Impact of health and nutrition on school readiness

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Common conditions of poor health and nutrition can affect education in a number of ways. First of all, health and nutrition has an impact on children's access to education, particularly where disease leads to serious physical or mental disabilities. However, this chapter addresses the impact of health and nutrition on children's ability to learn once they do enroll in school - their 'school readiness'. This impact on school readiness may have knock-on effects for children's educational achievement and attainment, particularly where effects of disease and poor nutrition on brain development persist as cognitive impairments or emotional problems throughout the school-age years.

School readiness refers to a range of competencies that preschool children should possess to benefit from the school environment. In order to be ready for school, in this sense, children require certain cognitive skills, such as language abilities and numeracy, a level of physical and motor development, and appropriate socioemotional development. Each of these factors will be given individual consideration in reviewing the evidence for an effect of preschool health and nutrition on school readiness.

Undernutrition

Effects on cognitive development

Undernutrition (also called 'protein energy malnutrition') is a general term applied to children with heights and weights below age-referenced criteria. It typically results from a severe or chronic lack of a range of essential nutrients rather than from just a lack of protein. This complicates the discussion of the cognitive consequences of undernutrition because several different causal factors may be involved, each potentially associated with a different means of affecting brain and behavior.

Nevertheless, evidence suggests that undernutrition impairs children's mental development in the early years, through one mechanism or another. A low height or weight for age is associated with impairment in developmental levels of young children (see [4] for a review). For example, in Guatemala the length and weight of 1-2-year olds was related to their scores on a test on infant mental development [5].

Children hospitalized with severe malnutrition show lower developmental levels, but not more so than in children hospitalized for other reasons [6]. Similarly, on recovery the development levels of severely malnourished children remain impaired but this is likely attributable to chronic undernu-trition rather than the acute episode itself [7].

Quality evidence of the relationship between nutrition and cognitive development comes from intervention trials that fall into two categories: preventative and therapeutic. We look here at these in turn. In many countries steps have been taken to prevent malnutrition in children by beginning nutritional supplementation in pregnancy and continuing in infancy. This approach has been successful in improving cognitive development. In Guatemala, such a supplementation program found small improvements in cognitive function for children between 3 and 7 years [8]. Supplementation in Mexico from shortly after birth and throughout the first 3 years was found to improve children's school performance and language skills [9]. In addition, from 8 months of age, supplemented children became increasingly active and by 2 years of age were showing eight times more activity than non-supplemented children. A similar program with high-risk mothers in Bogotá, Colombia was successful in improving the mental development of their children at 18 months and also their language skills at 36 months [10]. One group of mothers in this study received education on how to stimulate cognitive development in their children. This program improved children's language skills assessed at 18 months and 36 months. In addition, the nutritional supplementation and maternal education program worked synergisti-cally: supplementation improved the effectiveness of stimulation (or vice versa) such that the benefit of receiving both interventions was greater than the sum of the independent benefits of the two interventions. A final finding is worthy of note from this study: Overall girls benefited more from the program than boys. This study is fairly unusual in reporting such an effect. However, if gender differences were found to be common in children's response to nutritional supplementation, this would have important implications for the gender equity goals of Education for All.

One study in Kenya [11] found a benefit of a school-feeding program for children's educational outcomes. Children were given a breakfast meal throughout and an ECD class, and improvement was found in educational achievement but not in tests of cognitive function, and was only evident in schools with an experienced teacher. The improvement in educational achievement was around 0.4 SD.

Results from therapeutic trials also provide strong evidence of a link between nutritional supplementation and cognitive development. These studies have typically involved remedial nutritional supplementation of malnourished children. In Bogotá, Colombia children from a poor urban area who underwent four periods of an educational stimulation and nutritional supplementation program between the ages of 42 and 84 months showed a gain in general cognitive ability of 0.80 SD in comparison with a group who received the same treatment for only one period between the ages of 74 and 84 months [12]. In so doing, these children closed the gap in IQ between themselves and a group of richer urban children. In this study, children received both nutritional supplements and education, and it is not possible to decipher which of these two interventions was most influential in improving children's cognitive abilities. A more recent study in Jamaica helped resolve this issue by giving poor, urban and undernourished children aged 9-24 months a 2-year program of either nutritional supplements, stimulations, both interventions or neither intervention. The gains in overall development quotient (DQ), an IQ equivalent for infants and young children, were impressive. Nutritional supplementation accounted for an increase of 6.1 DQ points (0.66 SD) over 2 years, while stimulation improved DQ by 7.3 points (0.79 SD). The effects of the two interventions were additive (receiving both interventions was better than receiving only one of them) but there was no interaction between them (nutritional supplementation did not improve the effectiveness of the stimulation program, for example). Significantly, the children who did receive both treatments effectively closed the gap in DQ between themselves and adequately nourished children [13].

Long-term effects on cognition

The above studies show that undernutrition leads to impaired school readiness in terms of cognition. The reason for concern about delayed school readiness is that children are likely to perform less well at school as a result. But is there evidence of this? It is certainly possible that differences in school readiness at the age of school entry may lead to poor achievement, which in turn leads to drop out and repetition, and thus deficits become compounded. On the other hand, mental development can be quite robust to early difficulties. For example, large differences in language abilities in the preschool years typically even out in the early years of primary school. The following reviews the evidence that preschool undernutrition has long-term effects.

Beginning with the most profound nutritional insults, severe malnutrition in early childhood has a long-term effect on development. Children in Jamaica who were admitted to hospital suffering from severe malnutrition between the ages of 6 and 24 months were found to lag behind adequately nourished children, who had been hospitalized for other reasons at ages 7, 8, 9 and 14 years, on a range of IQ tests. At 14 years they were substantially delayed in overall IQ (1.50 SD below the control group), vocabulary (1.33 SD) and tests of educational achievement, even after accounting for differences in the background of the two groups of children [14]. These are substantial differences that are far from unique. Similar results have been found in more than a dozen other studies [15].

Other results from experimental interventions strengthen the evidence for a long-term effect of nutrition on cognition and also demonstrate the potential for reducing the gap between severely undernourished children and their peers. The study in Jamaica found that a 3-year program to teach mothers how to improve the development of their child (aged 6-24 months at the beginning of the program) conferred significant long-term benefits on undernourished children. At age 14 years, the undernourished children whose mothers had taken part in the education program were only 0.28 SD behind adequately nourished children on overall IQ scores and 0.68 SD ahead of undernourished children who had not taken part in the intervention.

It is clear that severe malnutrition has a substantial long-term effect on child development. Of potentially greater concern is the effect that mild and moderate malnutrition has on child development, given the high prevalence of this condition amongst children in developing countries. This issue has again been addressed by researchers in Jamaica who followed 127 undernourished children for 8 years. As discussed above, these children received a 2-year program of nutritional supplementation, psychosocial stimulation, both interventions or neither intervention. Four years after the end of interventions, perceptual/motor skills - but not other cognitive skills - were superior in those children who had received stimulation [16]. The same skills were also superior for children who had originally received a nutritional supplement and whose mothers had the highest verbal intelligence. One explanation for this interaction was that the most intelligent mothers were also the ones giving children the most stimulation. There were no effects of the intervention on general cognitive abilities or on memory, although each intervention group had higher scores than the control subjects on more of these cognitive tests than would be expected by chance. Thus, stimulation, and to a lesser extent supplementation, had modest effects on children's cognitive abilities over 4 years.

The study also compared the stunted children taking part in the original intervention with other children from similar backgrounds, but who were known not to be stunted at the time of the interventions. These non-stunted children had higher scores on the general cognitive factor than previously stunted children, although they were no better in perceptual-motor skills or memory.

There were similar findings 8 years after the end of the intervention. Children who received stimulation as infants had a higher IQ (by 0.42 SD) at ages 11-12 years, while supplementation had no effect on cognitive abilities of children at this age. Again, children who were stunted before 2 years of age had a lower IQ (by 0.60 SD) and performed less well on eight out of nine cognitive tests (effect size range 0.38 SD to 0.61 SD) at age 11-12 years than children who were not stunted before 2 years of age [17].

A more recent study in Vietnam [18] adds to our understanding of the interaction between educational and nutritional interventions in early childhood. In this study, children aged 0-3 years in five communities were given nutritional supplements. In two of these communities children took part in an ECD project at ages 4-5 years. At ages 6-8 years those who had received both interventions scored 0.25 SD higher on the Raven's Progressive Matrices Test (a test of non-verbal reasoning) than those who had received only the nutritional intervention. The effect was particularly pronounced for those who were stunted at the time of testing. Amongst stunted children, those who had received both interventions scored significantly better (0.67 SD) than those who had only received the nutrition intervention. Furthermore, the ECD intervention appeared to counteract the impact of stunting on cognitive abilities, whereas those who had received nutritional supplements but no ECD intervention showed a large (~0.5 SD) difference between stunted and non-stunted children (Fig. 1).

In another long-term follow-up study in Guatemala, children given nutritional supplements prenatally and in the immediate postnatal period (up to 2 years) were found to perform better as adolescents (aged 13-19 years) on tests of vocabulary, numeracy, knowledge, and reading achievement [19]. Interestingly, these benefits were found only for those children of low socio-economic status. In tests of reading and vocabulary, the effect of supplements was most evident for children with the highest levels of education. Performance in tests of memory and reaction time were better in supplemented children, although the improvement did not depend on

Figure 1. Impact of two preschool interventions in Vietnam on cognitive abilities of children aged 6-8 years.

socio-economic status or education. A later study of women in this cohort [20] found a positive effect of the nutritional intervention on educational achievement but only for those who had completed primary school.

The studies in Jamaica and Guatemala show that a fairly sustained program of nutritional supplementation and/or psychosocial stimulation, lasting for 2 years, can have long-term benefits for children's development. A study in Indonesia shows that even a 3-month program of supplementation can have long-term effects [21]. Children supplemented before 18 months were found to have improved performance on a test of working memory at age 8 years, although no effect was observed on other measures of information processing, vocabulary, verbal fluency and numeracy.

Undernutrition and motor development

Motor development is an important aspect of school readiness and can often be closely associated with cognitive development. Four studies were found that reported the impact of nutritional supplementation on motor development. Three of the studies were reported above and found a greater impact of the intervention on motor development than on cognitive development. A third study found an impact on motor development but not on cognitive development. The first study found improvement in motor development of infants in Taiwan by 8 months of age [22] following supplementation during pregnancy and early infancy. The second study is the preventative trial in Columbia [10]. At 18 months this program was successful in improving the motor development of their children to a greater extent than their mental development. In another preventative trial in West Java, Indonesia [23], a short-term intervention - only 90 days of nutritional supplementation beginning after pregnancy - found improvements in the motor development of children at between 6 and 20 months of age. No impact was found on mental development. Finally, in the Jamaican study, giving nutritional supplementation and/or psychosocial stimulation to undernourished children, larger gains were found for the locomotor sub-scale of the assessment battery than for mental development - a 12.4 point (1.04 SD) increase was found due to supplementation (compared with 6.1 points for mental development) and 10.3 points (0.87 SD) due to stimulation (compared with 7.1 points for mental development). A possible interpretation of these results is that nutritional supplementation is more important for motor development than for mental development. Four years after the end of interventions, motor skills were superior in those children who had received stimulation [16].

Socio-emotional development

Evidence on social and emotional development is more scarce than evidence on mental and motor development. This is due in part to the difficulty in measuring development in this domain and the time-consuming observation techniques that are typically involved. But some evidence suggests that both chronic and acute malnutrition is associated with changes in social and emotional development in young children. For example, in Kenya, undernourished infants were found to be less sociable than adequately nourished infants [24]. Acute episodes of severe undernutrition can lead to increased apathy, decreased activity and a less frequent and less thorough exploration of the environment [15]. After the acute episode, all behavior returns to normal except for the thoroughness of exploration of the environment.

Similar to motor and cognitive development, aspects of social and emotional behavior can be improved by interventions. The program in Mexico [9], which gave nutritional supplements from shortly after birth and throughout the first 3 years, was found to improve adaptive behavior and personal and social behavior in addition to the cognitive improvements reported above. Similarly, the supplementation program with high-risk mothers in Bogotá, Columbia found improvements in personal and social skills as well as the cognitive and motor improvements reported above [10].

Children who enter school with poor socio-emotional developmental levels are a concern because they are less able to adapt to the school and less able to learn. The link between socio-emotional development and cognitive development is clear. For example, in Kenya, children who were undernourished at 6 months were also less sociable, and those who were less sociable at 6 months had lower development scores at 30 months and poorer verbal comprehension scores at 5 years [24]. However, poor socio-emo-tional development is a concern in its own right for the school-age child. In addition, there is good evidence from Jamaica that nutritional deficiencies in early childhood have a long-term impact on socio-emotional outcomes. Children who were stunted before aged 2 years in this study were more likely to have conduct disorders aged 11-12 years [25]. However, those who received psychosocial stimulation during early childhood as part of this program were found in a recent follow-up to be less anxious and depressed with fewer problems of poor attention and low self-esteem [26]. There were no such beneficial effects from children who received nutritional supplementation as part of this program.

It is not clear from this study how such long-term effects arose. It is possible that they represent the continuation of social and emotional benefits of the psychosocial intervention, which were already evident in early childhood. Alternatively, they may have resulted from, for example, improved cognitive abilities that resulted from the intervention and led to increased self-esteem and other positive psychosocial outcomes. However, taking findings of short-term and long-term effects together, there is strong evidence that undernutrition can lead to poor socio-emotional outcomes, which will affect school readiness.

Timing

It might be expected that nutritional deficits in the first year of life have the greatest impact on development. However, evidence does not bear this out. A study in Colombia found that giving nutritional supplements to children between 6 months and 36 months of age had a greater impact on cognitive development at 36 months than supplements given to the mother in the third trimester of pregnancy and then to the child up to 6 months of age, and the same impact as a continuous supplementation running from the third trimester of pregnancy to 36 months [10]. A longer-term study in the Philippines found that malnutrition in the second year of life actually had a greater impact on the performance of 8-year-old children on a non-verbal test of intelligence than malnutrition in the first year of life [27].

Other studies support early supplementation. In Indonesia, children supplemented before - but not after - 18 months of age were found to have improved performance on a test of working memory at age 8 years [21]. Another study in the Philippines found that children stunted in the first 6 months were more likely than those stunted later on to have impaired cognitive performance at 8 years of age [28]. This however was explained by the fact that the children suffering the earliest bouts of malnutrition also suffered the most severe and persistent malnutrition. A confounding factor such as this is a reminder of the difficulty in interpreting findings related to timing effects of nutritional deficiencies on cognitive development. At present, there is no strong evidence that early (first year of life) interventions with children suffering from or at risk of malnutrition are more effective than interventions at a later age.

Maternal behavior

A child's development is shaped by a complex interaction of factors in its environment. Just as a child's active interaction with its environment is crucial for development so is the active engagement of others in their environment. Nutrition can play a part in this too. In Egypt and in Kenya, maternal behavior towards toddlers was found to be influenced by the nutritional intake of the child more than that of the mother [29], with poorly nourished children more likely to be carried by their mother and in general stay closer to their mother than adequately nourished children [30].

In addition to the effect child malnutrition has on maternal behavior, evidence from Mexico suggests that mothers of malnourished children behave differently towards their children even before the onset of malnutrition [31]. They were less likely than other mothers to reward the successes of their child, were less affectionate and talked less to them. This could be because mothers of children who become malnourished are less well educated than other mothers [14]. In addition, mothers of malnourished children may often be poorly nourished themselves, which in turn affects their behavior. In Kenya, it was found that although toddlers were protected from the effects of temporary food shortages, their mothers were not and maternal nutritional deficiencies led to changes in the quality of mother-child interactions [32].

These findings have clear implications for children's development. We have seen that psychosocial stimulation is perhaps the most important factor preventing poor cognitive outcomes in malnourished children. If these children typically receive poor levels of stimulation from their parents - for whatever reason - the lack of stimulation is likely to compound the effects of nutrition on their development.

Low birth weight

A number of the intervention studies reported above begin nutritional supplementation before birth in recognition of the importance of prenatal nutrition. Children with a low birth weight or more generally, those born small for their gestational age (SGA) have poor developmental outcomes with implications for school readiness. Differences between SGA babies and those of normal birth weight typically do not appear in the first year of life [33], although this can depend on environmental factors. In Brazil, developmental delays were observed only in SGA babies who also received little stimulation in the home. Similarly, low birth weight affects infant development to a greater extent in the homes of illiterate mothers as compared to literate mothers. Deficits in developmental levels appear with high-risk infants in the second year with clear significant differences apparent by the third year. Some deficits were also found in the development levels of SGA babies between the ages of 4 and 7.

Breast feeding

The percentage of infants who are exclusively breastfed in the first 6 months of life fell from 43% in 1998 to 34% in 2004 [34]. In Western and Central Africa the figure is only 20%. This is of concern because breast feeding is associated with a moderate long-term improvement in cognitive development. A review of 17 studies in developed countries estimated that breast feeding led to an improvement of 3.2 IQ points (~0.21 SD), which was fairly stable across the lifespan from 3 to 50 years of age [35]. Low birth weight babies benefit most from breastfeeding, gaining 5.2 IQ points (0.35 SD) compared with a gain of 2.7 points (0.18 SD) for children of normal birth weight.

The effects of breastfeeding also depend on the length of time that infants were breastfed. Scandinavian children breast fed for longer than 6 months were found to have improved cognitive tests outcomes at 5 years compared with children who were breastfed for less than 3 months [36]. However, it is difficult to be certain about such findings since mothers who choose to breastfeed are often more educated or more wealthy and this could explain some of the difference in IQ scores [37], although review studies do attempt to account for such factors in their estimates of IQ differences [38]. In general, the evidence is not conclusive but is strongly suggestive of a link between breast feeding and cognitive ability in later life.

Iron-deficiency anemia

Iron deficiency and mental development: Children < 2 years

A number of studies have found that infants with iron deficiency have lower developmental levels than iron-replete children. Lower scores on the Mental Development Index and the Psychomotor Development Index of the Bayley Infant Development Scales for iron-deficient children have been found with 12-month-old children in Chile [39], 12- to 23-month-old children in Costa Rica and [40], 6- to 24-month-old children in Guatemala [41], and 12- to 18-month-old children in Indonesia [42].

Only one rigorous randomized controlled trial has been conducted on the impact of iron supplementation on children less than 2 years of age in a low-income country that has met rigorous criteria for experimental design (a double-blind randomized controlled trial). This study in Indonesia [42] gave iron supplementation (iron sulfate) or placebo to iron-deficient children aged 12-18 months. Those receiving iron supplementation showed impressive gains in the Bayley Scales of Infant Development. Their Mental Development Index rose by 19.3 points (1.3 SD). This represents a substantial improvement by children receiving iron supplementation. At the end of the 4-month trial, these children had similar developmental levels to those who were not iron deficient in the first place.

Other studies have conducted supplementation trials over a similar time period (a 12 weeks), although none had the same rigorous experimental design. One other study in Indonesia succeeded in eliminating differences between iron deficient and iron-replete children after supplementation, while in two other studies, in Chile [39] and Costa Rica [40], there was no observed effect of supplementation. However, in the Costa Rica study, children whose iron status recovered completely also showed improvement in their mental and psychomotor development indices. A number of shorter term trials (< 15 days) have also been conducted. There is no evidence of improvement of iron-deficient children in such trials [43].

Taken together, the evidence from all trials suggests that iron supplementation can improve the development of children under 2 years if sustained over a sufficiently long period of time (~12 weeks).

Iron deficiency and mental development: Children aged 2-6 years

A number of studies have compared iron-deficient/anemic children with iron-replete children. Working in the preschool age group, Pollitt et al. [44] found that Guatemalan children with iron-deficiency anemia took longer to learn a discrimination task than their iron-replete peers. The difference between the two groups was substantial in this test (> 3 SD), although there were no differences in two other tests. Similarly, Soewondo et al. [45] found that Indonesian children with iron-deficiency anemia were slower than iron-replete children in a categorization task, although the two groups performed similarly on tests of learning and vocabulary. No such differences were found with younger children in one study in India [46].

All five studies in the preschool age group have found improvements in the cognitive function of iron-deficient children following iron supplementation, including improvements in a learning task [44, 45] and in an IQ test [46]. One study in Zanzibar [47] gave 12 months of iron supplementation and deworming treatment to children aged 6-59 months from a population in which iron deficiency was common. They found that iron supplementation improved preschoolers' language outcomes by 0.14 SD.

One study has looked at the impact of iron supplementation in a preschool setting. This study [48] was conducted with 2-6-year olds in informal settlements in East Delhi. Children who received 30 days of iron supplementation had improved attention in class, as rated by their teachers. The improvement was around 0.18 SD in comparison with the control group. However, there was no impact on a measure of general cognitive development.

All these studies indicate that iron deficiency can lead to substantial impairments in cognitive development, which are likely to impair children's readiness for school. What is the evidence that such deficiencies have long-term implications for children's school achievement?

The most comprehensive study to address this question followed a group of Costa Rican infants for more than 10 years [49, 50]. At 12-24 months of age, 30 of the group of 191 infants had moderate anemia and received treatment. At age 5 years, formerly anemic infants performed less well on a range of tests of non-verbal intelligence, after accounting for differences between the two groups in a number of variables such as socio-economic status, birth weight, maternal IQ, height and education. Verbal skills were more equally matched between groups. At age 11-12 years, the formerly anemic group performed more poorly in writing and arithmetic, and spatial memory. Older children only were poorer in a selective attention test.

A number of other studies have found similar long-term effects of iron deficiency [43]. Anemic infants in Chile [51] were later found to have lower IQs and poorer performance on a range of tests of verbal and visual abilities at 5 years of age. Studies have attempted to quantify the relationship between infant anemia and later cognitive impairment. A study with infants in Israel [52] found that a reduction in hemoglobin levels of 10 g/l at 9 months was associated with a reduction of 1.75 IQ points at 5 years of age (although no effect on developmental levels was found at 2 and 3 years of age). Children in the anemic group were found to be learning less well and to be less task-oriented than control children in second grade [53].

The results from these studies should be interpreted with a degree of caution. None of the studies reported in this section allows causal inferences to be drawn. In each study, the anemic group most likely differed from the control groups on a number of background variables such as socio-economic status. One study [51] found that, in comparison to the control group, the homes of anemic infants were less stimulating and their mothers were more depressed and less affectionate. Thus, we cannot be sure that differences in performance between groups are not attributable to these other background characteristics, even though comprehensive attempts were made to control for them statistically in most studies.

Notwithstanding this caveat, the evidence of the effect of anemia and iron deficiency on the brain, on the behaviors of infants, preschoolers and their caregivers, and the suggestion that the effect is a long-term one, combine to make a persuasive case for early intervention to prevent iron deficiency.

Iron deficiency and motor development

Iron supplementation is found to have a substantial impact on the motor development of infants and also a significant effect on older preschool children. One study in Indonesia gave iron supplementation (iron sulfate) or placebo to iron-deficient children aged 12-18 months and scores on the Psychomotor Development Index of the Bayley Scales of Infant Development rose by 23.5 points (1.6 SD). Most studies find cognitive or motor impacts of around 0.2-0.4 SD, but this study in Indonesia shows that iron supplementation can have truly substantial effects on development.

A study with older (6-59 months) preschool children in Zanzibar [47] found that 12 months of iron supplementation and deworming treatment improved preschoolers' motor outcomes by 0.18 SD.

Such effects found with children of enrollment age persist into the school-age years. In Costa Rica, formerly anemic infants performed poorly on motor tests at 5 years of age and again aged 11-12 years [50]. Anemic infants in Chile [51] were also later found to perform poorly on a range of tests of motor function.

Socio-emotional development

There is clear evidence that iron-deficiency anemia affects social and emotional development. In Costa Rica [40], infants with iron-deficiency anemia were found to maintain closer contact with caregivers; to show less pleasure and delight; to be more wary, hesitant, and easily tired; to make fewer attempts at test items; to be less attentive to instructions and demonstrations; and to be less playful. In addition, adults were found to behave differently towards iron-deficient children, showing less affection and being less active in their interactions with these children. Such findings have serious implications for the amount of stimulation children receive, both from their own exploration of the environment and in the stimulation they receive from their caregivers.

When these infants were followed up at age 11-12 years [49], the formerly anemic group was more likely to have a number of behavioral problems. They were more anxious and depressed, had more attention problems, social problems and behavioral problems overall. They were also more likely to repeat grades at school and to be referred for special service.

lodine deficiency

Iodine is required for the synthesis of thyroid hormones. These hormones, in turn, are required for brain development, which occurs during fetal and early postnatal life [54]. Mental development is affected by both maternal hypothyroidism (a deficiency in maternal thyroid activity), which affects development of the fetal brain during the third trimester, and hypothyroid-ism in the newborn, which affects postnatal brain development. In either case, a spectrum of neurological disorder can ensue, from severe mental retardation associated with cretinism to more subtle neurological impairments. Nearly 50 million people suffer from iodine-deficiency disorder-related brain damage. A relatively small proportion of these (< 10%) are cretins with the remainder suffering more mild impairments.

Iodine supplementation in pregnancy reduces cretinism and improves IQ and school achievement between 8 and 15 years of age in one study [55] and between 14 and 16 years of age in another [56].

The clear evidence from these intervention studies is supported by findings of impaired cognitive function in adults and children living in iodine-deficient areas. An estimate based on an analysis of 21 studies suggests that general intelligence is 0.40 SD lower in iodine-deficient areas [57]. However, there is no clear evidence for the cognitive benefits of targeting preschool children with iodine supplementation.

Other micronutrients

A few other micronutrients have been studied in relation to their effect on the cognitive development of young children. There is a growing literature on zinc and mental development. In the UK, children with dyslexia were found to be deficient in zinc and have higher concentrations of toxic metals in their sweat and hair [58]. Animal studies show that zinc deficiency in offspring causes impaired learning, which can be corrected by zinc supplementation [59].

One study has been conducted to investigate the impact of maternal zinc supplementation on cognitive development. This study in Bangladesh [60, 61] gave zinc (30 mg daily) or placebo (cellulose) to pregnant women from 4 months' gestation to delivery. At 6 months, the children whose mothers had been given zinc supplementation had poorer outcomes in both mental development and psychomotor development indices. This is likely due to an imbalance of micronutrients and suggests caution should be exercised when targeting single micronutrient deficiencies for supplementation.

Disease

Cognitive impacts of malaria

The most significant infectious disease for the mental development of young children is cerebral malaria. In addition to the mortality and severe neurological sequelae associated with cerebral malaria, many children suf fer more subtle cognitive deficits, which may affect their ability to learn later on in life. In Kenya, children aged 6-7 years were studied 3-4 years after hospitalization due to cerebral malaria with impaired consciousness

[62] and were found to be 4.5 times more likely than other children from similar backgrounds to suffer cognitive impairment ranging from severe learning difficulties requiring care to mild cognitive impairments. Almost half of such children had had no neurological problems at the time of hos-pitalization. Similarly, in Senegal children aged 5-12 were found to have impaired cognitive abilities due to a bout of cerebral malaria with coma before the age of 5, possibly due to a primary deficit in attentional abilities

[63]. A third study in the Gambia looked at children who suffered from cerebral malaria that was not accompanied by neurological symptoms at the time [64]. These children had poorer balance 3.4 years after recovery implying some impaired motor development. However, no other cognitive deficit was found. In addition to the direct effects on cognitive function, an episode of cerebral malaria can leave an individual with an increased chance of epileptic episodes, which in turn can lead to cognitive impairment [65].

Cerebral malaria is clearly a major cause of cognitive impairment in preschool children. However, the incidence of serious attacks of malaria declines sharply in the school years. Is there evidence that early childhood malaria continues to be a problem for children's learning? Only one study has investigated the long-term impact of early childhood malaria prevention on subsequent cognitive development. This study in the Gambia [66] found that children who were protected from malaria for three consecutive transmission seasons before the age of 5 years had improved cognitive performance at age 17-21 years. For those who had received the longest protection from malaria, the improvement in cognitive function was around 0.4 SD.

There was also clear evidence of the impact of malaria protection on educational attainment. Children who had been protected from malaria in early childhood stayed at school for around 1 additional year (see Fig. 2).

Malaria can be prevented. Use of insecticide-treated bed nets is effective

[67] and is listed as one of the Millennium Development Goal quick wins

[68]. Use of anti-malarial drugs for intermittent preventive treatment or to treat clinical attacks may help reduce the burden of this disease [69].

Socio-emotional impacts of malaria

The effects of cerebral malaria extend beyond the cognitive domain. Psychotic episodes have been reported following bouts of cerebral malaria in Nigeria [70, 71]. However, it is not clear to what extent such episodes are common in preschool children or if other socio-emotional sequelae are present in this age group.

2 years in program 3 years ill program

Figure 2. Impact of early childhood malaria prevention on years of schooling in the Gambia.

2 years in program 3 years ill program

Figure 2. Impact of early childhood malaria prevention on years of schooling in the Gambia.

Cognitive impacts of HIV infection

There is little evidence on this issue from developing countries but research in high-income countries has demonstrated that HIV infections are associated with lower IQ and academic achievement and impaired language in the late preschool and early school-age years [72], and with poorer visual-motor functioning in older children [73]. This is likely to be due in part to the effects of HIV on cognitive development before children enroll in school. Studies including children from infancy to school age find that such deficits in cognitive function can be reduced or reversed with antiretroviral therapy (ART) [74-76]. A wide age range of children took part in these studies, spanning preschool and the school-age years. It seems likely that therapy directed specifically at preschool children will be beneficial, although one study [77] found that improvement in cognitive abilities in response to 36 months of ART was greater for children older than 6 years compared with younger children.

HIV infection and socio-emotional development

A number of studies have found that the adaptive behavior (skills required for everyday activities) of children living with HIV improves after treatment. In one study [76], after 6 months of zidovudine (AZT) treatment, almost all behavioral domains assessed (communication, daily living, socialization, but not motor skills) showed significant improvement overall. In another study infants with HIV-associated encephalopathy (degenerative brain disease) were rated as more apathetic and nonsocial in their behavior than nonencephalopathic infants. Older children (mean age around 8 years) with encephalopathy had significantly higher scores on scales measuring depression, autism, and irritability compared to non-encephalopathic patients from this age group. A subgroup of patients showed a significant decrease in these elevated scores after a 6-month course of AZT.

Orphanhood

HIV/AIDS brings with it many other factors that may affect children's education. Children living with HIV/AIDS are more likely than other children to have lost one or both parents. Evidence suggests that children living with HIV/AIDS suffer from psychosocial problems. One study in Tanzania has found increased rates of depression in AIDS orphans [78]. A more recent study in Zimbabwe [79] found that orphans had a higher rating on a measure of depression than non-orphans by 0.13 SD for boys and 0.20 SD for girls. Female orphans were also more likely to suffer from poor self-esteem. Both of these studies were conducted with older children. Further evidence is required for preschool children.

Worms

Evidence on the cognitive impact of worm infections comes mainly from the school-age years. School children in South America, Africa and South-East Asia who are infected with worms perform poorly in tests of cognitive function [80]. When infected children are given deworming treatment, immediate educational and cognitive benefits are apparent only for children with heavy worm burdens or with nutritional deficits in addition to worm infections [81-85]. One study in Jamaica [83] found around a 0.25-SD increase in three memory tests attributable to treatment for moderate to heavy infection with whipworm (Trichuris trichiura). However, for most children, treatment alone cannot eradicate the cumulative effects of lifelong infection nor compensate for years of missed learning opportunities. Deworming does not lead inevitably to improved cognitive development, but it does provide children with the potential to learn. Children in Tanzania who were given deworming treatment did not improve their performance in various cognitive tests, but they did benefit more from a teaching session in which they were shown how to perform the tests [86]. Performance on reasoning tasks at the end of the study was around 0.25 SD higher in treated children than in those who still carried worm infection. The treated children's performance was similar to children who began the study without infection. This suggests that children are more ready to learn after treatment for worm infections and that they may be able to catch up with uninfected peers if this learning potential is exploited effectively in the classroom.

It is likely that worm infections have a similar impact for preschool children. Infections are prevalent in this age group, although worm loads typically do not reach peak intensity until the school-age years. A study in Kenya showed that 28% of 460 preschool children (0.5-5 years) harbored hookworm infection, 76% were anemic and that anemia was more severe in those children with hookworm [87]. Evidence of a cognitive impact of worm infections in preschoolers is not clear. Two studies [48, 88] have demonstrated cognitive improvements in preschool children following combined treatment for worm infections and iron-deficiency anemia. However, neither study was able to disentangle the effects of the two treatments.

Other parasitic infections

Infection with Giardia lamblia has been associated with mental development. Giardia is a protozoan parasite that is ingested and inhabits the gastrointestinal tract. It contributes significantly to caseloads of diarrhea. One study in Peru [89] followed a cohort of children some of whom had had diarrheal diseases, parasitic infection and severe malnutrition in the first 2 years of life. Severe malnutrition at this age was associated with an IQ 10 points (0.67 SD) lower at age 9 years. Those who had suffered two or more episodes of Giardia lamblia per year scored 4.1 points (0.27 SD) lower than children with one episode or fewer per year. It is likely that this association is due to Giarda infection causing, or acting as an index of, malnutrition.

Otitis media (Glue Ear)

Otitis media is an inflammation of the middle ear cavity often resulting from spread of infection from the nose or throat. In acute cases, pus is produced pressurizing the eardrum and causing perforation in chronic cases.

Otitis media is common in developed and developing countries [90]. Around 6% of primary school and preschool children were found to have chronic otitis media with effusion (OME) in Vietnam [91] and South India [92]. In Tanzania, 9.4% of rural and 1.4% of urban school children were found to have chronic OME.

OME has mild effects on language development [93] and other cognitive skills. The effect depends on the length of infection and caregiver environment [94]. Children from low socio-economic status backgrounds are more likely to suffer effects of OME. Although research has not documented the effect of OME on cognitive development in developing countries, this result suggests that the effect may be greater than in developed countries.

Meningitis

Meningitis has a high prevalence in developing countries, with associated mortality and risk of severe neurological problems for survivors. Other survivors of meningitis do not have obvious neurological problems and yet suffer long-term behavioral problems.

In Ghana, survivors of meningitis aged 2-73 were more likely to suffer from feelings of tiredness (odds ratio = 1.47) and were more often reported by relatives to have insomnia (odds ratio = 2.31) [95]. However, meningitis infection did not affect school attendance amongst school-age cases.

Studies in developed countries have found that children who appear well after bacterial meningitis have more nonspecific symptoms like headache, and more signs and symptoms indicating inattention, hyperactivity and impulsiveness than their siblings [96]. Survivors of bacterial or viral meningitis go on to perform less well at school, to be more likely to repeat a grade and to be referred to a special needs school. They are also more likely to have behavioral problems in the home [97]. Cognitive abilities are also affected. Survivors of meningitis have lower IQs than their peers (~0.3 SD) at ages 7 and 12 years [98] with no sign of the gap narrowing with age. Conversely, behavioral problems of meningitis survivors are greater than their peers and actually increase with age.

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