 0.6 for both dietary groups. The 12- to 18-mo-old children gained less length than the WHO international reference population but gained weight at a similar rate; the mean change in LAZ was –0.3 ± 0.6.
For the entire group of children, plasma Zn decreased from 11.5 µmol/L on enrollment to 10.6 µmol/L after 6 mo of complementary feeding. On enrollment, at the age of 6 mo, 55/240 (23%) children had low plasma Zn measurements, and after participating in the study for 6 mo, at the age of 12 mo, 77/216 (36%) children had low plasma Zn measurements (difference 13%; 95% CI 4–21%). No child had a low plasma Se measurement on enrollment or at the age of 12 mo.
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Discussion |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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One limitation of this study was that feedings were not directly observed; thus, we cannot be certain that the different foods were fed to children as outlined in the protocol. This was an effectiveness trial rather than an efficacy trial. However, health assistants were able to visually confirm that an appropriate amount of food had been removed from the jars during their home visits. Although visual inspection of FS and fish powder containers in the home was conducted to gauge compliance, this observational method has not been validated as a measure of dietary intake in young children. Mothers did not register complaints or preferences for one food or another and compliance did not differ between the 2 groups. An additional limitation of our study was that we did not have a control group that received no intervention; thus, we cannot compare our outcomes to current practice. Enrolling village members in a study without providing every participant with an intervention would have been very difficult, because it is inconsistent with the common Malawian cultural value of communitarianism. After discussions with village leaders, it was deemed impractical to have such a control group. No other dietary intake assessments were made in the study population. Caution should be exercised in extending these findings to groups of children having different habitual diets, particularly diets with a higher fat content, and to groups of children living in different settings, particularly those in urban areas.
Approximately 10% of each group dropped out of the study. The primary reasons for not completing the study were cultural objections to blood-drawing or the child's family moved away from the region (Fig. 1). There were no objections to the foods themselves and there were no significant differences in the number of dropouts or deaths for the 2 groups. In addition, those who dropped out were similar in nutritional status to those who completed the study. As such, we feel that the attrition rates did not bias our conclusions.
The best historical comparison group is 518 children of the same age living in the same geographic area that participated in an antioxidant supplementation study in 2003–2004 (20). This comparison group included essentially all children residing in 8 villages; these children were measured monthly. There have been no major changes in livelihood or lifestyle in these villages from 2002 to 2006. The historical control children gained 1010 ± 440 g from 6 to 12 mo and 1020 ± 430 g from 12 to 18 mo while linear growth was 6.4 ± 1.2 at 6–12 mo and 5.1 ± 1.4 cm at 12–18 mo. The rate of weight gain from 6 to 12 mo in children consuming FS was greater than the historical controls (P = 0.02, Student's t test) and the rate of weight gain from 12 to 18 mo for all children in the complementary feeding trial was greater than the historical controls (P < 0.01, Student's t test); the linear growth of study children and historical controls did not differ.
The finding that infants receiving FS had greater weight gain than those receiving FP, without more linear growth, is consistent with an observational study from Congo and Burkino Faso in which populations of infants consuming breast milk with very different quantities of monounsaturated fatty acids and PUFA exhibited different growth patterns. Among these Congolese and Burkinabe infants, those consuming relatively more polyunsaturated fats gained more weight but not more length (21). FS, rich in lipids from soy and sunflower oil, has much more polyunsaturated fats than corn flour. The lack of improved linear growth seen in our study is in contrast to findings from a micronutrient supplementation study in Ghana (22), where infants who received their micronutrients in a FS showed more linear growth than children who received micronutrient sprinkles or tablets. The findings from Ghana suggested that dietary essential fatty acids might be responsible for improved linear growth. In our study, FS contained ample amounts of dietary essential fatty acids, yet no improved linear growth was seen, suggesting other nutrients and environmental factors also play a role.
Previous reports of complementary feeding interventions to increase the energy density of the food have also shown modest results. Bhandari et al. (23) found that children in families who received educational interventions to add oil to infant food had little difference in weight gain and a small improvement in linear growth. A recent controlled trial involving underweight but otherwise healthy 6-mo-old infants in Malawi showed a mean improvement in weight-for-age Z-score and LAZ of 0.2 when supplemented with a FS for 3 mo compared with unsupplemented children (11).
Despite receiving 7 mg Zn/d, an amount 2–3 times the recommended intake for infants 7–12 mo old, the fraction of children with low plasma Zn measurements rose from 23% at 6 mo to 37% at 12 mo. The ANCOVA analysis indicates that this decrease was not primarily the result of acute inflammation. While any biochemical method of measuring Zn deficiency has an unacceptably high rate of false negatives in individuals, plasma Zn determinations have been recommended as an accurate method to assess the Zn status of a population (18). Among this population of rural Malawian children, such a high prevalence of plasma Zn < 9.9 µmol/L indicates poor Zn status that was not ameliorated by either complementary feeding regimen. The phytate content in the daily ration of FS was 121 mg and in the FP was 161 mg, resulting in dietary phytate:Zn molar ratios of 8:1 and 11:1, respectively. This suggests that Zn bioavailability for both FS and FP was in the intermediate range if these complementary foods were not consumed with other foods containing large amounts of phytate. Yet these plasma Zn data indicate that the children did not maintain normal Zn homeostasis, suggesting that nondietary factors, such as abnormal stool losses of Zn, may be playing an important role in the poor Zn status of the population.
Whereas the nutrient composition of FS and FP does differ in many respects (Table 1), the FS and FP diets (complementary food + estimated breast milk intake) provide adequate amounts of all macro- and micronutrients with the exception of iron. FP provides only 3 mg iron/d, whereas the estimated average requirement for 7- to 12-mo-old children is 6.9 mg iron/d. This estimation of nutrient adequacy was made assuming that among the study children, breast milk intake was similar to that measured in another complementary feeding study in Malawi (24), that the breast milk nutrient composition was similar to that in other African countries, and that the energy density of the complementary food did not affect breast milk intake, as has been clearly shown in previous work (24). Unfortunately, there were no readily available indigenous foods that could be added to FP to increase the iron intake such that it would reach the estimated average requirement. The potential consequences of inadequate iron intake in late infancy are anemia and reduced psychomotor development, characteristics that were not measured in this study. Iron supplementation given to children at risk for growth faltering in the developing world has been shown not to affect weight gain; thus, it was not considered as an explanation for the findings of this study (25,26).
FS was 3.5 times more energy dense than FP. Studies of energy intake by weanlings in developing countries have shown that infants often consume substantially less than the recommended amounts (27–30). It has been suggested that low energy density of the infant's diet and infrequent feedings account for the energy deficit (31). An infant's smaller body size limits the amount of food he or she can eat at a given feeding and to achieve adequate nutrition with low-density porridge requires that infants be fed several times each day. This proves to be very time consuming and impractical in resource-poor settings in which the primary caretaker, the mother, is also the principle farmer as well as the caretaker of other young children. Thus, the high energy density of FS may contribute to the greater weight gain in children consuming FS over FP in this study.
The acceptance and consumption of a complementary food is affected by the cultural milieu in which the child is raised, the developmental stage of the child, the organoleptic properties of the food, and the resources available for the preparation of the food. Because FS and FP are very different in their taste, texture, and the preparation needed prior to consumption, these factors may well have affected the amount of complementary food the children consumed. FS is a sweet viscous liquid that may be easier for younger children to swallow and more palatable than the FP, a soft solid containing small granules and a strong fish taste. FS was prepared as a ready-to-use food on a monthly basis and thus was available to mothers whenever they found it convenient to feed their infants. FP was prepared daily with the cooking of the family's meal and fed in conjunction with mealtimes. The ready-to-use nature of FS may have facilitated more frequent feeding or feeding at times when the child was more likely to eat than FP. Children receiving FS outside of the family mealtime might be more likely to consume additional family foods at mealtime, thus increasing total dietary intake. FS was a specialized food designated for infant feeding, quite distinct from habitual Malawian foods, whereas FP was similar to the traditional food, indistinguishable in appearance from food consumed by older children and adults. The specialized nature of FS may have limited its sharing between family members more than FP (32). Mothers may have been reluctant to save FP for a few hours so that their infants could be fed at times when the extended family was not eating, because they had been told that it was likely to be contaminated with bacteria. Further study of these nonnutrient characteristics of FS is indicated to determine how household FS use contributes to greater weight gain.
Practical implementation is a crucial component of successful complementary feeding interventions in the developing world. Processed, specialized infant foods are often unavailable to rural African mothers at a minimum of expense (33). Both FS and FP were prepared in rural Malawian villages using ingredients, devices, and methods that were accessible to all mothers. Because of this operational consideration, both FS and FP may be useful strategies for subsequent complementary feeding interventions in the developing world.
Effective interventions to reduce stunting and growth faltering are urgently needed in the developing world. Advantages seen with using FS in this trial were encouraging, but modest, and did not result in normal growth when compared with international standards. A FS with additional Zn in combination with infection prevention strategies, such as bed nets for malaria, an expanded spectrum of immunizations, or acute respiratory infection management, should be tested to reduce the rate of growth faltering in Malawi.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Author disclosures: C. A. Lin, M. J. Manary, K. Maleta, A. Briend, and P. Ashorn, no conflicts of interest.
9 Abbreviations used: FP, fortified porridge; FS, fortified spread; LAZ, length-for-age Z-score.
Manuscript received 11 September 2007. Initial review completed 10 October 2007. Revision accepted 12 December 2007.
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