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24. Habitual Guatemalan diets and catch-up growth of children with mild to moderate malnutrition

Benjamin Torún, Benjamin Caballero,' Samuel Flores-Huerta, Fernando Viteri

Institute of Nutrition of Central America and Panama (INCAP) Guatemala City. Guatemala

Objective

To determine whether a diet based on traditional Central American foods could promote adequate catch-up growth of children with mild-to-moderate malnutrition, provided that: (a) there were no constraints in the amounts of staple foods available to satisfy the children's appetite; (b) the energy density of some foods and beverages was increased by adding oil and sugar; and (c) an adult would help and stimulate the children to eat at mealtimes.

Experimental Details

Subjects

Nine boys and four girls of mixed Mayan and Caucasian descent (Ladings), 15 to 40 months old (mean ± SD = 27 ± 7).

All children were apparently healthy when admitted to INCAP, but most were underweight for their height. All had been attending a child-care centre in Guatemala City, six days per week, for at least four months. Their weight-for-height had been stable a minimum of three months prior to the present study. Four children had 92 per cent or more of the weight expected for their height, compared with the 50th percentile of the Boston Standards. Since weight-for-height is one of the criteria used for the discharge of children treated for protein-energy malnutrition at INCAP and, in our experience. some children do not show further catch-up in weight-for-height beyond 92 per cent, it was decided to evaluate the results of the study as a subgroup of nine children admitted with less than 92 per cent weight-for-height and four children admitted with a higher weight-for-height. For the same reasons, measurements done in the nine children admitted with less than 92 per cent weight-for-height were evaluated before and after reaching that level of catch-up in weight.

TABLE 1. Characteristics of the Children at the Beginning of the Study

a Mean of first seven days of the study

b Weight expected for height: 100 % = 50th percentile of Boston Standards

Anthropometric and other characteristics of the children are shown in table 1.

Study Environment

INCAP's Clinical Centre in Guatemala City; 1,500 metres above sea-level; temperature 18 to 24° C throughout the year; relative humidity to 40 to 60 per cent.

TABLE 2. Average Composition and Frequency of Consumption of Diets Customary for many Children of Pre-school Age in Rural Guatemala

Bean:corn ratio = 15:85 by weight and 29:71 by protein contents.
Animal protein = 16% of total.
Energy from fat (including natural fat content of all foods) = 16% of total energy.

Duration of the Study

Two weeks were allowed for adaptation to the new environment at INCAP, the metabolic ward personnel, the foods, and times of meals. After that, 11 children were studied for 12 to 14 weeks and two were studied for nine weeks. The metabolic balance studies were not interrupted during days of illness.

Diet

1. The diet was based on the proportions of foods eaten by pre-school children from poor socioeconomic-level families in Guatemala (table 2). The menus shown in table 3 were prepared for three daily meals and a mid-afternoon snack, with variations over the seven days of the week. The variety of vegetables, fruits, and dairy equivalents were limited to those shown in table 3 for practical reasons of food preparation in the metabolic kitchen. A child could eat as much as he wanted of any food. except bread and the foods of animal origin (milk, egg, meat), which were limited to the maximum amounts shown in the menus, although the children were not forced to finish any portion. Black beans and corn are the main staples, and they were offered in separate proportions of approximately 45 55 by protein content. although the children were free to eat any amount they wanted of either staple or of the other foods. except for those limited to a maximum, as described above. Drinking water was available ad libitum.

TABLE 3. Menus Offered to the Children^a

a All foods offered ad libitum except when amounts are specified Lemonade and water offered ad libitum at bedtime.
b Black bean (Phaseolus vu/garis) puree
c Corn-based beverage (atole) and soft corn bread (tamale)
d Sweet bread roll prepared with sugar and lard
e Chayote = guisquil = Sechium edule

2. The energy density of the diet was increased by adding 27.4 9 of vegetable oil per 500 9 of cooked black beans, ready to eat (5.5 per cent oil), and sugar to the beverages (10 per cent to the milk and 20 per cent to corn atole and lemonade).

3. A nurse's aide played the role of "mother" at mealtimes, encouraging the children to eat, without forcing them, and helping those who needed assistance. If a child did not want to eat, he sat at the table with the others until all finished (usually 30 to 45 minutes).

4. Foods and beverages were prepared with sugar fortified with vitamin A and NaFeEDTA (1.5 9 retinol and 13 mg Fe/100 9) and with iodized salt (1 :10,000-15,000). No other vitamin or mineral supplements were given.

Physical Activity

The children were encouraged to be as active as healthy children who live in a good home environment. This was done through daily outdoor walks and participation in games that required walking, running. jumping, or climbing. The children were not forced to participate in those activities when they did not feel like doing so, nor were they ever pushed to exhaustion. The activities alternated with periods of rest or sedentary play to avoid boredom or fatigue.

Indicators and Measurements

Food Intake

Each food was served in separate dishes or cups. The amounts eaten at each meal were measured by weighing the food containers immediately before and after the meal. Corrections for spillage were done when necessary. Water, but no food. was allowed between meals and it was also measured.

Collection of Urine and Faeces

Urine and faeces were collected in 24-hour periods from 12 children throughout the study. Those who were not fully toilet-trained wore urine-collection bags, and their physical activity was only moderately affected. Twenty-four-hour specimens were collected on every fourth day from the youngest child in the group.

Urine collections began and ended near 7 a.m. of two consecutive days and the volume was adjusted to 24 hours. Stools were pooled between 1 p.m. of two consecutive days without use of faecal markers.

Metabolic Balance Studies

The daily faecal pools and aliquots for each food were homogenized and dried to a constant weight in convection ovens at 95 ± 10° C. Previous tests showed that there were no differences in dry matter, total nitrogen, and total energy contents of faeces dried in this manner and those dried in vacuum ovens at 30 to 40° C. The powdered faeces and foods were homogenized and stored in air-tight jars until analysed.

Urine, faecal. and food aliquots were analysed for total nitrogen (micro-Kjeldahl). Seven-day faecal pools were prepared in proportion to the dry matter excreted each day. The energy contents of aliquots of those seven-day pools and of foods were measured by bomb calorimetry, using dry, certified benzoic acid as standard. Net energy intake was calculated as the bomb calorimetry value of intake (gross energy) minus faecal energy.

Apparent nitrogen and energy digestibilities were calculated from dietary and faecal contents. "True" nitrogen digestibility was calculated assuming obligatory faecal losses of 20 mg N/kg/day. "True" nitrogen balance was calculated by subtracting from intake the urinary and faecal nitrogen, assuming 8 mg N/kg/day as integumental and other insensible N losses. Nitrogen balance and energy absorption were calculated in 12 children on a weekly basis, pooling the dietary, urinary, and faecal data of seven consecutive days because of the daily variability in ad libitum food intake, the variation in protein sources in each day's menus, and the unreliability of faecal N analysed in one 24-hour collection. In the child on whom faecal collections were performed on every fourth day, N balance and digestibility and energy absorption were calculated in 28-day periods (i.e. pooling data of seven consecutive collections representing the seven days of the week).

Anthropometry

The children were weighed naked every morning before breakfast. Length (reclining height), leg and arm circumference. and subcutaneous thicknesses at three sites (subscapular, tricipital, and paraumbilical) were measured every 14 days by one of two well-standardized physicians. Height measurements were always checked on two consecutive days.

Total Energy Expenditure

Energy expenditure was estimated by monitoring the children's heart-rate (HR) throughout the day and calculating energy expenditure from individual determinations of heart rate and oxygen consumption (VO₂). The heart-rate/oxygen-consumption relationship was determined in each child at monthly intervals. HR was continuously monitored with light-weight, portable, heart-beat accumulators (Transmed, San Luis Obispo, California). for at least 10 days before and after the determination of the HR-VO₂ relationship. These measurements were not done when a child was ill because the HR-VO₂ relationship is altered. The relationship was determined with the child lying down and then walking on a treadmill at various grades, without approaching maximum workloads, while HR was monitored by telemetry. Oxygen concentration in exhaled air was determined with a microfuel analyser (Teledyne, San Gabriel, California) calibrated with standard gases, and air volume with a dry-gas meter calibrated with a 660-litre Tissor gasometer. Volumes were converted to standard conditions of temperature, pressure, and humidity (STPD), and energy expenditure was calculated assuming 4.9 kcal/litre O₂ m, STPD, as the energy equivalent of oxygen consumption during mild-to-moderate exercise.

Total daily energy expenditure was calculated from HR during 14 "active" hours of the day (6 a.m. to 8 p.m.) and from basal energy expenditure (BMR) during 10 hours of night (8 p.m. to 6 a.m.). Technical problems did not permit direct BMR measurements in these children, and an average value of 2.3 kcal/kg/hour was used, derived from many measurements done by us in similar children with a coefficient of variation of ± 7 per cent.

Other Biochemical and Haematological Determinations

Routine haematological, urinary, and stool analyses were done on admission to INCAP. Determinations of haemoglobin, serum iron, TIBC, ferritin. plasma proteins, and vitamin A were done on admission, 45 days later, and at the end of the study.

Statistical Analyses

Changes in weight were evaluated by regression analysis. Data calculated or measured at 7- and 14-day intervals were evaluated by analysis of variance or regression. The changes between beginning and end of the study were analysed by the Student's paired t test.

TABLE 4. Infectious Episodes during Treatment

a. URI = upper respiratory infection

TABLE 5. Average Daily Food Intake Calculated on a Weekly Basis (mean + standard deviation)

a Groups differ. P < 0 05.
b Groups differ. P < 0.01
c Net energy = food energy (bomb calorimetry) - faecal energy (bomb calorimetry).

Unless otherwise noted, the data in the text and tables are expressed as the mean + standard deviation.

Summary of Main Results

Health

The children were healthy most of the time, but ten children had a total of 17 infections. These ranged from impetigo without systemic manifestations to shigellosis with high fever and diarrhoea (table 4). The periods of illness affected appetite for food, weight-gain, and metabolic balances. The data were, therefore, analysed separately for the days (or weeks) when the children were healthy or ill.

Food Intake

1. Foods were divided into "solids" and "liquids" (atole, milk, lemonade, water), since intake of the former allows a better assessment of appetite because the intake of liquids is influenced by both hunger and thirst. Total food intake was 41.7 9 solid foods and 83.7 9 liquids/kg body weight/day, with weekly variations of 18 and 16 per cent respectively (standard deviations = 7.5 and 13.2 g/kg/day respectively). The nurse's aides in charge of assisting the children at mealtimes were initially helping them more than might be expected from the average working woman from a low economic and educational background in Guatemala. This solicitude was decreased after the first five children admitted to the investigation had been under study for 31 days. Those children diminished their food intake by 10-15 per cent during the following two to three weeks.

During periods of illness there was a tendency to decrease solid food and dietary energy intakes (table 5). On comparing the children's intakes when they were not ill, it was found that they ate more solids when their weight was below 92 per cent of that expected for their height than afterwards (table 5), suggesting a decrease in appetite as they approached normal weight-for-height.

2. The average net energy intake of the 13 children was 98.3 ± 4.3 kcal/kg/day. Most (76.5 per cent) was derived from carbobydrates, 7.8 per cent from proteins, and 15.7 per cent from fat. The sugar used in food and beverage preparation provided around 40 per cent of the net dietary energy, which is approximately two times higher than the proportion of energy derived from sugar in the average diet of rural Guatemalan children.

TABLE 6. Initial and Final Anthropometric Measurements of Children Admitted to the Study with Less or More than 92 per cent of the Weight Expected for their Height^a

a. Weight expected for height: 100% = 50th percentile of Boston Standards
b. Using each child's average weight during the first and )last weeks on the study
c. Mean + standard deviation.
d Corrected for subcutaneous skinfold thickness.
e Sum of three sites tricipital, subscapular, and paraumbilical.
f Children admitted with different weight-for-height had different initial values, P < 0.01. All final values were greater, than initial, except for lean arm diameter
(P < 0.01).

TABLE 7 Mean Rates of Change in Anthropometric Measurements of Children Admitted to the Study with Less or More than 92% of the Weight Expected for their Height^a

a Weight changes calculated by individual regression analysis throughout the entire study, including days of illness All other changes calculated by individual differences between the initial and final measurements
b Mean ± standard deviation
c Corrected for subcutaneous skinfold thickness
d Sum of three sites: tricipital, subscapular. and paraumbilical
e. Groups differ, P < 0.05

Dietary energy intake decreased when the children were ill (table 5) and it was higher in the earlier stages of catch-up growth (i.e. while weight was below 92 per cent of that expected for height). Five healthy children whose weight-for-height had become stable during the last two weeks of the study. and whose mean weight-gain continued at the rate expected for the children's age and size (0.6 ± 0.4 g/kp/day), had net energy intakes of 90.5 ± 5.5 kcal/kg/day during those two weeks. Five other healthy children with high growth-rates at the end of the study (1.6 + 0.7 g/kg/day) and whose weight-for-height was still increasing, had net energy intakes of 97.9 ± 7.7 kcal/kg/day during the last two weeks. The energy intake of these rapidly growing children was higher than that of children growing at a slower rate (P < 0.05).

"Metabolizable" dietary energy is about 0.7 kcal/kg/day less than the net energy intakes, if it is assumed that 5 kcal are lost per gram of urinary nitrogen and 8 kcal per gram of sweat nitrogen.

3. The average protein intake was 1.99 ± 0.51 g/kg/day. It showed the same trends of change as those of solid food intake (table 5). The protein-energy ratio was slightly higher during the early phases of catch-up growth than in the latter part of the study (P = 8.1 and 7.7 per cent respectively). Black beans and corn provided 70 per cent of the protein, other vegetable foods 17 per cent, and animal foods 13 per cent. The ratio of bean/corn protein ingestion was 53.47 ± 2, which coincides with an optimal aminoacid complementation.

TABLE 8. Changes in Weight Calculated by Regression Analysis of Various Time Segments (g/kg/day)

a. Excluding days of illness that produced weight loss (see table 4).
b. Number of days used in the weighed regression analysis
c. Including five days with diarrhoea and marked weight loss.
d. Groups differ: paired and group t" test. P < 0 01
e. Groups differ: paired "t', P < 0.05; group "t", P < 0 01.

Growth and Catch-up

The anthropometric changes shown in table 6 indicate good rates of growth and tissue accretion. The increments in leg circumference suggest an increase in muscle mass. The increments in subcutaneous skinfold thickness suggest that there was also an enlargement of the body fat stores. The children admitted to the study with less than 92 per cent of the weight expected for their height had a larger increment in subcutaneous fat than those admitted with more than 92 per cent.

Weight

Table 7 shows that over the whole study period, children gained weight at or above the rate expected for children of the same height which is around 0.6 g/kg/day. The only exception was child 482 who lost much weight during a nine-day episode of shigellosis with several days of high fever and profuse diarrhoea. During the 53 days that he was not ill, he gained 0.74 g/kg/day (table 8).

Changes in body weight were evaluated by regression analysis, taking into account three circumstances that might influence weight: (a) illnesses, (b) degree of nutritional deficit, and (c) influence of the persons feeding the children.

The average change in weight during the 12 infectious episodes that were accompanied by weight loss or a decrease in the rate of weight gain was -2.04 ± 3.42 g/kg/day, ranging from 0.33 to - 11.65 g/kg/day. The child with the greatest weight loss had profuse diarrhoea. If he were excluded from the analysis, the rate of weight loss during the illnesses would have been -1.17 ± 1.68 g/kg/day, ranging from 0.33 to 4.96 g/kg/day.

When the children were not ill, they grew more when their nutritional deficit had been more severe (table 8). The cut-off point of 92 per cent of the expected weight-forheight was selected based on the criteria described under "Experimental Details"; the velocity of weight gain, however, did not tend to level off at that point (see below). If the cut-off point had been selected for each child when the individual growth rates clearly began decreasing, the difference in weight gains between early catch-up and the latter phase would be even greater than that shown in table 8.

Three of the four children who were admitted to the study with 92 per cent or more of the weight expected for their height gained weight at the same rate as those who reached 92 per cent after admission (1.27-1.71 g/kg/day), and they continued increasing in weight-for-height. The only exception was child 482 who lost much weight shortly after beginning the study due to the episode of shigellosis mentioned above. He later began catching up, albeit at a relatively slow rate, and at the end of the study had again reached 92 per cent of the standard weight-for-height.

As mentioned above, the first five children admitted into the study were helped to eat at mealtimes more vigorously than planned for the first 31 days. By that time, three had surpassed 92 per cent of weight-for-height and two were at 91 per cent. They gained weight at a faster rate than those who were helped less and who had not yet reached 92 per cent of weight-for-height (3.41 ± 1.23 and 2.16 ± 1.01 g/kg/day, respectively, P < 0.05).

Height

Table 7 shows that, on the average, height increments were slightly below the 0.3-0.33 mm/day expected for children of these sizes. Four children continued growing within the channel of stunted height that they had at the beginning of the study, five showed a small catch-up in height-for-age, and four decreased by 1 or 2 per cent.

Weight-for-Height

All children except one (child 482) increased in the weight expected for their height. The children admitted with less than 92 per cent caught up with the others by the end of the study (table 6). Child 482 decreased from 92 to 88 per cent when he had shigellosis, but by the end of the study had reached 92 per cent again. Child 478 increased from 82 to 88 per cent by the end of the study. All others finished at a level between 92 and 106 per cent.

The velocity of weight gain did not decrease in all children at the same point of catchup in terms of weight-for-height. It tended to level off in one child at 88 per cent, in four at 93 to 94 per cent, in two at 96 to 98 per cent. and in one about 106 per cent, while it had not levelled off in five children who were still increasing in weight-forheight at the end of the study and had reached 92 to 98 per cent of the expected value.

Food Digestibility

Apparent absorption of dietary energy was 91.3 ± 1.7 per cent. Apparent protein digestibility was 66 ± 7 per cent. "True" digestibility was 73.7 ± 7 per cent.

Nitrogen Balance

On the average, all children were in positive nitrogen balance. The mean N retention for all children throughout the study was 94 ± 37 mg N/kg/day (n = 146 child-weeks), assuming integumental losses of 8 mg/kg/day. The weekly N retentions were lower during the weeks when the children were III than when they were healthy (98 + 36, n = 131; and 62 ± 30 mg N/kg/day, n = 15, respectively; P < 0.01). The decrease in N retention was due to a lower protein intake and an increase in urinary nitrogen excretion, relative to N intake, and an increase in urinary nitrogen excretion, relative to N intake, when the children were sick. The proportion of ingested nitrogen excreted each day through urine was greater on the days of illness (40 ± 17 per cent, n = 112) than when the children were not sick (35 ± 11 per cent, n = 9101 paired "t" test for eight children = 3.647, P < 0.01).

There were no differences in the weekly N balances of the whole group of children as a function of time (i.e. week by week). The weekly nitrogen retentions and their daily proportions of ingested nitrogen excreted through urine were similar whether or not the children had reached 92 per cent of weight-for-height.

Energy Expenditure

Measurements of the heart-rate-oxygen-consumption relationship and of continuous heart-rate monitoring were obtained from only 11 children. The estimates of the total energy expended by those children, as calculated from heart-rate monitoring in three or four different occasions at 20- to 30-day intervals, were 66 ± 7 kcal/kg/day.

TABLE 9. Blood Chemistry and Haematology during the Study Period (Mean _ SD; n = 13)

a Values differ from the preceding determination, student's paired "t" test, P < 0 01 b n= 11

These values were too low. This may be because of an underestimation of basal energy expenditure (since basal metabolic rate increases during catch-up growth), inaccuracies in the heart-rate measurements, or a combination of both. The low energy expenditure resulted in a mean energy retention (net intake-expenditure-urine and skin losses) that was too high 31.5 kcal/kg/day, or about 19 kcal/g weight gain.

Haematological and Biochemical Analyses

Table 9 shows that the haematological indicators (packed red-cell volume and haemoglobin concentration) and the indicators of iron nutriture and body-iron stores improved within 45 days from the start of the study. On admission to INCAP, subnormal levels in the concentration of blood haemoglobin were found in seven children, of serum iron in seven, of transferrin saturation in ten children, and of plasma ferritin in seven. Forty-tive days later, only two children had subnormal values of those indicators, and by day 90 only one child had moderately low values of serum iron and transferrin saturation. The improvement can be attributed to the intake of NaFeEDTA in sugar, since it was estimated that the amounts of food iron provided by the experimental diet were similar to the amounts in the diets eaten by the children in day-care centres for at least four months prior to their admission to INCAP. It must be noted that the intake of sugar (on the average 108 g/day) was higher than the 4045 g/day expected in children from the general population, since sugar was added to all beverages (except water) to increase the energy density of the overall diet. This high amount of sugar provided, on average, 14.1 mg Fe from NaFeEDTA.

The other biochemical indices of nutritional status that were analysed were normal on admission and continued so throughout the study.

Comments and Conclusions

1. The experimental diet allowed good catch-up in terms of weight. Height catch-up, however, was observed in only five children. This could have been caused by dietary inadequacy, an experimental period that was too short to allow height increments, or irreversible stunting as a consequence of chronic malnutrition from an early age.

2. The occurrence of acute infections did not interfere with the overall catch-up in weight or positive metabolic balances.

3. The results confirm the conclusions of previous studies with well-nourished children* namely, that:

- Habitual Central American diets can satisfy the protein and energy needs of preschool children if: (a) dietary energy density is increased; (b) sufficient amounts of the staple foods are available; (c) the foods are prepared and offered to the children as they would be to adults; (d) an adult or older child helps the preschooler at meal-times; (e) the child lives in an environment with good sanitation.

- It is not essential to provide foods of animal origin every day of the week.

- It is not necessary to modify the composition of the diet during or after short, acute, episodes of disease if the foods are available in sufficient amounts to satisfy the child's appetite.

- The energy needs of children two to four years old can be satisfied with net dietary intakes of 85-80 kcal/kg/day. Intakes of 95 105 kcal/kg/day allow catch-up in mild-to-moderate malnutrition.

4. It is still necessary to show whether or not the preceding conclusions are correct when children live in an environment with poor sanitation and are prone to a high infectious morbidity.

Acknowledgements

The investigations were carried out with the financial assistance of the Danish International Development Agency (DANIDA) and the United Kingdom's Overseas Development Administration. The Food and Agriculture Organization of the United Nations (FAO) administered funds from DANIDA and made the award to INCAP. Drs. Caballero and Flores-Huerta participated in the investigations with a fellowship from the United Nations University World Hunger Programme. Dr. Ramiro Batres and Ms. Roquea Sidiqqua participated in the analysis and interpretation of parts of the investigations.

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