Donald T Simeon & Sally M Grantham-McGregor. Cambridge World History of Food. Editor: Kenneth F Kiple & Kriemhild Conee Ornelas, Volume 2, Cambridge University Press, 2000.
Most research on nutrition and human mental development has focused on protein-energy malnutrition (PEM), which consists of deficits in energy and protein as well as other nutrients (Golden 1988). But there is also an extensive literature on the importance to mental development of trace elements and vita-mins, as well as the impact of short-term food deprivation. Thus, although the bulk of this essay focuses on PEM and mental development, we begin with an examination of these other areas of concern.
Vitamins and Trace Elements
General Vitamin and Mineral Deficiencies
It is well understood that severe vitamin deficiencies may have drastic effects on mental development. Serious thiamine and niacin deficiencies, for example, as well as those of folic acid and vitamin B12, can cause neuropathy (Carney 1984). But milder, subclinical vitamin deficiencies are much more common, and thus their influence on mental development is presumably of much greater importance. Unfortunately, the extent to which multivitamin and mineral supplements inf luence intelligence in schoolchildren remains unknown, although this question has been the subject of at least five clinical trials (Schoenthaler 1991).
One study of 90 Welsh children using a multivitamin-mineral supplement over a nine-month period indicated that supplementation produced an increase in nonverbal IQs (Benton and Roberts 1988). A similar study of 410 children in the United States over 13 weeks also revealed an overall increase in nonverbal IQs (Schoenthaler 1991). However, in a Belgian study of 167 children who were supplemented for five months, only boys whose diets had previously been nutritionally deficient showed an increase in verbal IQs (Benton and Buts 1990). Other studies, one in London and the other in Scotland, reported no significant effects of supplementation (Naismith et al. 1988; Crombie et al. 1990).
Reasons for inconsistent findings may have to do with differences in the duration of the programs or may lie in the nature of the children’s normal diets. Because supplementation is most likely to benefit children whose diets are deficient in one or more of the chief nutrients, more consistent results might have been obtained if the subjects had been restricted to children with deficient diets. Another problem with these studies is that a variety of vita-mins and trace elements were administered in the supplements. Thus, it is not possible to single out those nutrients that may have played key roles in raising nonverbal IQs.
Among the trace elements there are two that have been the subject of much research and are known to have a substantial influence on mental development.
One is iodine, which is required for the production of thyroxine. Iodine deficiency during pregnancy can cause deficits in fetal brain maturation, resulting in cretinism. There are two types of cretinism, neurological and myxedematous; mental retardation is a symptom of both. Other symptoms of neurological cretinism include spastic diplegia and deaf-mutism, whereas dwarfism is symptomatic of myxedematous cretinism.
Cretinism, however, is not the only manifestation of iodine deficiency, and a number of others have been identified. These are referred to as iodine-deficiency disorders (IDD) (Hetzel 1983) and include goiter, neuromotor delays, deaf-mutism, and an increase in both pre- and postnatal mortality rates (Stanbury 1987).
Cretinism seems to be the extreme in a spectrum of cognitive and psychomotor deficits caused by iodine deficiency. Studies in Indonesia and Spain have indicated that village children living in iodine-deficient regions had poorer levels of mental and motor development than other village children who did not live in such areas (Bleichrodt et al. 1987). It may be that other disparities between the villages played a role in the differences. But, in a village in Ecuador, iodine supplementation of pregnant mothers reportedly led to improved motor development of the children, in comparison with children in a nonsupplemented village (Fierro-Benitez et al. 1986). Similar results were derived from a clinical trial conducted in Zaire (Thilly et al. 1980).
Yet in other studies, iodine supplementation seems to have been less effective. One of these, conducted in Peru, reported no effect on the development of the infants of mothers supplemented during pregnancy (Pretell et al. 1972). Two other studies involved schoolchildren. One, carried out in Bolivia, revealed no changes in school achievement and development despite iodine supplementation (Bautista et al. 1982), and a Spanish study discovered no effect on the mental or psychomotor development of supplemented children (Bleichrodt et al. 1989).
Clearly, more research of a conclusive nature is needed. There are some 800 million persons at risk of iodine deficiency in Asia, Africa, and Latin America; close to 200 million persons in the world suffer from goiter, and more than 3 million are cretins (Hetzel 1987). This is especially tragic because iodine deficiency is so easily prevented by the consumption of iodized salt or iodized oil, or by iodine injection.
Iron is the second of the trace minerals that play a decided role in mental development. Its deficiency is the main cause of anemia, an important nutritional problem in both developed and developing countries. Because anemia symptoms include listlessness and lassitude, iron deficiency can and does negatively affect the cognitive processes.
Early investigations indicated associations between iron-deficiency anemia and poor levels of cognition in children. However, there were problems in eliminating social factors that could also be causal (see, for example, Webb and Oski 1973). Subsequent studies on iron-deficient children suggest, among other things, that the adverse effects of iron deficiency on the cognitive processes are most apparent when the deficiency is severe enough to cause anemia.
Age has much to do with such findings, as does the duration of the periods of iron supplementation. For example, in five studies, supplementation was given for periods of less than two weeks, and developmental levels assessed on infant scales were used as outcome measures. No significant gains from supplementation were discovered in four of the studies, which were conducted in Guatemala (Lozoff et al. 1982), Costa Rica (Lozoff et al. 1987), Chile (Walter et al. 1989), and North America (Oski and Honig 1978). A fifth study, in Chile, did find an improvement in developmental levels, although the absence of a placebo group compromised the results (Walter, Kovalskys, and Stekel 1983).
In another group of studies, however, children under two years of age were supplemented for longer periods. Two such studies were preventive trials in which high-risk children were supplemented from the age of 2 to 3 months and then tested at 12 months. In Chile, such supplementation produced better development (Walter et al. 1989), and in Papua New Guinea, supplemented children had longer fixation times than the controls (Heywood et al. 1989). On the other hand, in the United Kingdom, a group that underwent two months of supplementation did not produce better development scores than a placebo group, although a greater number of treated children achieved normal rates of development (Aukett et al. 1986). In Costa Rica, after three months of supplementation, children who experienced complete recovery of their iron status clearly benefited from the supplements (Lozoff et al. 1987). However, a study in Chile found no effect after three months of supplementation (Walter et al. 1989).
It appears that, as a rule, the longer the duration of treatment, the more likely there will be benefits in developmental levels. It has been suggested that iron deficiency affects such development because it reduces a child’s span of attention (Pollitt et al. 1982). But children under two years of age are difficult to assess, and only one study thus far has attempted to look at the matter (Heywood et al. 1989).
Results seem to be more positive in children over two years of age. Indeed, 10 studies have reported improvement in mental functions after iron supplementation. Three of these were conducted in Indonesia, and improvements in both cognitive functions and school achievement levels were reported after two or three months’ treatment (Soemantri, Pollitt, and Kim 1985; Soemantri 1989; Soewondo, Husaini, and Pollitt 1989).
In India, two studies found improved cognitive functions after three months of supplementation (Seshadri and Gopaldas 1989); another, in Egypt, reported the same after four months of treatment (Pollitt et al. 1985). In India, two additional clinical trials showed improvements in IQ scores after three months of supplementation with both iron and folic acid (Seshadri and Gopaldas 1989). In the United States, the results of two studies, which were not true clinical trials, indicated that supplementation produced improvements in the cognitive functions of anemic children (Pollitt, Leibel, and Greenfield 1983a), and similar conclusions were reached in Guatemala (Pollitt et al. 1986). But two other studies, in the United States and Thailand, showed no apparent improvements with iron supplementation (Deinard et al. 1986; Pollitt et al. 1989).
From the foregoing, then, it would seem that there is good evidence to indicate that iron-deficiency anemia has detrimental effects on the mental development of children over the age of two, and that supplementation will erase those effects. In younger children, however, the evidence is less conclusive. In fact, there is little or no evidence of benefits with supplementation lasting less than two weeks, and although investigations with longer-term treatment have yielded more positive findings, such findings are inconsistent.
Nonetheless, the evidence generated by such investigations is of vital importance because about 51 percent of preschool-age and 38 percent of school-age children in developing countries, and 10 percent of preschool-age and 12 percent of school-age children in developed countries, are anemic (DeMaeyer and Adiels-Tegman 1985).
Short-Term Food Deprivation
Although improvement in school achievement is one of the goals of school feeding programs, there have been few well-designed evaluations of their effectiveness (Pollitt, Gersovitz, and Gargicilo 1978). The best results are most likely to be derived from such programs in developing countries where the prevalence of undernutrition is greater. But, unfortunately, most investigations conducted in these countries have tended to be poorly designed (Levinger 1986).
One exception was a small Jamaican study using a matched control group. It related improvements in school achievement to the school feeding plan, but not to improvements in nutritional status as such (Powell, Grantham-McGregor, and Eston 1983). It was speculated that the mere alleviation of hunger during school hours produced improvements in cognitive functions and behavior.
The most sensitive method of examining the effects of short-term food deprivation on mental functions involves studies in which children are used as their own controls and in which their performance is compared with and without breakfast. Four such studies (including three from the United States) have reported detrimental effects on mental functions when breakfast was omitted. In one of these, the omission of breakfast showed a deterioration in cognitive functions only in children with low IQs (Pollitt, Leibel, and Greenfield 1981). When the investigation was replicated, deterioration was found in the cognitive functions of all children (Pollitt et al. 1983b). Another study indicated that the detrimental effect on cognitive functions became worse as the period of deprivation increased (Conners and Blouin 1983).
In Jamaica, an investigation into the effects of missing breakfast among both undernourished and adequately nourished children discovered that the cognitive functions of undernourished children deteriorated with the omission of breakfast, whereas those of adequately nourished children did not (Simeon and Grantham-McGregor 1989).
The reason for the impact of short-term food deprivation on cognitive functions is not clear. However, it likely has a metabolic basis, which may result in changes in arousal levels (Pollitt et al. 1981) or in neurotransmitter levels (Wurtman 1986).The relationship between arousal levels and performance is complex (Kahneman 1973) and varies with the nature of the task (Hebb 1972) and the subjects (Eysenck 1976).
It does seem clear that undernourished children are more susceptible to cognitive function impairment resulting from short-term food deprivation than are adequately nourished children. It is possible that malnutrition may serve to sensitize the children to the stress of the omission of food. In other words, they may appraise the situation as being more threatening than do better-nourished children (Barnes et al. 1968; Smart and Dobbing 1977). But the response of malnourished children may also be due to abnormalities in carbohydrate metabolism. Illustrative is the fact that, during severe PEM, children have low fasting glucose and insulin levels (James and Coore 1970; Alleyne et al. 1972).
In concluding this discussion of short-term food deprivation and cognitive functions, we should note that although the impact of such deprivation appears to be small, there may be important consequences. If, for example, food deprivation occurs frequently over a long period, the effects may be cumulative and lead to poor levels of development and school achievement. Indeed, food deprivation, which is hardly uncommon in malnourished children, may play a significant role in the low levels of mental development generally found in such children.
There have been three major classifications of PEM, with the Gomez classification being the first (Gomez et al. 1955): Children suffering from PEM were described as being mildly, moderately, or severely malnourished, depending on their deficits in weight compared to reference values for their sex and age. However, a second classification—the Wellcome classification—takes into account the presence of edema as well as weight deficits (Wellcome Trust Working Party 1970).
These two classifications are generally used in the identification of children with severe PEM. But the use of weight and age alone is not very useful in discriminating between different types of mild-to-moderate PEM. For example, a child with a low weight-for-age may be tall and thin or short and fat. To address this problem, J.Waterlow (1976) introduced a third classification, which employs height expressed as a percentage of the expected value for age and sex, and employs weight as a percentage of the expected value for the height and sex of an afflicted child. Low height-for-age, or stunting, is thought to reflect long-term PEM, whereas low weight-for-height, or wasting, is believed to reflect recent nutritional experiences.
The prevalence of mild-to-moderate PEM in developing countries ranges from 7 to 60 percent, whereas that of severe PEM is between 1 and 10 percent (Grant 1990). PEM has a decided impact on mental development, and with an estimated 150 million children suffering from the affliction worldwide, its potential cost in human, as well as social and economic, terms is staggering.
A number of observational studies have associated mild-to-moderate PEM with poor mental develop-ment. Yet PEM tends to occur amid economic deprivation that has its own deleterious effects on development. Because it is not possible to control for many of these factors, the most effective way to determine the impact of PEM lies in the use of experimental study designs.
Unfortunately, there have been only a few experiments in which at-risk children have been supplemented and their mental development compared with that of controls. What follows is a brief summary of the findings of observational studies and experimental studies, although only those in which there was statistical control of confounding background variables are mentioned.
Investigations examining associations between mild-to-moderate PEM and the mental development of preschool-age children have been conducted in Colombia (Christiansen et al. 1977), Guatemala (Lasky et al. 1981), and Jamaica (Powell and Grantham-McGregor 1985). The results of the three studies indicated that PEM was associated with poor development.
Another seven studies involved school-age children. Undernutrition in children was associated with poor school achievement levels in the Philippines (Popkin and Lim-Ybanez 1982; Florencio 1988), Nepal (Moock and Leslie 1986), and India (Agarwal et al. 1987), and with low IQs in Jamaica (Clarke et al. 1991). In Guatemala, a study showed a close association between undernutrition and low IQs, whereas in Kenya, malnutrition was correlated with poor levels of cognitive functions (Johnston et al. 1987; Sigman et al. 1989).
There are two types of supplementation investigations: preventive and remedial. The former focuses on high-risk mothers who are supplemented during pregnancy, and on their off-spring who are supplemented in early childhood to prevent them from becoming undernourished. By contrast, in remedial studies, the focus is on already undernourished children who are supplemented to improve their nutritional status.
The findings of experimental studies in developed countries are especially likely to be inconsistent. In one preventive investigation, carried out in North America, supplementation during pregnancy provided the infant with only small advantages in play, and none in development, during its first year of life (Rush, Stein, and Susser 1980). Two other trials revealed no apparent benefits for the infants whose mothers had received supplements (Osofsky 1975; Pencharz et al. 1983). In a fourth study in which supplementation began during pregnancy and continued during the first year of life, children experienced large gains in development, compared with their older siblings (Hicks, Langham, and Takenaka 1982).
One reason for the inconsistency in the findings of these four studies is that in a developed region like North America, the children under scrutiny would probably not have become malnourished, regardless of whether they had supplemented mothers.
A fifth supplementation study in the developed world was remedial. Carried out as a clinical trial in England (Lucas et al. 1990), it investigated the effects of an enriched formula on the development of small preterm children. Marked benefits were shown at 18 months, especially in motor development.
It is the case, however, that studies conducted in developing countries where malnutrition is endemic are much more useful in determining whether the association between PEM and mental development is causal. One from Colombia, in which the supplementation was preventive, produced evidence of beneficial effects, first in motor development (Mora et al. 1979) and later in language (Waber et al. 1981). In Taiwan, supplementation of pregnant mothers, but not of children, led to benefits in motor development when the children were eight months old, although there was no effect on mental development (Joos et al. 1983). Supplementation of both mothers and children, however, resulted in gains in mental and motor development in Mexico (Chavez and Martinez 1982), and in cognitive functions in Guatemala (Freeman et al. 1980).
As for remedial studies, in one conducted in Colombia, both malnourished and adequately nourished children were supplemented for one year. Only those who had been malnourished improved in their development (Mora et al. 1974). In a second such investigation in Colombia, a supplementation-stimulation program was found to encourage mental development and a subsequent improvement in school performance. Moreover, such positive effects increased with the duration of the program. However, supplementation alone had no effect on development (McKay et al. 1978).
Jamaica was the site of a third remedial study, in which children ages 9 to 24 months, with low heights-for-age, were given nutritional supplementation for two years. There was a beneficial effect on development. Locomotor development was affected first, followed by mental functions. This clinical trial also had a stimulation component, and the effects of supplementation and stimulation were additive and not interactive (Grantham-McGregor et al. 1991).
To sum up, in developing-world countries, improvement in mental development was found in studies in which supplementation was preventive. This was also the case in two of the three remedial investigations. There were design flaws in some of the investigations, but considering the consistency of the findings across developing countries, the evidence indicates that both remedial and preventive supplementation encourage development. In general, however, the benefits are small, perhaps because the gains in growth were also small in the supplemented children. Indeed, the actual levels of supplementation were less than intended because of the problems of food sharing and substitution that occur in supplementation studies (Beaton and Ghassemi 1982).
Finally, the importance of the cumulative effect of mild-to-moderate undernutrition (or its absence) throughout childhood cannot be accurately assessed in supplementation programs lasting a relatively short period of time and producing only small improvements in growth.
The most common method of defining severe PEM in children is the Wellcome classification, which includes those suffering from marasmus, kwashiorkor, or marasmic-kwashiorkor.
Because it is not ethical to conduct experimental studies with severely malnourished children, investigations have been observational, and most of the children studied were treated in hospital in the acute stage. Early studies reported poor levels of mental development in children with severe PEM (see, for example, Gerber and Dean 1956). There followed a series of cohort studies of school-age children who survived severe PEM in early childhood.
As in examinations of mild-to-moderate PEM, a main problem was that the poor socioeconomic environment in which the victims lived tended to confuse the relationship between PEM and poor mental development. The use of well-matched controls was therefore essential and improved over time. Two strategies were employed to control for social background. The first was the use of siblings of the index children as controls, and the second included the use of children from similar socioeconomic backgrounds.
These strategies, of course, have inherent problems. Although it is reasonable to assume that both the index child and the sibling have lived under similar socioeconomic conditions, there are unavoidable biases when siblings are used as controls. It is not possible, for example, to control for age and birth order, both of which affect development. In addition, it is possible that a child who has become severely malnourished has not been treated the same way as a sibling who was not malnourished. Most importantly, it is probable that the siblings were also malnourished and, consequently, had lowered levels of mental development themselves. Finally, there is evidence that long-term PEM may have greater negative effects on mental development than an episode of severe PEM (Grantham-McGregor, Powell, and Fletcher 1989). Therefore, the true effects of severe PEM are likely to be worse than those determined from studies using sibling comparisons.
The use of nonsibling controls from the same socioeconomic class also presents problems. Families of children with severe PEM tend to be poorer (Richardson 1974) and to have less stimulating home environments (Cravioto and DeLicardie 1972) than their control comparisons, and both of these factors can affect mental development. In the following discussion, research on the effects of severe PEM on mental development during its acute phase will be discussed first, followed by a look at investigations of its long-term sequelae. Finally, the effects of severe PEM, as demonstrated by studies conducted in developed countries, will be reviewed.
In early reports, children suffering from severe PEM were described as apathetic (Williams 1933) and having poor levels of mental development (Cravioto and Robles 1965; Yatkin and McLaren 1970; Monckeberg 1979). Although there was some evidence of improvement after clinical recovery, these studies had no controls. But, in a controlled study in Jamaica, severely malnourished children were found to have lower levels of mental development when compared with controls hospitalized for other illnesses. The developmental levels of both groups improved during their hospital stay. However, the mal-nourished group failed to reduce their deficit relative to the controls. The children who had suffered from PEM were also less active, more apathetic, and less exploring than the controls (Grantham-McGregor et al. 1990).
Long-Term Effects with Nonsibling Controls
In examining the long-term effects of PEM, eight studies were identified in which school-age children who had previously suffered from the illness were compared with nonsibling controls. In seven of these efforts, the mal-nourished children had lower levels of mental development than the controls. One, conducted in India, indicated that the index children had lower scores in perceptual, abstract, and verbal abilities, as well as in memory and sensory integration (Champakam, Srikantia, and Gopalan 1968).
Two other studies were conducted in Jamaica. In the first, the index children were found to have lower IQs (Hertzig et al. 1972) and lower school achievement levels (Richardson, Birch, and Hertzig 1973) than controls. The second Jamaican study also found deficits in IQs (Grantham-McGregor, Schofield, and Powell 1987) and school achievement (Powell and Grantham-McGregor 1990). In Barbados, children who had previously been severely malnourished were found to have lower IQs than controls (Galler et al. 1983b), and more behavior problems (Galler et al. 1983a), learning disabilities (Galler, Ramsey, and Solimano 1984a), and motor delays (Galler et al. 1984b).
In Uganda, severe PEM was also found to be associated with deficits in mental and motor development (Hoorweg and Stanfield 1976), and in Nigeria, children who had been severely malnourished had lower scores in a number of tests of cognitive functions (Nwuga 1977). Similarly, in South Africa, children who had previously suffered from severe malnutrition had lower IQs, lower levels of school achievement, and more behavior problems than controls (Stoch and Smythe 1976).Another South African study, however, was the only one of the eight under discussion that reported no difference in development between survivors of severe PEM and controls (Bartel et al. 1978).
Long-Term Effects and Sibling Controls
The long-term effects of PEM have also been examined in eight studies in which the development of school-age children who had previously been severely malnourished was compared with that of their siblings. Five of these studies revealed deficits in development. In Nigeria, index children were found to have lower IQs than their siblings (Nwuga 1977), whereas in India they had poorer levels of school achievement (Pereira, Sundaraj, and Begum 1979). In Mexico, boys who were previously severely malnourished had lower IQs than their siblings, although no difference was found with girls (Birch et al. 1971). In Jamaica, index children had lower verbal IQs (Hertzig et al. 1972) and more behavior problems (Richardson et al. 1973) than siblings, but there was no difference in school achievement levels. In South Africa, there was no difference in IQs between previously severely malnourished children and their siblings. However, the index children showed lower school achievement and produced lower scores on a drawing test (Evans, Moodie, and Hansen 1971).
Yet, severe PEM was found to have no effect on children’s school achievement in Peru (Graham and Adrianzen 1979), and none on motor development in South Africa (Bartel et al. 1978). Another South African study examined the impact, on young adults, of severe PEM in early childhood. No difference was found in school attainment or in social adjustment when compared with their siblings (Moodie et al. 1980).
As we have mentioned, in studies conducted in developing countries, it is difficult to separate the effects on mental development of severe PEM from those of poor environment. Therefore, investigations using subjects from developed countries can be helpful. Unlike the situation in developing countries, where poverty is the primary cause of malnutrition, children in developed countries generally become malnourished because of diseases, such as cystic fibrosis. Since the children’s developmental state tends not to be associated with deprived social conditions, such cases present an opportunity to view the long-term effects of severe PEM from a fresh angle.
The results of these studies have been inconsistent. Small deficits in children’s development were demonstrated in some instances (Klein, Forbes, and Nader 1975; Winick, Meyer, and Harris 1975; Carmona da Mota et al. 1990), but no deficits were found in others (Lloyd-Still et al. 1974; Valman 1974; Ellis and Hill 1975). It is possible that the findings in developed countries have not been as consistent as those in developing countries because the children in the former tended to have less severe episodes of PEM that continued for shorter periods.
It is also possible that the environments in which the children were raised after the episode of PEM had a modifying effect. Psychosocial stimulation can improve the development of severely malnourished children. Such improvements were only transient in the wake of short-term programs (McLaren et al. 1973; Cravioto and Arrieta 1979) but lasted for several years following a three-year program (Grantham-McGregor et al. 1987). This effect is consistent with animal studies in which stimulation has decreased the adverse effects of severe PEM on development (Levitsky 1979).
Clearly, then, there are problems with inferring a causal relationship between severe PEM and poor mental development on the basis of nonexperimental studies. Nonetheless, the results of the studies reviewed indicate that children who are severely mal-nourished in early childhood and are raised in deprived conditions usually have lower levels of mental development than similarly deprived children who are not severely malnourished. The effects have been more consistent in studies in which malnourished children were compared with nonsibling controls rather than with siblings. This may be because of over-matching in the latter studies.
The mechanism linking PEM to poor mental development is not clearly established, but there are several hypotheses that assume a causal relationship. Children who died from severe PEM have been found to have smaller brains than comparison children (Winick and Rosso 1969; Rosso, Hormazabal, and Winick 1970; Dickerson, Merat, and Yusuf 1982), and it is certainly possible that impairments in brain growth may have adverse effects on mental development. Although findings from animal studies indicate that the anatomical changes due to PEM are persistent (Bedi 1987), it is not clear if this is the case in humans. In addition, it is not known if children with mild-to-moderate PEM also experience impaired brain growth.
The brain function of severely malnourished children has also been investigated by using evoked brain potentials. However, here the findings have proven inconsistent. In Mexico, abnormal auditory evoked potentials were found in severely malnourished children when compared with matched controls, and the abnormality persisted after clinical recovery (Barnet et al. 1978). In South Africa, the results of electroencephalograph (EEG) measurements indicated that children who had previously been severely malnourished had delays in brain development when compared with their siblings, but there was no difference when compared with nonsibling controls (Bartel et al. 1979). On the other hand, two other South African studies found no difference in EEGs when previously severely malnourished children were compared either with their siblings (Evans et al. 1971) or with nonsibling controls (Stoch and Smythe 1976).
It has been speculated that malnourished children are less active, explore their environments less, and thus acquire skills more slowly than adequately nourished ones. It may well be that in addition, their caretakers become less responsive to them, thus exacerbating poor development. Yet, although malnourished children have been shown to have lower activity levels and poorer developmental levels than adequately nourished children (Chavez and Martinez 1982; Meeks Gardner et al. 1990), there is no evidence showing that reduced activity precedes poor development (Grantham-McGregor et al. 1990).
In conclusion, it seems clear that various nutritional deficiencies have adverse effects on mental development. There are concurrent deficits in development in the face of mild-to-moderate PEM, severe PEM, short-term food deprivation, and iron-deficiency anemia. Maternal iodine deficiency has long-term effects on development, and severe PEM, usually, has long-term effects on mental development, if the children live in poor environments. But it has not yet been established that less severe PEM has long-term sequelae.