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© 2003 The American Society for Nutritional Sciences J. Nutr. 133:3957S-3964S, November 2003


Supplement: Animal Source Foods to Improve Micronutrient Nutrition in Developing Countries

Food Supplements Have a Positive Impact on Weight Gain and the Addition of Animal Source Foods Increases Lean Body Mass of Kenyan Schoolchildren1,2,3

Monika Grillenberger*, Charlotte G. Neumann{dagger}, Suzanne P. Murphy**, Nimrod O. Bwibo{ddagger}, Pieter van't Veer*, Joseph G. A. J. Hautvast* and Clive E. West*,{dagger}{dagger},4

* Division of Human Nutrition and Epidemiology, Wageningen University, Wageningen, The Netherlands, {dagger} Schools of Public Health and Medicine, University of California, Los Angeles, CA 90095, ** Cancer Research Center, University of Hawaii at Manoa, Honolulu, HI 96813, {ddagger} Department of Pediatrics, University of Nairobi, Nairobi, Kenya and {dagger}{dagger} Department of Gastroenterology, University Medical Centre, Nijmegen, The Netherlands

4 To whom correspondence should be addressed. E-mail: clive.west{at}wur.nl.


    ABSTRACT
 TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Observational studies of dietary patterns and growth and studies with milk supplementation have shown that children consuming diets containing animal source foods grow better. This study evaluates the growth of 544 Kenyan schoolchildren (median age 7.1 y) after 23 mo of food supplementation with a meat, milk or energy supplement (~1255 kJ) compared to a control group without a supplement. Multivariate analyses controlled for covariates compared gain in weight, height, weight-for-height Z-score (WHZ), height-for-age Z-score (HAZ), mid-upper-arm circumference, triceps and subscapular skinfolds, mid-upper-arm muscle and mid-upper-arm fat area. Children in each of the supplementation groups gained ~0.4 kg (10%) more weight than children in the Control group. Children in the Meat, Milk and Energy groups gained 0.33, 0.19 and 0.27 cm more, respectively, in mid-upper-arm circumference than children in the Control group. Children who received the Meat supplement gained 30–80% more mid-upper-arm muscle area than children in the other groups, and children who received the milk supplement gained 40% more mid-upper-arm muscle area than children who did not receive a supplement. No statistically significant overall effects of supplementation were found on height, HAZ, WHZ or measures of body fat. A positive effect of the milk supplement on height gain could be seen in the subgroup of children with a lower baseline HAZ (<=-1.4). The results indicate that food supplements had a positive impact on weight gain in the study children and that the addition of meat increased their lean body mass.


KEY WORDS: • animal source foods • growth • body composition • schoolchildren • Kenya

Nutrition intervention programs initially focused on increasing the protein and energy intake of the target population (14), but suboptimal growth observed in children in developing countries has been shown to be related to micronutrient deficiencies as well. Several studies with single or combined micronutrient supplements, especially zinc (5,6) and iron (713), improved growth in children, but more information is needed on the effects of specific foods containing these and other micronutrients needed for optimal growth. Diets in developing countries are mostly plant based, and intake of protein from meat is usually extremely low, providing only 15% of dietary protein compared with ~60% in developed countries (14). Animal source foods (ASF)5, such as meat and milk, can supply multiple micronutrients in an efficient and digestible way and also provide the high quality protein necessary for child health, growth and development.

Meat is rich in heme iron, zinc, riboflavin, vitamin B-12, niacin and vitamin B-6, but it is low in vitamin A and folate. Milk is a good source of vitamin A, calcium, phosphorus, vitamin B-12, riboflavin and folate, but it is low in zinc and iron. Even when small amounts of ASF are part of the usual diet of children, they consistently are associated positively with growth (1517). Although supplementing children with milk or milk products has been shown to have beneficial effects on growth (4,1824), milk does not improve iron or zinc status.

Diets in developing countries usually contain high amounts of substances that reduce the bioavailability of micronutrients. This low bioavailability, especially of iron and zinc, from plant sources can be improved by consuming meat, even in the presence of dietary inhibitors (2527).

No controlled feeding intervention study has been conducted thus far to evaluate the effect of supplementing children with different ASF on their physical and cognitive development compared to a control group. Therefore, we performed a 2-y intervention study in which meat and milk were added to the usual plant-based diet to examine whether regular intake of small amounts of these foods could improve the growth of children suffering from moderate stunting and multiple micronutrient deficiencies.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Study area

The study was conducted in Kyeni South Division of Embu District in Eastern Province, Kenya. The study area is on the slopes of Mt. Kenya, near the Equator, with an elevation ranging from 1200–1460 m. The region is characterized by distinct rainy and dry seasons, with mild weather year-round. The study area includes a relatively fertile zone with higher rainfall and a semi-arid area at lower elevations. During the study period there was a drought that resulted in low harvests of the staple crops, maize and beans. Cash crops, which are produced in the area on a small scale, include coffee, cotton and tobacco.

Studies in this area in the 1980s showed that the intake of ASF is low, with only 1% of the energy intake of schoolchildren supplied by milk and <1% from meat (28). Intakes of iron, zinc, calcium, riboflavin and vitamins B-12, D, E and A are inadequate in toddlers and schoolchildren (29).

Study design

All children enrolled in class 1 (median age 7.1 y) from 12 selected primary schools (n = 554) participated in the study. They received either a daily food supplement or no supplement (control). Schools were assigned randomly to one of three different food supplements. These were isocaloric and contained meat, milk or extra fat (referred to as the "energy supplement"). Because three large schools had more than one class 1 classroom, each of these schools was randomly assigned to each of the groups, such that these schools could not be randomized to the same food supplementation group. The feeding started on August 31, 1998, at the beginning of the last school term of the year, and ended in July 2000. The school year in Kenya begins in January and comprises three terms, with three 1-mo breaks in April, August and December. The supplement was distributed for 18 mo, when schools were in session. In the new school year in 1999 the children moved to class 2, and in January 2000 they moved to class 3. Repeaters were kept in the study and continued to be fed with their original class. Every child in a class where a food supplement was distributed participated in the feeding, irrespective of whether data were collected from them or whether their data were included in the analyses.

Approval was obtained from the University of California, Los Angeles, Human Subject Protection Committee, the Ethics Committee of the University of Nairobi, School of Medicine, Kenya, and the Office of the President, Government of Kenya. All local and district authorities were involved in the implementation of the study, and the community was extensively informed about the aim and procedures of the intervention. Informed verbal consent of the parents of the study children was obtained before the study.

After completion of the study, the households in the control group were given a local milk goat. This was chosen by the parents through representative committees as compensation for the food their children missed during the course of the study.

Preparation, distribution and composition of food supplements

The vehicle for the food supplements was githeri, a local dish made from dry white maize (Zea mays), Mwitemania beans (kidney beans, Phaseolus vulgaris), tomatoes, onions, iodized salt (Kensalt, 168.5 mg potassium iodate/kg; Salt Manufacturers, Kenya), vegetable fat (Kimbo, fortified with 124 IU of retinol per gram; Unilever, Kenya) and sukuma wiki (kale or collard greens, Brassica oleracea). For the meat supplement, minced beef (10% fat) was added; for the milk supplement, a glass of ultrahigh–temperature cow's milk was served after the consumption of the githeri; and the energy supplement contained additional fat. The food supplement was thoroughly mixed to ensure that all children received the same amount of all ingredients and that part of the mixture would not be consumed preferentially (such as pieces of meat). It was deemed important that only local foods and familiar preparation methods were used, but for hygienic and logistical reasons, the milk and meat were purchased from reputable wholesalers within the region or from Nairobi. Taste tests were conducted with schoolchildren, and where necessary, recipes were adjusted. During the first school term of the intervention (from September to November 1998), the meat, milk and energy supplements contained an estimated energy content of ~1050 kJ/serving. The amounts of some ingredients then were increased, because children grew in height and weight, to achieve a total energy content of ~1255 kJ, which was maintained at this level throughout the intervention phase. The milk and meat supplements provided more than half of the recommended daily intake of vitamin A and >75% of the recommended daily amount of vitamin B-12. The meat supplement provided nearly one-third of the recommended iron and more than half of the recommended daily amount of zinc, whereas the milk supplement provided >75% of the recommended intake of riboflavin.

The food was prepared in a central location following strict hygienic preparation methods and weighed into plastic bowls, each of which was labeled with a child's name, and transported while still hot in insulated containers by car to the schools. The food was served during the first school break at 9:30 a.m. This time was chosen to avoid breakfast or lunch being replaced by the food supplement. Project staff ensured that each child received the food container that was labeled with his/her name and that no food was spilled or exchanged between the children. Afterwards, the bowls and cups were collected. The milk leftovers were measured at school, and later at the cooking site the food leftovers were weighed and the amounts were recorded.

Data collection

Twelve local women who had worked as enumerators in the Nutrition Collaborative Research Support Program on Food Intake and Human Function (NCRSP) in the same location in 1984 were retrained to perform the anthropometric data collection. A supervisor monitored the interviews/measurements, checked the forms, and maintained and calibrated the equipment. The area of the 12 schools was divided into three clusters to facilitate data collection and supervision. The enumerators were rotated between clusters and schools to prevent bias. The methods used were based on the NCRSP study. The forms were pretested and adapted. The ages of the children were derived from the census questionnaires or from the school register.

Anthropometry

Weight, mid-upper-arm circumference (MUAC), triceps skinfold thickness and subscapular skinfold thickness were measured every month in the first year and every other month in the second year. Height was measured every 4 mo in the first year and every 8 mo in the second year following recommended protocols (30,31). Weight was measured to the nearest 0.1 kg on an electronic digital scale (Seca, Columbia, MD) and shoes and as many clothes as possible were removed. The boys were weighed in short trousers and a shirt (average total weight 230 g) and the girls were weighed in a tunic and a blouse (average total weight 280 g). The weight of the clothes was deducted from the weight of the children. Height was measured (with the children shoeless) to the nearest 0.1 cm with a locally manufactured wooden board fitted with a measuring tape, a fixed-foot plate and a movable headboard. The height of the mother was measured once during the study by a light portable wooden device with a footplate, a measuring tape and a headboard. MUAC was measured using a plastic insertion tape (Perspective Enterprises, Kalamazoo, MI) on the left relaxed arm, midway between the tips of the acromion and olecranon processes. The reading was taken to the nearest 0.1 cm. Skinfold thickness was measured with a Lange caliper (Cambridge Scientific Industries, Cambridge, MD). To reduce intraindividual error, each skinfold thickness measure was performed in triplicate and the mean value was used for analyses. The triceps skinfold was taken to the nearest 0.5 mm at the same mark as the MUAC on the left arm. The subscapular skinfold was measured to the nearest 0.5 mm, below and to the right of the inferior angle of the left scapula, at an angle of 45°.

All measurements were obtained independently by two enumerators, and the mean of their measurements was used as the actual value. If the difference of their measurements exceeded preset limits (0.5 cm for height, 2 mm for triceps and subscapular skinfolds, 0.2 cm for MUAC and 0.1 kg for weight), the measurements had to be repeated, and the mean of this pair of measurements was used. Measurements generally were conducted at school; however, when a child was absent or when the school was closed, measurements were made at the child's home.

All enumerators underwent initial and ongoing training and standardization. The accuracy of the equipment was checked before every round of measurements. Intrateam and interteam measurement error was monitored by independently repeating all anthropometry during the same session in a random sample6. The technical error of measurement was expressed as a standard deviation (, where d is the difference between paired measurements and n is the number of paired measurements). The intrateam technical errors of measurement were 0.15 kg for weight, 0.11 cm for height, 0.11 cm for MUAC, 0.29 mm for triceps skinfold and 0.23 mm for subscapular skinfold. The interteam technical errors of measurement were 0.11 kg for weight, 0.30 cm for height, 0.11 cm for MUAC, 0.47 mm for triceps skinfold and 0.38 mm for subscapular skinfold.

Estimates of mid-upper-arm muscle area and mid-upper-arm fat area, indicators of body muscle and subcutaneous fat mass (32), were derived from measurements of the triceps skinfold and the MUAC by standard formulas (33). The EpiInfo2000 program (version 1.0.5; Centers for Disease Control and Prevention, Atlanta, GA), which uses the CDC/WHO 1977/1985 reference curves for age, sex, height and weight (34), was used to transform the height and weight measurements into sex- and age-specific Z-scores: height-for-age Z-score (HAZ), weight-for-age Z-score (WAZ) and weight-for-height Z-score (WHZ). For girls aged >10 y (or >137 cm) and boys aged >11.5 y (or >145 cm), WHZ could not be calculated due to lack of reference data in the EpiInfo program (n = 13).

Food Intake

A semiquantitative 24-h recall method was used to estimate the usual intake of energy, macronutrients, micronutrients, dietary fiber and phytate by the study children.

All days of the week except Fridays and Saturdays (because no food intake data was collected on Saturdays and Sundays) were proportionately included in the survey to account for any day-of-the-week effects on food and/or nutrient intakes. Food models and local plastic dishes and utensils were used to estimate the portion sizes. Mothers of the study children were encouraged to maintain the usual home diet for the children in the study. The food intake data were analyzed with the WorldFood Dietary Assessment System, version 2.0 (35). For the baseline food intake, an average of three food intake measurements was used.

Physical examination and morbidity

Before the intervention, experienced local physicians performed a clinical examination of each child. All children were dewormed with a single dose of mebendazole before the intervention, and deworming was repeated 8 mo later. Retrospective information on morbidity was collected monthly by interview. The enumerator visited the household and asked a caregiver, usually the mother, about any illness or symptoms the child experienced on the day of the visit and/or in the previous week using a structured questionnaire. The questionnaire included general symptoms of diseases and 16 major illness categories based on previous studies. Guidelines were established as to when the supervising nurse or a physician should revisit a child. Quality control measures included intensive preliminary and ongoing training of enumerators, close supervision of enumerators and re-interviews of 15% of the children. A score was derived to categorize the diseases/symptoms as mild and severe. Any seriously ill children were referred for treatment to the local health center.

Demographic information

Data on the socioeconomic status (SES) of each family was collected before the intervention. A SES score was derived from the following variables: land ownership and area cultivated, number and type of livestock owned, source and amount of income, income from food products, type and income from cash crops, expenditures, household possessions, the construction of the house and the type of fuel used for cooking. Social factors included church and Sunday school attendance and membership in self-help groups or organizations. An index of "modernity" included use of bank, telephone and/or post office, ownership of a National Social Security Fund card, credit from a cooperative, a bank account, household adoption of agricultural or other improvements or innovations and whether household members listened to radio/TV and/or read the newspaper at least once a week.

Data analysis

All forms were checked by the supervisors in the field to allow immediate revisits for gross errors or missing data. Forms were collected twice a week from the field offices and they were checked and cleaned. The forms then were entered by scanning using TELEform (Cardiff Software, Vista, CA) or they were entered manually in an Access database (Microsoft, Redmond, WA). The data then was printed and checked for errors against the forms and range-checked by computer.

Mixed linear regression models, as implemented in the SAS PROC MIXED procedure (SAS version 8; SAS Institute, Cary, NC), were used to test the effect of supplementation on the anthropometric outcome variables. Because the unit of randomization was not the individual child but the school, a nested factor (i.e., schools nested within supplementation groups) was used as the random factor, and supplementation (in the crude models) or supplementation and other covariates (in the adjusted models) were used as fixed factors. The slopes of each child's regression of the anthropometric outcome variables on time were used as the dependent variables, reflecting their average change during the study period. The inverse of the squared errors of the slopes of the individual children were used as weights in the analysis. In this way, children with more stable estimates of the outcome variables and higher numbers of observations had more influence in regressions evaluating associations between the food supplements and growth. None of the variables required transformation for departure from normality or skewness.

The effect of supplementation on the outcome variables first was examined in unadjusted models. Baseline variables that appeared to be different among the supplementation groups and that were associated with any of the anthropometric outcome variables were examined for their potential of being confounders. This was done by comparing the estimates of supplementation effect in the unadjusted model with the estimates in the model adjusted for the potential confounder. If the difference was >10%, the variable was deemed to be a confounder and was included in the model of the respective outcome variable. To improve the precision of the estimated supplementation effects, covariates that were considered important determinants of growth (based on a conceptual model) were included in the models. These were sex, SES, baseline age, morbidity (classified as mild and severe illness), baseline energy intake from home diet (average of three 24-h recalls) and the baseline value of the outcome variables for each model. For the height model, the mother's height was included, and instead of baseline height, the baseline HAZ of the child was included. In the models of weight, MUAC, triceps and subscapular skinfolds, mid-upper-arm muscle area and mid-upper-arm fat area, baseline WHZ was included as a proxy for wasting. Because the height of the mother is an important determinant of children's growth, it is probably an indicator of the genetic potential for growth, a shared environment and the SES of the family.

A backward elimination procedure was used for selection of covariates. Covariates with probability values <0.05 were retained in the model. Confounders were kept in the model irrespective of their statistical significance. The models were used to compute least squares means, standard errors and contrasts of the outcome variables. Subgroup analyses for sex, baseline age and SES for all outcome variables, and baseline HAZ for change in height and HAZ, were performed using the median as a cutoff. P-values presented were based on two-tailed tests, and those <0.05 were regarded as statistically significant.


    RESULTS
 TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The trial profile is given in Figure 1. Of the 554 children randomized to the three food supplements and the control group, 7 left before the feeding intervention started, 14 were handicapped, 33 were siblings and 2 households were not cooperative, leaving data on 498 children for analysis. Data from children for whom the food supplement was changed because of food preferences (n = 17) or change of school (n = 25) only were included in the analysis for the time period when they ate the originally assigned food supplement. One child died during the study due to illness. Complete data for height (i.e., 7 observation points) were available for 78% of the children, whereas 10.8% had 5 or 6 observation points, 3% had 3 or 4 data points and 8% had only 1 or 2 data points. For the other anthropometric variables, the maximum number of observation points was 16, which were available for 72% of the children. For 91% of the children >50% of the complete data points were available.



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FIGURE 1  Trial profile.

 
The amount of food supplement consumed, as a proportion of the total amount of food supplement provided, was similar for the supplementation groups: 82.1% for the meat supplement, 80.1% for the milk supplement (79.1% for the milk itself) and 80.4% for the energy supplement.

Descriptive statistics for the anthropometric outcome variables at baseline and the covariates for the supplementation groups and control group at baseline are presented in Table 1. Of the total children, 25.3% were stunted (HAZ < -2) and 4.6% were severely stunted (HAZ < -3). Less than 2% of the children were wasted (WHZ < -2). The girls had a higher mean HAZ than the boys (-1.20 and -1.53, respectively).


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TABLE 1 Baseline anthropometric outcome variables and covariates of study children1

 
Table 2 presents results of the multivariate analysis of the effects of food supplementation on the anthropometric outcome variables. The estimates of the adjusted models are controlled for the identified confounders and covariates.


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TABLE 2 Changes in anthropometric variables over 23 mo1

 
For weight gain, there was a statistically significant supplementation effect for the duration of the study. Children in each of the supplementation groups gained ~10% more weight than the children in the Control group. This supplementation effect was greater in the boys, in the younger children, and in the children with lower SES (data not shown). The average WHZ decreased for all groups, but the decrease in the Meat and the Energy groups was ~50% less than that in the Milk and Control groups. The boys receiving the meat supplement had a decrease in WHZ that was 0.36 (~120%) less than in those who received the milk supplement (p = 0.05), 0.24 (~80%) less than those with the energy supplement (p = 0.18) and 0.39 (~130%) less than those in the Control group (p = 0.04). For the girls, no distinct differences in WHZ among the groups were seen (data not shown).

For height gain, children in the Milk and Energy groups gained negligibly more height than those in the Meat and Control groups. As shown in Figure 2, for children with a higher baseline HAZ (above the median of -1.4), no distinct differences among any of the groups could be seen, but for children with a baseline HAZ below the median, the Milk-supplemented children gained 1.3 cm (15%) more height than the children in the Control group (p = 0.05) and 1 cm (11%) more height than those in the Meat group (p = 0.09). For change in HAZ, no pronounced supplementation effects were seen.



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FIGURE 2  Height gain (means ± SE) for the supplementation and control groups by baseline HAZ (low HAZ, <= -1.4; high HAZ, > -1.4). None of the differences were statistically significant.

 
For gain in MUAC, compared to control children, those who received the meat supplement gained ~90% more, the children who received the milk supplement gained ~50% more and those who received the energy supplement gained ~70% more in arm circumference (differences were significant for the Meat and Energy groups). The differences between the supplementation groups and the Control group were greater in the boys and in the children with lower SES (data not shown).

Children in the Meat group gained ~80% more mid-upper-arm muscle area than those in the Control group and ~30% more than those in the Milk and Energy groups. Children in the Milk and Energy groups gained ~40% more mid-upper-arm muscle area than those in the Control group.

No statistically significant differences were found for any of the variables measuring body fat, but children in the Energy and Control groups tended to have greater average increments in triceps skinfold thickness and mid-upper-arm fat area than children in the Meat and Milk groups.


    DISCUSSION
 TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The above study, we believe, is the first controlled intervention to investigate the effect of supplementation with meat or milk, comparing it to an isocaloric food supplement and a Control group without a supplement. Children provided with a daily school-based food supplement consisting of a local maize and bean dish, irrespective of what other ingredients were added, gained more weight and MUAC than children who did not receive a supplement. The equicaloric addition of meat had a beneficial effect on gain in lean body mass.

Generally, the nutritional status of the children did not improve as much as expected or it worsened over the study period, as indicated by the decreasing WHZ and stagnating HAZ. This could be attributed to the lack of rainfall and two periods of severe food shortage during the study period and/or to the reduction of the usual diet at home because of the food supplementation at school. Data for the study are now being analyzed to test if the home food consumption of the children was reduced during the study.

The lack of differences in weight and MUAC gain among the supplementation groups indicates that the additional energy provided by the food supplements might have been of greater importance than the micronutrients provided by the ASF. The energy intake from food consumed at home measured at baseline was insufficient in approximately half of the children in all groups and probably dropped during the study in periods of food shortage. If a constant energy intake is assumed, the provision of an extra 1255 kJ might have helped approximately one-quarter of the children in each in the supplementation groups to reach the recommended levels of energy intake (i.e., ~6700 kJ). Other studies, conducted in several countries, have shown that children gain weight when additional energy is provided through food supplementation (1,3,19,20,36,37). By contrast, a high-energy low-protein snack with or without micronutrients had no effect on weight or height in Thai children who were moderately stunted (38). In our study, boys had a statistically significant difference in WHZ change between the Meat and Milk groups and the Meat and Control groups. At baseline, their WHZ did not differ from that of the girls, but their HAZ and WAZ were smaller by 0.31 and 0.22, respectively, so their potential to grow may have been greater than that of the girls.

Children in the Meat group had a statistically significant greater gain in mid-upper-arm muscle area than those in the Milk and Energy supplementation groups and the Control group. To a lesser extent, children who received the milk or energy supplement also gained more mid-upper-arm muscle area than those who did not receive a supplement. Probably larger amounts of high quality protein and more bioavailable micronutrients, particularly zinc, in the meat supplement compared to those of the other supplements caused the observed beneficial effect. In addition, the meat protein was expected to increase the bioavailability of iron and zinc from the plant foods contained in the supplements (i.e., maize, beans and green leaves). Zinc is known to promote protein synthesis and consequently muscle protein. The increase in muscle mass might have led to the observed increased physical activity, which was significantly greater in the meat-supplemented children (C. G. Neumann, personal communication). On the other hand, the increased activity seen in the meat-supplemented children might have promoted an increase in muscle mass.

Mid-upper-arm fat area increased most in the energy-supplemented children and decreased slightly in the milk-supplemented children, but changes over time were <5% and differences between supplementation groups were small. The subcutaneous fat on the trunk (estimated by subscapular skinfold) decreased similarly in all groups over the study period. These findings indicate that the additional energy from the food supplements was not used to increase body fat. Other food supplementation studies showed an overall growth response with increases in MUAC and triceps skinfold (24) but no increase (23) or a decrease in skinfold thickness (39). In New Guinea schoolchildren who consumed a protein-deficient diet, supplementation with energy increased skinfold thickness but not height, whereas supplementation with protein and energy increased height but not skinfold thickness (19).

Contrary to our expectations, we did not find an overall effect of supplementation on height gain. Only the subgroup of children who were more stunted (HAZ <= -1.4) seemed to benefit from the milk supplement and gained more height than those in the other supplementation groups, particularly compared with those in the Meat and Control groups. It is known that diets containing ASF are beneficial for growth (15,17,4043). Children who are raised on strict vegan diets do not grow normally (16,44). Intake of milk and dairy products in the study population generally is small and the calcium intake of schoolchildren in the study is low (29). Baseline food intake data in the present study indicates that 99% of the children have calcium intake below the recommended daily level of 800 mg, so the additional intake of ~300 mg of calcium through the milk supplement may have had a positive effect on linear growth. On the other hand, the milk calcium might have reduced the absorption of iron (45) and zinc (46) from the supplement. The protein intake of our study children (home diet at baseline plus supplement) was at least three times the recommended amount; therefore, it is unlikely that protein was the limiting factor for growth. It could be that the high prevalence of micronutrient deficiencies in the study population (J. H. Siekmann, unpublished results) prevented the efficient use of the energy provided by the supplement (47). The micronutrients provided by the supplements might not have been sufficient to promote linear growth because of the initial poor status of these nutrients. Because the proportion of wasted children in the study was low, it was not anticipated that an increase in weight would happen first, before linear growth could respond. It might be that the energy provided was sufficient to promote a gain in weight but not in height.

We are not aware of other studies' supplements in which meat has been fed to children, but trials have been conducted to evaluate the effect of milk supplements on growth. For example, in the United Kingdom, where 1 pint (570 mL) of school milk was provided daily to boys ages 6–11 y, their height increased by 2 cm in 1 y more than in a control group (18). Another study of socially disadvantaged school children in the United Kingdom showed a positive, significant effect of providing 190 mL of milk on weight and height gain (21). The age group, sample size, amount of milk given and duration of the latter study were very similar to those in our study. Two studies on the effect of skim milk powder on growth in school children in New Guinea showed increased growth in weight and height (19,20). The Institute of Nutrition of Central America and Panama food supplementation trial in Guatemala found that child growth was promoted through a supplement providing extra energy and that there were no additional benefits on growth of a supplement that had milk powder added (39). This was probably due to nutrients other than protein and energy being inadequate in the milk supplement (41).

It could be that the 2-y intervention was too short to produce detectable differences in height gain between the different supplement groups and the control group, although other food supplement interventions in children of this age group have lasted for only 10 or 13 wk (19) up to 21.5 mo (21) and produced an improvement in height.

The results suggest that children with higher nutrient need, such as boys, and younger and moderately stunted children benefited more from the food supplements. This is expected because they have a greater potential for growth. Children from households with lower SES also benefited more from the supplements, probably because their nutrient intake and other factors relating to growth are inadequate.

One strength of our study is the attempt to measure other factors that might have influenced the growth outcomes. These were considered in the multivariate analyses and helped to explain the impact of the supplementation on the outcome variables. The statistical analyses took into account the fact that the study had a nested design, i.e., the food supplement was randomized by school and not by child. Embu District was an appropriate area to test the effects of ASF because the habitual diet contains no or very little meat and dairy products and is low in fat and largely cereal- or tuber-based. All analyses were controlled for morbidity; therefore, it is unlikely to have confounded the results to any large degree.

We tried to keep the study children and their families, teachers, field workers and everybody else involved in the study unaware of the different types of food supplements, but it is possible that some of them found out. This could not be avoided in the setup of the study within the communities. Although there could have been some bias in favor of the meat and milk supplementation groups because these foods are culturally perceived as nutritious foods, this is not very likely and anthropometric measurements are not subjective.

In conclusion, the results show clearly that the weight and MUAC of children can be improved through the daily provision of a food supplement containing local foods and that enrichment with meat can increase lean body mass.


    ACKNOWLEDGMENTS
 
We thank all participants and field and office workers of the Child Nutrition Project in Embu for their contribution to this study. We are grateful to all government officials, headmasters, teachers, doctors, hospital workers and others who facilitated our work.


    FOOTNOTES
 
1 Presented at the conference "Animal Source Foods and Nutrition in Developing Countries" held in Washington, D.C. June 24–26, 2002. The conference was organized by the International Nutrition Program, UC Davis and was sponsored by Global Livestock-CRSP, UC Davis through USAID grant number PCE-G-00-98-00036-00. The supplement publication was supported by Food and Agriculture Organization, Land O'Lakes Inc., Heifer International, Pond Dynamics and Aquaculture-CRSP. The proceedings of this conference are published as a supplement to The Journal of Nutrition. Guest editors for this supplement publication were Montague Demment and Lindsay Allen. Back

2 This research was supported by the Global Livestock Collaborative Research Support Program (GL-CRSP) through the Office of Agriculture of the United States Agency for International Development under Grant No. PCE-G-00-98-00036-00 to the GL-CRSP. Back

3 Supported in part by the Netherlands Organization for International Cooperation in Higher Education (NUFFIC) and the International Foundation for the Promotion of Nutrition Research (ISFE), Switzerland. Back

5 Abbreviations used: ASF, animal source foods; HAZ, height-for-age Z-score; MUAC, mid-upper-arm circumference; NCRSP, Nutrition Collaborative Research Support Program; SE, standard error; SES: socioeconomic status; WAZ, weight-for-age Z-score; WHZ, weight-for-height Z-score. Back

6 Intrateam: weight 6% (n = 461), height 2% (n = 165), MUAC 6% (n = 462), subscapular skinfold 6% (n = 462) and triceps skinfold 6% (n = 462). Interteam: weight 5% (n = 373), height 3% (n = 255), MUAC 5% (n = 376), subscapular skinfold 5% (n = 376) and triceps skinfold 5% (n = 376). Back


    LITERATURE CITED
 TOP
 ABSTRACT
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