(introductory text...)

S. GRANTHAM-McGREGOR J.M. MEEKS GARDNER, S. WALKER and C. POWELL *

* Tropical Metabolism Research Unit, University of West Indies, Mona, St. Andrews, Jamaica.

Abstract

We examine the evidence that, in undernourished children, low levels of exploration and activity lead to poor development. In one study, children in the acute stage of severe undernutrition had reduced activity and exploration levels which readily improved with nutritional rehabilitation. Their developmental levels (i.e., developmental quotients = DQs) were low and remained so for several years. No association was found between activity and exploration levels and DQs.

Mildly to moderately undernourished children generally have low DQs. In both severely and moderately undernourished children, DQs and school achievement levels are more often associated with height-for-age than weight-for-height.

In two studies in clinical settings, when energy intake was reduced, children's activity levels or energy expenditure were also reduced. There is only limited evidence of reduced activity and exploration from studies of young undernourished children in their own homes. Undernourished school children were studied only once, and no evidence of reduced energy expenditure was found.

DQs and activity have not been examined together often. In one Asian study low exploration and DQs were found in undernourished children. In three studies of nutritional supplementation some evidence of increased activity and exploration and of improved development was found. However, there were problems in study design in two of them.

No evidence was found linking low activity to poor development in a causal relationship. We present preliminary findings from a Jamaican study of nutritional supplementation in 129 stunted children aged 9-24 months. They were compared with 32 non-stunted children from the same neighborhoods. The stunted group had lower scores on every subscale of the Griffiths Mental Development Scale. Using time-motion observation methods, they were also found to be less active than the non-stunted group. However, the stunted children had higher energy intakes per kilogram body weight. Activity levels were related to the children's locomotor quotients. When we controlled for locomotor quotients, no group differences remained.

1. Functional isolation

In 1970, LEVITSKY and BARNES observed that the effects of early undernutrition on the behavior of rats were similar to those of early environmental isolation. They later coined the term 'functional isolation' (LEVITSKY, 1979) and hypothesized that, because of lack of energy and poor muscular development, undernourished young rats failed to move around and explore their environment. In addition, their dams were less stimulating. The pups thus experienced a lack of stimulation similar to that of isolated rats. Any behavioral abnormality or developmental delay was attributed to this lack of exploration and reduced activity, rather than to alterations of the central nervous system. Since then, this has generally been accepted as at least one of the mechanisms linking poor development to undernutrition. In this paper, we will examine the evidence linking undernutrition, reduced activity and poor development in children.

2. Definition of malnutrition

The definition of malnutrition is confusing. In this paper, the term severe undernutrition will include clinically evident malnutrition, including marasmus, kwashiorkor, and marasmic-kwashiorkor (LANCET, 1970). Mild-to-moderate undernutrition will include any less severe forms. The diagnosis of undernutrition used to depend on deficits in weight compared with reference standards (e.g., LANCET, 1970). More recently it has been recommended that children be classified by height-for-age and weight-for-height (WATERLOW et al., 1977). Globally, low height-for-age (stunting) is much more prevalent than low weight-for-height (wasting) (KELLER, 1988). We will also briefly consider in this paper any association between development and stunting and wasting. First severe undernutrition, then mild-to-moderate undernutrition will be considered.

3.1. Developmental levels in the acute stage

It is well established that severely undernourished children have very low developmental levels during the acute episode. They usually show some improvement with nutritional rehabilitation, but remain at low levels for some time GRANTHAM-McGREGOR 1984). In a Jamaican study we compared 18 severely undernourished children (marasmus, kwashiorkor and marasmic-kwashiorkor) with 20 adequately nourished children of the same age who had been admitted to the same hospital with diseases other than undernutrition.

All children had developmental assessments on the Griffiths Test on admission to hospital and one month after returning home. On admission, both groups had low developmental quotients (DQs), but those of the severely undernourished group were markedly lower than those of the controls GRANTHAM-McGREGOR STEWART and DESAI, 1978). Both groups showed a similar improvement in hospital. There was no hint of the severely undernourished children improving more, inspite of rapid gains in weight-for-height.

3.2. Behavior

There is less information on the children's activity levels and behavior. Since WILLIAMS (1933) described kwashiorkor, it has been generally accepted that these children are extremely inactive, apathetic, irritable and explore their surroundings little (TROWELL, DAVIES and DEAN, 1982). However, reports reflect clinical impressions rather than systematic observations, and the possible effects of being admitted to hospital on a young child's behavior (BOWLBY, 1975) have been ignored.

In the Jamaican study, described above, we made systematic observations of 18 severly undernourished children on admission to hospital, and throughout nutritional rehabilitation (STEWART, SCHOFIELD and GRANTHAM-McGREGOR unpublished paper, 23rd meeting CCMRC, Barbados 1978), and we compared them with those of 20 adequately nourished children serving as controls.

Children were observed alone, in their cribs, for three 10-minute periods spread over 90 minutes. In these 10-minute periods, behavior was observed and recorded for 5 in every 30 seconds. It was noted if the child moved his limbs, head and body, and if it changed position. An activity rating was then devised from these records. In addition, it was recorded if the child was unhappy, apathetic, or alert in each recording period. It was also noted if he was exploring the contents of the crib with one or two hands, and an exploration rating was devised. On the same day, the children's behavior, when presented with a standard set of seven toys, was recorded. The time schedule for these observations was 3 seconds of observations in every 30 seconds for three 5-minute periods. In each recording period it was noted whether the child was exploring with one or two hands, and this was converted into a toy exploration rating. Also the actions performed on the toys were categorized into 13 different categories such as hold, push, bang, throw etc.

In the unstructured situation, we found that the severely undernourished children were markedly less active (p < .001) than the controls on admission to hospital. One week later, and until they left hospital (the severely undernourished were hospitalized for 16 to 111 days, median 42.5 days; the controls for 4 to 46 days, median 13.5 days), there was no longer any significant difference between the two groups (Figure 1). Initially, the malnourished children were apathetic in significantly more recording periods (median 19, range 0-60) than the controls (median 4, range 0-33, p < .05). This difference also disappeared in one week. A somewhat unexpected finding was that the controls were distressed and unhappy in more periods (median 19, range 0-60) than the severely undernourished children (median 0, range 0-20, p < .001). This difference also disappeared one week later. There was no difference in the exploration rating between the groups in the unstructured situation. We attributed this to the extra distress of the control children, and to the fact that the hospital was lacking in toys and social stimulation (STEWART and GRANTHAM-McGREGOR 1979).

Figure 1a. The activity ratings of severely undernourished (n = 14) and adequately nourished children (n = 18) on admission to hospital, one week later and on discharge from hospital.

Figure 1b. The exploration ratings of severely undernourished (n = 14) and adequately nourished children (n = 18) on admission to hospital, one week later and on discharge from hospital.

When toys were presented, the controls explored much more than the severely undernourished group (p < .001). This difference took longer to disappear, it remained significant one week later, but by the time the children left hospital the groups were the same (Figure 1). There were also differences in the quality of exploration, in that the controls explored more toys with a greater variety of play actions. All differences had disappeared when the children left hospital, except that the controls were still playing with more toys. However, when the age and the developmental levels of the children were controlled for, the groups were no longer different.

3.3. Relationship between development, activity and exploration

Recently we reanalyzed the data to determine whether there was an association between initial behavior and DQs following recovery. We calculated simple correlations between DQ following recovery and the initial behaviors (Table 1). We considered the children's DQs after returning home more valid, and attributed the initial low values to the children's anxiety at being in hospital, fear of strangers and generally feeling unwell. There was a significant negative association between apathy and DQ in the control group, and the association approached significance (p < .1) in the severely undernourished group. There was no association between the amount of toy exploration, or the activity rating and DQ in the separate groups. When the groups were combined, all these associations were significant. In these deprived children, a decline in DQ with age is expected. Controlling for age did not change the pattern of associations. When DQ was predicted in a multiple regression analysis, with age, group, apathy, activity rating, and toy-exploration rating as independent variables, only age, group, and apathy entered the equation.

Table 1. Correlations between DQs one month after recovery and initial behavior

	Severely undernourished	Controls	Combined groups
	(n = 18)	(n = 20)	(n = 38)
Age	-.46 +	-.66 +	-.52 ++
Activity rating	.01	.23	.54 ++
Apathy	-.40	-.45 +	-.54 ++
Toy-exploration rating *	.22	.07	.44 ++

* undernourished group, n = 17.
⁺ p < .05
⁺⁺ p < .01

Within-group associations between activity, exploration and DQs may have failed to reach significance because the groups were small. Also the behavioral measures may not be sensitive to small differences in DQ. A further possibility is that current activity and quantity of exploration are not directly related to development but only to severe undernutrition. The findings established that severely undernourished children had low developmental levels and showed no sign of improvement relative to the controls during nutritional rehabilitation. In contrast, the behavioral abnormalities of apathy, reduced activity and exploration were transient and improved rapidly. It is not possible to say which nutrients were responsible for these changes. There may have been more subtle behavioral differences remaining after recovery that were not measured. Furthermore, the relationships between behavior and developmental level following the establishment of poor development may not be the same as those which preceded it. The relationship between apathy and poor development in both groups requires further investigation; apathy may be related to severity of systemic illness.

3.4. Relationship between development and anthropometry

In the above Jamaican investigation, a second group of severely undernourished children who participated in an intervention program were also studied. The data from both undernourished groups were combined. The relationship between initial nutritional status of the children and their DQs one month after leaving hospital was then examined GRANTHAM-McGREGOR 1982) (Table 2). When the age of the children and their participation in the intervention were controlled for, only height-for-age significantly predicted DQ levels. Weight-for-height and the presence of oedema did not.

Table 2. The relative effect of different nutritional indices on DQ in 38 severely undernourished children

Independent variables	Standardised regression coefficients
Intervention	.372 +
% expected height-for-age	486 +
% expected weight-for-height	.156
Oedema	.046

+ p < .01

In another Jamaican study (GRANTHAM-McGREGOR, POWELL and FLETCHER, 1989), we individually matched 29 children who had recently recovered from severe malnutrition (mixed cases of kwashiorkor, marasmus, marasmic-kwashiorkor) with 29 children of the same age (±3 months), height and social background. The matched group had not suffered from an episode of severe undernutrition. We carried out developmental assessments with the Griffiths Mental Development Scales. In addition, we tested 15 non-stunted children of the same age and similar but not identical social background (Table 3). The severely undernourished group had only slightly and non-significantly lower DQs than the matched group, and both groups were markedly lower than the non-stunted children. In these children, it would appear that an episode of severe undernutrition had only a small effect on development over and above that associated with stunting. It is difficult to explain why in Chile, in a larger sample of undernourished children, COLOMBO, DE ANDRACA and LOPEZ (1988) found no association with height-for-age.

Table 3. Scores, adjusted for age, on the Griffiths Mental Development Scales of the three groups

Scale	Severely		Stunted		Non-stunted undernourished
	(n = 29)		(n = 29)		(n = 15)
	Mean	SD	Mean	SD	Mean	SD
DQ ac	98	10	100	13	108	15
Hearing & speech	105	16	104	22	110	20
Hand & eye a	98	13	102	10	109	19
Performance ab	91	12	95	16	105	14

a severely undernourished and non-stunted p < .01.
^b stunted and non-stunted p < .01.
^c stunted and non-stunted p < .05.

3.5. Children after recovery from the acute episode

There have been many reviews of studies of mental development of older children who had suffered from severe undernutrition in early childhood (e.g., POLLITT and THOMSON, 1977; GALLER 1984; GRANTHAM-McGREGOR, 1989). The evidence is reasonably consistent that severely undernourished children persist in having low levels of IQ, if they return to poor environments. However, owing to the difficulty in separating the effects of undernutrition from those of poor environments a causal relationship cannot be inferred conclusively. Also there is some evidence that undernutrition interacts with the quality of the environment (POLLITT, 1988).

I am unaware of any study of activity levels of previously severely undernourished children. Several investigators have taken histories from mothers or teachers of the children's behavior. In Uganda (HOORWEG, 1976), previously severely undernourished children were more likely to rest more at home, and in Barbados (GALLER, 1984) they were more likely to be sleepy at school. To what extent these behaviors reflected current dietary intake and social background, or were attributable to the early episode of malnutrition is not clear.

3.6. Jamaican study

In the Jamaican study of behavior in severely undernourished children discussed above GRANTHAM-McGREGOR STEWART and DESAI, 1978), part of the undernourished group participated in a 3-year programme of psychosocial stimulation. Those who did not participate in this intervention remained with very low DQ levels, whereas the stimulated group showed a marked improvement (GRANTHAM-McGREGOR, SCHOFIELD and POWELL, 1987; Figure 2). At the end of the intervention, the children's behavior was observed in the presence of their mothers or guardians in a standardized task with a pegboard GRANTHAM-McGREGOR SCHOFIELD and HAGGARD, 1989). The non-stimulated, severely undernourished group played less with the toy and stayed closer to their mothers than the controls. In contrast, the stimulated severely undernourished group behaved the same as the controls, playing for as long and not staying close to their mother.

Figure 2. The DQs of three groups of children on the Griffiths Test from admission to hospital to 48 months after returning home, and their IQs on the Stanford Binet at 60 and 72 months, expressed in standard scores.

The important findings were that, several years after recovery, severely undernourished children had abnormal behavior which could have contributed to their continued poor development. Further, the low level of exploration was probably improved by stimulation without nutritional supplementation. Supplementation was only given while the children were in hospital. Both the non-stimulated and stimulated severely undernourished groups were similar in nutritional status. They remained with lower heights-forage and head-circumferences-for-age than the controls, but caught up to them in weight-for-height.

The severely undernourished children who received increased stimulation caught up to the adequately nourished group in all subscales of the Griffiths test except for the locomotor one. We hypothesized that the lack of locomotor improvement may have been due to their continuing poor nutritional status.

3.7. Conclusions

The following conclusions concerning severely undernourished children can be reached:

1. They have low levels of development and show a marked reduction in activity and exploration in the acute stage.

2. The behavioral differences in activity and exploration disappear rapidly with nutritional rehabilitation whereas the developmental deficit does not.

3. Developmental levels are more closely related to height-forage than to weight-for-height or oedema.

4. Several years following recovery, some behavioral deficits can be observed. They are probably due to poor stimulation or continuing poor nutrition, however, they may be persistent effects of the acute episode, which were not apparent immediately after recovery.

4.1. Development and anthropometry

In five studies of the determinants of school achievement or IQ, when social background factors were controlled, height-for-age was a significant predictor (in the Philippines (FLORENCIO, 1988), in Guatemala (JOHNSON et al., 1987), in Nepal (MOOCK and LESLIE, 1986), in India (AGARWAL et al., 1987), and in China (JAMISON, 1977)). In contrast, weight-for-height was not, except in one other study in the Philippines (POPKIN and LIM-YBANEZ, 1982). Stunting was also found to be associated with poor neurosensory integration (CRAVIOTO, DELICARDIE and BIRCH, 1966) in school-aged Mexican children.

An association between height-for-age and development has also been shown in several studies of young children in communities where undernutrition is endemic (e.g., in Guatemala (LASKY et al., 1981), in Chile (MONCKEBERG, 1972), and in Jamaica (POWELL and GRANTHAM-McGREGOR 1985)). In the Guatemalan study, weight controlling for height was also associated with development. An exception to these findings is a Chilean study by COLOMBO and colleagues (1988), in which no association was found between height-for-age and IQ, in stunted or previously severely undernourished school children.

Associations with poor development are more frequently found with stunting than with wasting. It is possible that wasting represents shorter periods of undernutrition than stunting; alternately stunting may have a different nutrition-related aetiology from wasting (GOLDEN, 1988). A further possible explanation is that stunting is more closely associated with poverty and sociocultural deprivations which also affect development.

4.2. Development and nutritional supplementation

Stunting is associated with many sociocultural disadvantages (MARTORELL, MENDOZA and CASTILLO, 1988), which may themselves affect children's development. Probably, the best way of determining whether there is a causal link between undernutrition and poor development is from studies of nutritional supplementation. These have been extensively reviewed elsewhere (GRANTHAM-McGREGOR, 1987). In general, where supplement was given to undernourished populations from pregnancy and throughout early childhood, a concurrent improvement in development and cognitive functions could be observed. There are, however, many problems which make it difficult to interpret these findings. There is limited evidence to indicate a benefit persisting after supplementation has stopped.

It also remains uncertain whether supplementation given to children who are already undernourished has a benefit.

4.3. Activity and exploration

In Guatemala, the effect of reducing energy intakes on activity, was observed in two studies in a clinical setting. Small groups of children who had recently recovered from severe undernutrition, were studied. Reduced energy expenditure was found in one study (TORUN and VITERI, 1981) and reduced activity levels in the other VITERI and TORUN, 1981). However, this short-term change in both intakes and activity may not represent the habitual situation in free-living children.

In a few studies, activity levels have been observed in free-living children using time-motion methods. In Uganda (RUTISHAUSER and WHITEHEAD, 1972), local children aged 18 months to 3 years, who were on low dietary intakes, were found to be less active than adequately nourished expatriate children. However, the control group was small, and there were cultural and class differences which may account for the activity difference. In Guatemala (TORUN, 1984), 3-year-old children with low weights-for-height were found to be less active than those with higher weights-for-height. However, no details of this study were reported.

In The Gambia, the doubly-labelled water technique was used to determine the energy expenditure of free-living children aged 2 to 24 months (VASQUEZ-VELASQUEZ, 1988). They were found to expend less energy than the FAO/WHO/UNU recommended dietary intake (WHO, 1985). However, it has been suggested that the values recommended by FAO may be too high (PRENTICE et al., 1988).

SPURR and REINA (1988) studied 242 six- to 16-year-old Colombian children. Approximately half the children were undernourished. They measured daily energy expenditure with heart rate monitors as well as basal and resting metabolic rates. They found no evidence of undernourished children expending less energy in activity. In none of the above studies were measures of the children's development or behavior reported.

4.4. Studies with development and behavioral measures

In only few studies have both activity and development been measured. In two Asian studies, GRAVES (1976, 1978) compared the behavior of undernourished children (weight-for-age between 60-65% of standard) with that of adequately nourished ones. The children were aged 7 to 18 months and were observed in a standard setting with their mothers in a free-play situation. They also had developmental assessments on the Gesell Schedules. Unfortunately, locomotor activity was not measured.

In both studies, undernourished children stayed longer on their mothers laps. In one study, they manipulated the toys less and for a shorter period of time (GRAVES, 1978). In this study, the undernourished children's DQs were markedly lower than those of the controls. However, the mothers' behavior was similar in the two groups.

In the other study (GRAVES, 1976), there was no difference between the groups in the amount of toy manipulation, although the undernourished children threw and banged them less. There were also no significant differences in the children's developmental levels. There were, however, differences in the mothers' behavior. In neither study did Graves look for within-group associations between DQ and exploration. However the study in which large DQ differences were found was the one in which the amount of exploration was also less.

4.5. Nutritional supplementation and behavior

4.5.1. Mexico

A Mexican study of nutritional supplementation (CHAVEZ and MARTINEZ, 1982) is probably the most critical one for the present considerations. The study was prospective, began before the birth of the child, and longitudinal measures were taken of both activity and development throughout the first 2 years of life.

A cohort of village children were studied in the first year, and in the following year a second cohort were given nutritional supplementation and studied in a similar way. The mothers were supplemented in pregnancy and their children were supplemented throughout early childhood. Time-motion techniques were used, in which foot contacts with the supporting surface were counted to provide an activity rating. The supplemented children showed a higher level of activity from 8 months of age. Their activity increased steadily until they were six times more active than the non-supplemented group by 24 months. The supplemented children had higher DQs on the Gesell Schedules throughout the two years.

This study has frequently been cited as evidence for reduced activity being the mechanism linking undernutrition to poor development. In Figure 3, the activity data have been plotted on the same graph as the Gesell subscale scores of the children. It can be clearly seen that, far from the increased activity leading to improved development, there is little association between the two. The supplemented children's development was better from birth. There were some fluctuations, but the difference showed no sign of increasing. The timing suggests that, if there is a relationship, improved development leads to greater activity. In addition, there are problems with attributing the increased activity to the supplementation alone. The groups were observed a year apart, and there was no control for the increased attention received by the supplemented children.

Figure 3a. Activity ratings and scores on the Gesell subscales in two groups of children (CHAVEZ and MARTINEZ, 1982). Socio-personal D.Q.

Figure 3b. Activity ratings and scores on the Gesell subscales in two groups of children (CHAVEZ and MARTINEZ, 1982). Motor D.Q.

Figure 3c. Activity ratings and scores on the Gesell subscales in two groups of children (CHAVEZ and MARTINEZ, 1982). Language D.Q.

Figure 3d. Activity ratings and scores on the Gesell subscales in two groups of children (CHAVEZ and MARTINEZ, 1982). Adaptive beh. D.Q.

4.5.2. Colombia

In a nutritional supplementation study in Bogota (SUPER et al., 1981), mothers were supplemented in pregnancy and their children from birth for three years. Observations were carried out when the children were 4 and 8 months of age. In a complex analysis, the results were presented in summary scales. At 4 months, the supplemented children had higher scores on the 'activity scales than the non-supplemented groups. This included 'gross body movements' and 'quiet play' as well as other variables. Children who received both supplementation and stimulation were especially active. There was no effect of supplementation at 8 months of age.

4.5.3. Guatemala

A large supplementation study was conducted in four villages in Guatemala. Pregnant women and children under 7 years were nutritionally supplemented on a self-selection basis. The children's behavior in several games was observed when they were 6 to 8 years old (BARRETT and RADKE-YARROW, 1985). The children who had received the most supplement in the first 4 years of life and when their mothers were pregnant, were compared with those who had received less. The high-supplement group was judged to be more active and exploring than the low-supplement group. However, it is not clear whether some of the supplemented children were still being supplemented. Also, self-selection could be a severe confounder in this study.

4.6. Summary

The main findings from the review of children with mild-to-moderate undernutrition are:

1. They have low levels of development and school achievement, which are more often related to their height-for-age than their weight-for-height.

2. In a clinical setting, there is evidence from two studies that reduced energy intake results in reduced activity.

3. In free-living children, there is limited evidence of reduced activity in preschool children. Studies have had inappropriate controls or insufficient details have been published to evaluate. In the only study of school children, no reduction of activity was found.

4. Reduced exploration has been found in undernourished children.

5. In three studies of nutritional supplementation, increased activity and exploration have been found. However, in two of them increased stimulation or better home backgrounds could be confounding variables.

6. There is no evidence to support the hypothesis that reduced activity levels lead to poor mental development.

(introductory text...)

At present, we are conducting a study of stunted children. The main aim is to determine the effects of nutritional supplementation, psychosocial stimulation or both, on growth, development and activity levels. We are also comparing the stunted children with non-stunted children. A house-to-house survey of poor Kingston neighborhoods was carried out, and all children between 9 and 24 months of age had their lengths and weights measured. All those with lengths below -2SD and weights-for-heights below the median of the NCHS standards (HAMILL et al., 1979) were identified (n = 129). The children were randomly assigned to four groups: a stimulated group, a group which received nutritional supplementation, a group which received both treatments, and a control group. Each child of the control group was matched with a non-stunted child (heights above -1SD NCHS, n = 32) who was of similar age and lived nearest. On enrollment, many baseline measurements were taken, including anthropometry, developmental assessments, dietary intakes, social background, index of stimulation in the home, activity levels, and observations of mother and child. We are still analysing the baseline data, some of which we will report here.

5.1. Developmental levels

On enrollment, all children were given developmental assessments with the Griffiths Test. The stunted groups combined had significantly lower DQs, and their scores were lower on each subscale (Table 4). Their mothers were given the Bettye Caldwell Home Inventory (CALDWELL, 1967), modified for Jamaica, and their standard of housing was assessed. When we controlled for the stimulation in the home, mothers' IQ and height, standard of housing, sex, age and birthweight of the child, the DQs of the stunted and non-stunted groups were still significantly different.

Table 4. Developmental quotients and anthropometry on enrollment by group

	Stunted		Non-stunted
	n = 129		n = 32
	Mean	SD	Mean	SD
DQ	.2	9.0 ++	106.3	9.9
Locomotor	101.7	12.0 ++	113.9	12.1
Hearing & speech	96.3	12.9 ++	104.3	13.0
Hand & eye	103.7	11.4 +	109.0	13.6
Performance	90.8	11.7 +	98.0	13.2
Height-for-age °	-3.0	0.7 ++	0.1	0.6
Weight-for-height °	-1.0	0.7 ++	0.0	0.8

+ p < .05
⁺⁺ p < .01
° z-scores of the NCHS.

5.2. Activity levels

The activity levels of a subsample of the children were observed. Seventy-eight of the stunted and 26 of the non-stunted children, all between 12 and 24 months of age, were studied. Time-motion methods, similar to those of TORUN (1984), were used. In this method, all activities likely to occur are listed, and a check is made every 10 minutes to indicate which ones occurred. The assumption is then made that equal time is spent in each activity which occurs in the period. Torun pointed out that this tends to increase the time apparently spent in the more vigorous activities. We also demonstrated this in the pilot phase. Therefore, we changed the recording interval to one minute, as this more closely approximates the actual timing.

The proportion of time spent in each activity was calculated for the whole observation period. Energy costs of the activities were then taken from values reported by TORUN and VITERI (1989) which were expressed as multiples of BMR. The data were expressed as the proportion of time spent in vigorous, moderate and light or sedentary activities, according to their estimated energy costs. In addition, an activity rating was calculated by multiplying the percent of time spent in each activity by its estimated energy cost and then summing the products. In the pilot phase, 10 children were observed for 3 days. The activity ratings on the 3 days were highly correlated (r = 0.81 to 0.96) and the mean activity ratings were not significantly different on the different days. The children in the main study were observed for 4 waking hours, from 9.30 a.m., for 2 weekdays, never more than 2 weeks apart. Further details of the method and interobserver reliabilities have been reported (MEEKS GARDNER et al., 1990). We also recorded whether certain other activities occurred in the child's environment. Examples of these are whether the child was in a crib or playpen or being held, and whether anyone was talking to or playing with him.

The stunted children spent more time in light activities (p < .001) and less time in moderate (p < .01) and vigorous activities (p < .01) than the non-stunted children (Table 5). The activity rating was significantly lower in the stunted group (mean 1.4, SD .1, p < .01) than in the non-stunted group (mean 1.5, SD .1), and the difference was not due to one group being carried or restrained more than the other. However, in terms of energy cost, the difference was small.

Table 5. Percentage of time spent in activity categories and the activity rating by group

	Stunted		Non-stunted
	n = 79		n = 26
Activity category	Mean	SD	Mean	SD
Light	78	9 ++	73	7
Moderate	21	8 +	25	7
Vigorous	1	2 +	2	2
Activity rating	1.4	0.1 +	1.5	0.1

+ p < .01
⁺⁺ p < .001

In the pilot phase, we showed that observing for 4 waking hours gave very similar results to observing for all the waking time from 9.30 a.m. to 5.30 p.m. It is reasonable to assume that these data represent the activity levels of the children for at least this period of time. The amount of time the children slept, while the observers were present, was very similar in the two groups. Further, the mothers were asked how long their child slept the previous day, and again both groups reported very similar amounts (stunted mean 11.9, SD 1.3; non stunted 11.8, SD 1.4). The activity level increased significantly with age (r = .59 p < .001). It was not related to weight-for-height, sex or dietary intake data. The aetiology of the reduced activity in the stunted group was not therefore clearly related to reduced energy availability.

5.3. Relationship between activity and development

The relationship between the children's activity ratings and development was examined. Separate multiple regression analyses of the activity rating were calculated, using in turn DQs and each subscale quotient as independent variables. In each regression, age was entered first, then the developmental measure followed by group (stunted/non-stunted). The proportions of variance in activity ratings explained by the quotients are shown in Table 6.

Table 6. Percentage of variance in activity ratings explained by age, developmental and subscale quotients, and group

	Independent variables
Quotient used	Age	Quotient	Group
DQ	34.7 ++	6.4 +	1.3
Locomotor	34.7 ++	14.0 ++	0.2
Hearing & speech	34.7 ++	0.6	4.7 ++
Hand & eye	34.7 ++	1.0	4.6 ++
Performance	34.7 ++	2.2	3.5 +

+ p < .05
⁺⁺ p < .01

Once age was controlled for, DQ explained a significant proportion of variance (6.4%). The only subscale to explain a significant proportion was locomotor, which explained a larger proportion (14%) than DQ. It would appear that the relationship between development and activity is mostly attributable to locomotor ability. Once age and either DQ or the locomotor quotient were controlled for, there was no difference between the groups in activity.

We cannot determine from these cross-sectional data whether locomotor ability predicts activity or vice versa. However, it would seem likely that locomotor ability in this age range is a potent determinant of activity level. The activity observations were repeated six months later, and when these data will be fully analyzed the relationship should be clearer.

5.4. Dietary intakes

Two 24-hour dietary recalls were obtained from the guardians of the children (WALKER, POWELL and GRANTHAM-McGREGOR 1990). The recalls were taken on weekdays, when the children were well. The total energy and protein intakes were similar in both groups. However, when they were expressed per kilogram body weight, the stunted group actually had significantly higher intakes both in energy and protein than the non-stunted group (Table 7). This finding requires further investigation.

Table 7. Energy and protein intakes upon enrollment

		Stunted		Non-stunted
		(n = 129)		(n = 62)
		Mean	SD	Mean	SD
Energy	(kcal/d)	953	448	973	358
	(kcal/kg/d)	113	51 ++	85	31
Protein	(g/d)	26.6	17.8	29.0	14.1
	(g/kg/d)	3.1	1.9 +	2.5	1.2

+ p < 0.005
⁺⁺ p < 0.0001

A higher rate of morbidity in the stunted group may explain some of this difference, but is unlikely to explain it all.

5.5. Conclusions

It is unwise to draw firm conclusions before all the analyses are completed. The stunted children had markedly lower DQs than the non-stunted group, even at this young age. They were also less active, but did not have lower energy intakes per kilogram body weight. Therefore the reduced activity was not clearly related to reduced available energy.

The children's development was related to their activity rating mostly through their locomotor development. When their age and locomotor quotient were controlled for, the groups did not differ in activity ratings.

Acknowledgements

The Jamaican studies referred to in this paper were funded by the Ford Foundation U.S.A., Population Council and United Nations University. We thank S. Chang for assistance in the preparation of this paper.

References

AGARWAL, D.K., UPADHYAY, S.K., TRIPATHI, A.M., AGARWAL, K.N.: Nutritional status, physical work capacity and mental function in school children. Nutritional Foundation of India. Scientific report No. 6 (1987).

BARRETT, D.E., RADKE-YARROW, M.: Effects of nutritional supplementation on children's responses to novel, frustrating and competitive situations. Am. J. Clin. Nutr., 42, 102-120 (1985).

BOWLBY, J.: Attachment and Loss Vol. 2: Separation, Anxiety and Anger. Penguin Books, London, 1975.

CALDWELL, B.M.: Descriptive evaluation of child development and of developmental settings. Pediatrics, 40, 46-50 (1967).

CHAVEZ, A., MARTINEZ, C.: Growing up in a Developing Community. INCAP, Guatemala City, 1982.

COLOMBO, M., DE ANDRACA, I., LOPEZ, I.: Mental development and stunting. In: Linear Growth Retardation in Less Developed Countries, pp. 201-214, J.C. WATERLOW (Ed.). Nestle Nutrition Workshop 14. Raven Press, New York, NY, 1988.

CRAVIOTO, J., DELICARDIE, E., BIRCH, H.: Nutrition, growth and neurointegrative development: an experimental and ecologic study. Pediatrics (Suppl.), 38, No. 2 (1966).

FLORENCIO, C.A.: Nutrition, health and other determinants of academic achievement and school related behavior of grade one to grade six pupils. University of the Philippines, Quezon City, Philippines, 1988.

GALLER, J.: The behavioral consequences of malnutrition in early life. In: Nutrition and Behavior, pp. 63-118, J. GALLER (Ed.). Plenum Press, New York and London, 1984.

GOLDEN, M.H.N.: The role of individual nutrient deficiencies in growth retardation of children as exemplified by zinc and protein. In: Linear Growth Retardation in Less Developed Countries, pp. 143-164, J.C. WATERLOW (Ed.). Nestle Nutrition Workshop 14. Raven Press, New York, NY, 1988.

GRANTHAM-McGREGOR S.M.: Field studies in early nutrition and later achievement. In: Early Nutrition and Later Achievement, pp. 124-128, J. DOBBING (Ed.). Academic Press, London, 1987.

GRANTHAM-McGREGOR S.M.: The relationship between developmental level and different types of malnutrition in children. Hum. Nutr. Clin. Nutr., 36C, 319-320 (1982).

GRANTHAM-McGREGOR S.M.: Rehabilitation after clinical malnutrition. In: Malnutrition and Behavior: Critical Assessment of Key Issues, pp. 531-554, J. BROZEK, B. SCHÜRCH (Eds.). Nestle Foundation, Lausanne, Switzerland, 1984.

GRANTHAM-McGREGOR S.M.: The effects of undernutrition on mental development. In: Handbook of the Psychophysiology of Human Eating, pp. 321340, R. SHEPHERD (Ed.). Wiley Psychophysiology Series. J. Wiley and Sons Inc., Chichester, England, 1989.

GRANTHAM-McGREGOR S.M., POWELL, C., FLETCHER, P.: Severe malnutrition, stunting and mental development in young children. Eur. J. Clin. Nutr., 43, 403-410 (1989).

GRANTHAM-McGREGOR S.M., SCHOFIELD, W., HAGGARD, D.: Maternal-child interaction in survivors of severe malnutrition who received psychosocial stimulation. Eur. J. Clin. Nutr., 43, 45-52 (1989).

GRANTHAM-McGREGOR S.M., SCHOFIELD, W., POWELL, C.: Development of severely malnourished children who received psychosocial stimulation: six year follow-up. Pediatrics, 79, 247-254 (1987).

GRANTHAM-McGREGOR S.M., STEWART, M.E., DESAI, P.: A new look at the assessment of mental development in young children recovering from severe malnutrition. Dev. Med. Child Neurol., 20, 773-778 (1978).

GRAVES, P.L.: Nutrition, infant behaviour, and maternal characteristics; a pilot study in West Bengal, India. Am. J. Clin. Nutr., 29, 305-319 (1976).

GRAVES, P.L.: Nutrition and infant behaviour: a replication study in the Katmandu Valley, Nepal. Am. J. Clin. Nutr., 31, 541-551 (1978).

HAMILL, P.V.V., DRIZD, T.A., JOHNSON, C.L., REED, R.B., ROCHE. A.F., MOORE, W.M.: Physical growth: National Center for Health Statistics Percentiles. Am. J. Clin. Nutr., 32, 607-629 (1979).

HOORWEG, J.: Protein-energy Malnutrition and Intellectual Abilities. Mouton, S. Gravenhage, Paris, 1976.

JAMISON, D.T.: Child malnutrition and school performance in China. J. Dev. Econ. 20, 299-309 (1977).

JOHNSON, F.E., LOW, S,M., DE BAESSA, Y., MACVEAN, R.B.: Interaction of nutritional and socioeconomic status as determinants of cognitive development in disadvantaged urban Guatemalan children. Am. J. Physiol. Anthropol., 73, 501-506 (1987).

KELLER, W.: The epidemiology of stunting. In: Linear Growth Retardation in Less Developed Countries, pp. 17-40, J.C. WATERLOW (Ed.). Nestle Nutrition Workshop 14. Raven Press, New York, NY, 1988.

LANCET editorial. Classification of infantile malnutrition. Lancet, 2, 302 (1970).

LASKY, R.E., KLEIN, R.E., YARBROUGH, C., ENGLE, P.L., LECHTIG, A., MARTORELL, R.: The relationship between physical growth and infant behavioural development in rural Guatemala. Child Dev., 52, 220-226 (1981).

LEVITSKY, D.A.: Malnutrition and hunger to learn. In: Malnutrition, Environment and Behaviour, pp. 161-179, D.A. LEVITSKY (Ed.). Cornell University Press, Ithaca and London, 1979.

LEVITSKY, D.A., BARNES, R.H.: Malnutrition and animal behaviour. In: Nutrition, Development and Social Behaviour, pp. 3-16, D.J. KALLEN (Ed.). DHEW Publ. No. (NIH) 73-242, Washington, DC, 1970.

MARTORELL, R., MENDOZA, F., CASTILLO, R.: Poverty and stature in children. In: Linear Growth Retardation in Less Developed Countries, J.C. WATERLOW (Ed.). Nestle Nutrition Workshop Series, Vol. 14. Raven Press, New York, NY, 1988.

MEEKS GARDNER, J.M., GRANTHAM-McGREGOR S.M., CHANG, S., POWELL, C.A.: Dietary intakes and observed activity of stunted and non-stunted children in Kingston, Jamaica. Part II: Observed activity. Eur. J. Clin. Nutr., in press.

MONCKEBERG, F.: Malnutrition and mental capacity. In: Nutrition, the Nervous System and Behaviour, pp. 48-54. PAHO, Scientific Publication, No. 251, Washington, DC, 1972.

MOOCK, P.R., LESLIE, J.: Childhood malnutrition and schooling in the Teri region of Nepal. J. Dev. Econ, 20, 33-52 (1986).

POLLITT, E.: A critical view of three decades of research on the effects of chronic energy malnutrition on behavioral development. In: Chronic Energy Deficiency: Consequences and Related Issues, B. SCHÜRCH, N.S. SCRIMSHAW (Eds.), pp. 77-94. IDECG, c/o Nestle Foundation, Lausanne, Switzerland, 1988.

POLLITT, E., THOMSON, C.: Protein-calorie malnutrition and behaviour. A view from psychology. In: Nutrition and the Brain, Vol. 12, R.J. WURTMANN, pp. 261-306, J.J. WURTMAN (Eds.). Raven Press, New York, NY, 1977.

POPKIN, B.M., LIM-YBANEZ, M.: Nutrition and school achievement. Soc. Sci. Med., 16, 53-61 (1982).

POWELL, C.A., GRANTHAM-McGREGOR, S.M.: The ecology of nutritional status and development in young children in Kingston, Jamaica. Am. J. Clin. Nutr., 41, 1322-1331 (1985).

PRENTICE, A.M., LUCAS, A., VASQUEZ-VELASQUEZ, L., DAVIES, P.S.W., WHITEHEAD, R.G.: Are current dietary guidelines for young children a prescription for overfeeding? Lancet, ii, 1066-1069 (1988).

RUTISHAUSER, H.E., WHITEHEAD, R.G.: Energy intake and expenditure in 1-3 year old Ugandan children living in a rural environment. Br. J. Nutr., 28, 145-152 (1972).

SPURR, G.B., REINA, J.C.: Patterns of daily energy expenditure in normal and marginally undernourished school-aged Colombian children. Eur. J. Clin. Nutr., 42, 819-834 (1988).

STEWART, M.E., GRANTHAM-McGREGOR, S.M.: The experiences of young children in a Kingston hospital, Jamaica. W.I. Med. J., 28, 30-35 (1979).

SUPER, C.M., CLEMENT, J., VUORI, L., CHRISTIANSEN, N., MORA, J.O., HERRERA, M.G.: Infant and caretaker behavior as mediators of nutritional and social intervention in the barrios of Bogota. In: Culture and Early Intervention, pp. 171-187, T. FIELD, A. SOSTEK, P. VIETZE, P. LEIDERMAN (Eds.). Erlbaum, Hillsdale, NJ, 1981.

TORUN, B.: Physiological measurements of physical activity among children under free-living conditions. In: Energy Intake and Activity, E. POLLITT, P. AMANTE (Eds.), pp. 159-184. Alan R. Liss Inc., New York, 1984.

TORUN, B., VITERI, F.E.: Energy requirements of pre-school children and the effects of varying energy intakes on protein metabolism. In: Protein-Energy Requirements of Developing Countries: Evaluation of New Data, pp. 229-241, B. TORUN, V.R. YOUNG, W.M. RAND (Eds.). United Nations University, Tokyo, 1981.

TORUN, B., VITERI, F.E.: Nutrition and function, with emphasis on physical activity. In: Nutritional Problems of Children in the Developing World, M. KRETCHMER, F. E. VITERI, F. FALKNER (Eds.), 1989.

TROWELL, H.C., DAVIES, J.N.P., DEAN, R.F.A.: A Nutrition Foundation's Reprint of Kwashiorkor. Academic Press, New York, NY, 1982.

VASQUEZ-VELASQUEZ, L.: Energy expenditure and physical activity of malnourished Gambian infants. Proc. Nutr. Soc., 47, 233-239 (1988).

VITERI, F.E., TORUN, B.: Nutrition, physical activity and growth. In: The Biology of Normal Human Growth, pp. 265-273, M. RITZEN, A. APERIA, K. HALL, A. LARSON, A. ZETTERBERG, R. ZETTERSTRÖM (Eds.). Raven Press, New York, NY, 1981.

WALKER, S.P., POWELL, C.A., GRANTHAM-McGREGOR S.M.: Dietary intakes and observed activity of stunted and non-stunted children in Kingston, Jamaica. Part I. Dietary intakes. Eur. J. Clin. Nutr., in press.

WATERLOW, J.C., BUZINA, R., KELLER, W., LANE, J.N., NICHAMAN, M.Z., TANNER, J.M.: The presentation and use of height and weight data for comparing the nutritional status of children under the age of 10 years. Bull. WHO, 55, 489-498 (1977).

WHO: Energy and Protein Requirements. Report of a Joint FAO/WHO/UNU Expert Consultation. Technical Report Series 724. WHO, Geneva, 1985.

WILLIAMS, C.: A nutritional disease of childhood associated with a maize diet. Arch. Dis. Child, 8, 423-433 (1933).

Discussion (summarized by B. Torun)

Several questions were asked to clarify further details of the Jamaican study. McGregor's answers and clarifications were that (1) all the children in the study were already walking; (2) no days when they were ill were included in the observations; (3) there were no important differences in the behaviors of the mothers (at least among those that had been assessed); (4) the four hours of observation were selected at random; (5) the behavior of the mothers was spontaneous, i.e., mothers received no instructions on what to do or not to do.

According to Pollitt, at least three aspects must be considered when interpreting McGregor's results: (1) developmental assessments at this early age are not conceptually significant, unless they can be related to behavior at a later age (e.g., about two years later); (2) studies done in children suffering from hypopituitarism showed that although the development of these children was delayed, this could largely be explained by the mothers' attitude and behavior; (3) during the first three years of life, one can find associations between developmental assessments and growth indicators. Super added that there may be age-related differences in the accomodation response of children to low energy intake, as discussed by Torun in his presentation on short- and long-term effects of low energy intake on activity.

McGregor added that data on the dietary intake of the children in her study indicated that, per kg body weight, stunted children had higher intakes than non-stunted ones. When expressed in absolute terms, i.e., as kcal or g protein per day, intakes were similar in both groups. Since the stunted children were smaller and ligher, their intake per kg body weight was greater.

Shetty also found that energy intake per kg weight was greater in undernourished than in well-nourished Indian adults. Allen reported analogous findings among undernourished children in Mexico. Others commented that these findings are not universally consistent, as in several other studies undernourished children had lower intakes in absolute and relative terms.

Jackson commented that there may be other specific nutrient deficits that lead to 'wastage' of dietary energy. Torun added that studies on the dietary management of diarrhea in Guatemala showed that children gained more weight when vegetable-based diets were supplemented with Na, K and micronutrients.