a Ranges estimated from mothers' information.
Means differ: * p < 0.05; ** p < 0.01.
Source: Calculated from RUTISHAUSER and WHITEHEAD, 1972.

3.3.2 Guatemala

TORUN and CHEW (unpublished) studied 69 boys and girls, 26 years old, who lived in a poor neighborhood in the outskirts of Guatemala city. The activities that they performed between 8 a.m. and 5 p.m. were recorded and timed on two separate weekdays using a modified time-motion technique (TORUN, 1984). The 56 activities recorded were classified in six categories of physical effort, from sedentary to very heavy (Table 4).

Table 4. Activities performed by preschool children in a marginal area of Guatemala, and classified according to effort. The energy costs of the grouped activities were estimated as multiples of basal metabolic rate

Source: TORUN and CHEW, unpublished observations.

Twenty-one children were considered mildly malnourished, based on weights-for-height between 81 and 90% of the NCHS/WHO median values, whereas 43 had between 91 and 110%, and 5 between 112 and 119% of the standard weights-for-height.

Compared with the well-nourished children, the malnourished spent 11.2% more time in sedentary activities, and 4.8, 1.7 and 2.5% less time in light, heavy and very heavy activities, respectively (Figure 4A). The longer time spent in light physical activities at the expense of those that demanded more energy became even clearer, when the activities were classified in only three categories of physical effort (Figure 4B).

Energy expenditure was estimated applying energy-cost factors of 1.2, 2, 2.25, 2.5, 3 and 4 times basal metabolic rate (X BMR) to the six categories of activities observed. Based on information provided by the mothers, sleeping time was added at 1.0 X BMR, and an energy expenditure of 1.52 or 1.43 X BMR was assumed for the balance of 25 hours. The children with weight-for-height > 90% of the NCHS median had an estimated expenditure of 81 kcal/kg/d, compared with 77 kcal/kg/d among the mildly malnourished.

Sixty of the 69 children were studied again, 2 and 4 months after the beginning of a nutritional education and supplementation program, on 2 separate weekdays each time (TORUN and CHEW, unpublished). At the end of the 4-month period, weight-for-height had increased by 3% or more in 23 children, remained stable within ±3% in 27, and decreased more than 3% in 10 children. An analysis was done of the time that those three groups of children dedicated before and after the intervention to activities that demanded different levels of physical effort.

Figure 5 shows that the children whose nutritional status improved, reduced the time dedicated to sedentary and light activities and significantly increased the time in moderate activities. On the other hand, the children whose nutritional status deteriorated, increased the time devoted to sedentary activities by reducing heavy activities.

The comparison between groups (Figure 5), showed that the children whose weight-for-height improved: (a) reduced the time spent in sedentary and light activities, in contrast with the other two groups, (b) increased the performance of moderate physical activities, and (c) continued with the same proportion of heavy activities, in contrast with the children who lost weight-for-height.

4. School-age children

Spurr and collaborators (SPURR et al., 1986; SPURR and REINA, 1987, 1988a, b, c, 1989a) did a series of studies in a total of 300 boys and 146 girls between 6 and 16 years old, who lived in economically deprived urban areas of Cali, Colombia. They were classified as nutritionally normal (controls) when weight-for-height and weight-for-age were between 95 and 110% of Colombian standards, and as marginally undernourished when both indicators were < 95% of the standards. Total daily energy expenditure was calculated from individual heart rate to oxygen consumption calibrations when heart rate was above a critical value, from resting metabolic rate when heart rate was below that value, and from BMR at night.

In many of these children, energy expenditure was also calculated at specific times during the day from minute-by-minute heart rate measurements. This allowed the evaluation of patterns of activity of different intensity (SPURR and REINA, 1988b, c) and the time spent in activities with energy costs equivalent to various multiples of BMR (SPURR and REINA, 1989a).

During the school year, there were no consistent differences related to nutritional status in the patterns of activity levels (SPURR and REINA, 1988b). However, when a group of boys 10-12 years old were studied during an ordinary schoolday, and again about 6 months later in a summer camp, where they were encouraged to participate in supervised sports (soccer, basketball, calisthenics, foot races, etc.) and play (walks, swimming, games), important differences were observed between the marginally undernourished and the controls (SPURR and REINA, 1988c). As shown in Figure 6, the controls increased their activity level in the summer camp, compared with the schoolday. In contrast, the undernourished boys did not show marked changes between summer camp and school, except for a transient increase in activity level in the early afternoon. Consequently, the difference between the two nutritional groups became more accentuated at summer camp. Table 5 shows that the estimated total daily energy expenditure did not differ between groups on schooldays, but it did during the summer camp (p < 0.01) due to the increased expenditure shown by the control group in relation to the energy they expended on schooldays (p < 0.05).

Table 5. Total daily energy expenditure of 10- to 12-year-old boys, measured during the school year and about 6 months later in a summer camp (mean ±standard deviation)

Source: SPURR and REINA. 1988c.

Using the minute-by-minute heart rate technique, these investigators also calculated the time spent during daytime by boys and girls 6-8, 10-12 and 14-16 years old, in activities of light, moderate, high and very high intensity (SPURR and REINA, 1989a). Overall, they found no effects of nutritional status on the time allocated to the various levels of activity. However, if one looks at the time allocations separately for each age and sex group, there are differences between the undernourished and control children aged 6 to 8 (Figure 7): the undernourished boys spent more time in light activities and less in activities of high and very high intensity, compared with the control group. Similarly, the undernourished girls spent more time in moderate and less in heavy activities than their well-nourished counterparts.

This coincides with the separate (SPURR et al., 1986; SPURR and REINA, 1988b) or aggregate (SPURR and REINA, 1989a) reports on the total daily energy expenditure of these and other Colombian children: on the average, undernourished boys 6-8 and 1012 years old spent 18 and 10% less energy than their corresponding controls, respectively (p < 0.01). Mean energy expenditures tended to be lower than in the controls, but the differences were not significant (p > 0.1) among the 14-16-year-old boys (8%) and the girls aged 6-8 (7%), 10-12 (6%) and 14-16 (1%).

The sex-related differences in energy expenditure were explained by SPURR and REINA (1988b) as being due to cultural attitudes, whereby girls are less active than boys. We interpret the age-related differences as being due to social and peer pressures that increase as children grow older. The younger well-nourished boys are probably more prone to exert their physical activity without restraint during their daily routine, thereby increasing the difference from their undernourished peers, very much like what occured in summer camp (SPURR and REINA, 1988c). This is consistent with the nutrition-related differences in physical activity observed among preschool children in Uganda (RUTISHAUSER and WHITEHEAD, 1972) and Guatemala (TORUN and CHEW, unpublished).

5. Short- and long-term effects

5.1. Adaptation and accomodation
5.2. Reduction in energy expenditure
5.3. Behavior and social performance
5.4. Low physical activity and growth
5.5. Reduction in physical fitness

The studies that have looked at the effects of low or restricted energy intakes on the activity of infants and children, although small in number, coincide in that reduced intake leads to shorter duration or lower intensity of physical activity. This occurs within a few days after dietary energy decreases VITERI and TORUN, 1981). Initially, it seems to be a compensatory response to maintain energy balance without comprising growth. But if the dietary restriction is large enough, the decrease in activity and overall energy expenditure is not sufficient to preserve growth (TORUN and VITERI, 1981a).

5.1. Adaptation and accomodation

Children with a chronically low energy intake that is not so extreme as to produce the clinical signs and metabolic changes of severe malnutrition, maintain a state of energy balance. In discussing the implications of this balance, it is necessary to differentiate between what may be called adaptation and accomodation.

We speak of adaptation when metabolic and behavioral modifications allow a more efficient use of the energy available without producing undesirable effects (e.g., reducing BMR or performing mechanical work with less costly movements). This has a different connotation from metabolic and behavioral modifications that permit survival and function at the expense of actually or potentially undesirable effects (e.g., increased risk of diseases and severe malnutrition, or limitations to perform activities that are healthy or economically and socially desirable). This can be referred to as accomodation (SRIMSHAW and YOUNG, 1989; BENGOA et al., 1989).

5.2. Reduction in energy expenditure

A decrease in BMR in the absence of reduced growth rate or an improvement in mechanical efficiency has not been demonstrated in undernourished children to explain the reduction in total energy expenditure shown in the studies discussed above. Even if these phenomena had occured without being detected, they could not be the sole explanation for the reduction in energy expenditure. Infants, preschool children and school-age children did become less active and engaged less or no longer in certain activities (CHAVEZ et al., 1972; CHAVEZ and MARTINEZ, 1979; RUTISHAUSER and WHITEHEAD, 1972; VITERI and TORUN, 1981; TORUN and CHEW, unpublished; SPURR and REINA, 1989a).

This was more evident in younger children, probably because they were subject to less social constraints and peer pressure. In the case of children who go to school, it seems that the school routine, which occupies a large proportion of daytime and restricts free physical activity, tends to mask the potential differences in activity related to nutritional status. The differences may become evident when children are given the opportunity and are encouraged to be more physically active, as seen in the summer-camp studies of SPURR and REINA (1988c).

5.3. Behavior and social performance

CHAVEZ and MARTINEZ (1979) showed enhanced behavioral and exploratory activities associated with increased physical activity in the better nourished young preschool children. From the studies of preschoolers in Uganda and Guatemala it can be inferred that children who had adequate energy intakes and spent less time sitting or lying down and more time walking and moving around, had more frequent interactions with their peers, adults and their physical environment. This was, in fact, the subjective appraisal of the investigators and staff who participated in the clinical and community studies in Guatemala. Other investigators have also suggested that low energy intake and expenditure are likely to decrease the interactions between children and their immediate environment (GRAVES, 1976, 1978; RICCIUTI, 1981; BEATON, 1983).

POLLITT (1987) has pointed out the conceptual and methodological problems that do not allow making definitive statements about the influence of dietary energy deficiency on cognitive and socioemotional development. One of the major obstacles is the difficulty - if not impossibility - of isolating the nutritional components from other factors that affect the behavior and development of children. Nevertheless, the evidence that better nutrition allows more activity supports the suggestion of a sequential cause-effect linkage between adequate energy intake (r) enhanced physical activity (r) more interaction with people and the environment (r) better social performance and cognitive development.

5.4. Low physical activity and growth

Physical activity is markedly reduced in malnourished children. VITERI (1973) used an animal model to demonstrate that this reduced activity contributed, by itself, to growth impairment. Weanling rats were fed either 50 or 73% of the food normally eaten by rats of the same age. When they were inactive, living in small metabolic cages, growth in length and weight gain were significantly less (p < 0.01) than in pair-fed animals who lived in larger cages and were forced to run in a revolving drum twice daily.

The negative effect of inactivity on the growth of malnourished animals and the positive effect of exercise can be reversed, as shown in another experiment with a cross-over design with rats fed 60% of the normal food intake VITERI and TORUN, 1981). Whether the animals were inactive from the beginning of the study or became inactive after an initial period of forced activity, growth rate decreased. Conversely, an increment in activity produced better growth in length and weight.

The positive role of activity was further confirmed in the course of the nutritional rehabilitation of malnourished 2- to 4-year-old children (TORUN et al., 1976, 1979). When a group of patients were encouraged to participate in games that involved running after a ball, walking up a slope, climbing stairs and rolling and tumbling, they grew more in length and lean body mass than a control group of patients who continued with the usual, limited activities customary in most nutritional rehabilitation centers. Based on individual weekly calibrations of heart rate to oxygen consumption and heart rate monitoring, mean energy expenditure during the daytime was calculated as 1.97 X BMR in the more active children, compared with 1.70 X BMR in the control group.

In a more recent study using a similar program of physical activity in a hospital for malnourished children in Guatemala, but with food intake ad libitum, preliminary results indicated that the more active patients reached normal weight-for-height earlier than their less active counterparts (URIZAR and TORUN, unpublished).

It has not been shown whether physical activity has similar effects on the growth of children with mild and moderate dietary energy deficiency, but there are no reasons to believe that they would differ in this respect from the more severly malnourished children. As to the question of "How important is big?", we can answer that larger muscle (protein) and energy (fat) reserves might give poor, underprivileged children better protection against a recurrence of protein-energy malnutrition. Furthermore, as discussed below, small body size can limit maximal work output.

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