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Abstract
1. Functional isolation
2. Definition of malnutrition
3. Severe undernutrition3.1. Developmental levels in the acute stage
3.2. Behavior
3.3. Relationship between development, activity and exploration
3.4. Relationship between development and anthropometry
3.5. Children after recovery from the acute episode
3.6. Jamaican study
3.7. Conclusions4. Mild-to-moderate undernutrition
4.1. Development and anthropometry
4.2. Development and nutritional supplementation
4.3. Activity and exploration
4.4. Studies with development and behavioral measures
4.5. Nutritional supplementation and behavior
4.6. Summary5.1. Developmental levels
5.2. Activity levels
5.3. Relationship between activity and development
5.4. Dietary intakes
5.5. ConclusionsAcknowledgements
References
Discussion (summarized by B. Torun)
S. GRANTHAM-McGREGOR J.M. MEEKS GARDNER, S. WALKER and C. POWELL *
* Tropical Metabolism Research Unit,
University of West Indies, Mona, St. Andrews, Jamaica.
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.
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.
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
3.2. Behavior
3.3. Relationship between development, activity and exploration
3.4. Relationship between development and anthropometry
3.5. Children after recovery from the acute episode
3.6. Jamaican study
3.7. Conclusions
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.
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).
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.
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.
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 |
severely undernourished and non-stunted p < .01.a
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.
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.
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.
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
4.2. Development and nutritional supplementation
4.3. Activity and exploration
4.4. Studies with development and behavioral measures
4.5. Nutritional supplementation and behavior
4.6. Summary
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.
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.
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.
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.