Developmental potential in the first 5 years for children in developing countries (original) (raw)

Summary

Many children younger than 5 years in developing countries are exposed to multiple risks, including poverty, malnutrition, poor health, and unstimulating home environments, which detrimentally affect their cognitive, motor, and social-emotional development. There are few national statistics on the development of young children in developing countries. We therefore identified two factors with available worldwide data—the prevalence of early childhood stunting and the number of people living in absolute poverty—to use as indicators of poor development. We show that both indicators are closely associated with poor cognitive and educational performance in children and use them to estimate that over 200 million children under 5 years are not fulfilling their developmental potential. Most of these children live in south Asia and sub-Saharan Africa. These disadvantaged children are likely to do poorly in school and subsequently have low incomes, high fertility, and provide poor care for their children, thus contributing to the intergenerational transmission of poverty.

*Lead authors

†Steering group listed at end of the paper

This is the first in a Series of three articles about child development in developing countries

Introduction

A previous Lancet series1 focused attention on the more than 6 million preventable child deaths every year in developing countries. Unfortunately, death is the tip of the iceberg. We have made a conservative estimate that more than 200 million children under 5 years fail to reach their potential in cognitive development because of poverty, poor health and nutrition, and deficient care. Children's development consists of several interdependent domains, including sensory-motor, cognitive, and social-emotional, all of which are likely to be affected. However, we focus on cognitive development because of the paucity of data from developing countries on other domains of young children's development. The discrepancy between their current developmental levels and what they would have achieved in a more nurturing environment with adequate stimulation and nutrition indicates the degree of loss of potential. In later childhood these children will subsequently have poor levels of cognition and education, both of which are linked to later earnings. Furthermore, improved parental education, particularly of mothers, is related to reduced fertility,2,3 and improved child survival, health, nutrition, cognition, and education.3–7 Thus the failure of children to fulfil their developmental potential and achieve satisfactory educational levels plays an important part in the intergenerational transmission of poverty. In countries with a large proportion of such children, national development is likely to be affected.

The first UN Millennium Development Goal is to eradicate extreme poverty and hunger, and the second is to ensure that all children complete primary schooling.8 Improving early child development is clearly an important step to reaching these goals. Although policymakers recognise that poverty and malnutrition are related to poor health and increased mortality,5,9 there is less recognition of their effect on children's development or of the value of early intervention. This paper is the first of a three part series reviewing the problem of loss of developmental potential in young children in developing countries. The first paper describes the size of the issue, the second paper discusses the proximal causes of the loss, and the final paper reviews existing interventions. Here, we first examine why early child development is important and then develop a method to estimate the numbers of children who fail to fulfil their developmental potential. We then estimate the loss of income attributed to poor child development.

Why early child development is important

Children's development is affected by psychosocial and biological factors10 and by genetic inheritance. Poverty and its attendant problems are major risk factors.11–15 The first few years of life are particularly important because vital development occurs in all domains.16 The brain develops rapidly through neurogenesis, axonal and dendritic growth, synaptogenesis, cell death, synaptic pruning, myelination, and gliogenesis. These ontogenetic events happen at different times (figure 1)17 and build on each other, such that small perturbations in these processes can have long-term effects on the brain's structural and functional capacity.

Figure 1.

Human brain development

Reproduced with permission of authors and American Psychological Association17 (Thompson RA, Nelson CA. Developmental science and the media: early brain development. Am Psychol 2001; 56: 5–15).

Brain development is modified by the quality of the environment. Animal research shows that early undernutrition, iron-deficiency, environmental toxins, stress, and poor stimulation and social interaction can affect brain structure and function, and have lasting cognitive and emotional effects.18–24

In humans and animals, variations in the quality of maternal care can produce lasting changes in stress reactivity,25 anxiety, and memory function in the offspring,

Despite the vulnerability of the brain to early insults, remarkable recovery is often possible with interventions,18,26,27 and generally the earlier the interventions the greater the benefit.28

Early cognitive development predicts schooling

Early cognitive and social-emotional development are strong determinants of school progress in developed countries.29–31 A search of databases for longitudinal studies in developing countries that linked early child development and later educational progress identified two studies. In Guatemala, preschool cognitive ability predicted children's enrolment in secondary school32 and achievement scores in adolescence.33 In South Africa, cognitive ability and achievement at the end of grade one predicted later school progress.34 Three further studies had appropriate data that we analysed (from the Philippines35,36 and Jamaica37) or requested the investigators to analyse (from Brazil38,39). In each case, multiple regression of educational outcome (or logistic regression for dichotomous variables), controlling for a wealth index,40 maternal education, and child's sex and age, showed that early cognitive development predicted later school outcomes. Table 1 shows that each SD increase in early intelligence or developmental quotient was associated with substantially improved school outcomes. Further evidence of the importance of early childhood is that interventions at this age37,41 can have sustained cognitive and school achievement benefits (table 135–39).

Table 1.

Change in later school outcomes per SD increase in intelligence quotient (IQ) or developmental quotient (DQ) in early life*

Problem of poor development

National statistics on young children's cognitive or social-emotional development are not available for most developing countries, and this gap contributes to the invisibility of the problem of poor development. Failure to complete primary education (Millennium Development Goal 2) gives some indication of the extent of the issue, although school and family characteristics also play a part. In developing countries, an estimated 99 million children of primary-school age are not enrolled, and of those enrolled, only 78% complete primary school.44 Most children who fail to complete are from sub-Saharan Africa and south Asia. Only around half of the children enrol in secondary schools. Furthermore, children in some developing countries have much lower achievement levels than children in developed countries in the same grade.45 In 12 African countries, surveys of grade 6 (end of primary school) children showed that on average 57% had not achieved minimum reading levels (webtable).46–57

Indicators of poor development

In the following section we estimate the numbers of children who fail to reach their developmental potential. We first identify early childhood growth retardation (length-for-age less than −2 SD according to the National Center for Health Statistics growth reference58 [moderate or severe stunting]) and absolute poverty as possible indicators for poor development. We then show that they are good predictors of poor school achievement and cognition. Finally, we use these indicators to estimate the number of children involved. We identified stunting and poverty for indicators because they represent multiple biological and psychosocial risks, respectively, stunting and to a lesser extent poverty are consistently defined across countries, both are relevant to most developing countries, and worldwide data are available. We omit other risk factors that could affect children's development because they fail to fit all the above criteria and there is marked overlap between them and with stunting and poverty. However, by using only two risk factors we recognise that our estimate is conservative.

Assessment of stunting, poverty, and child development

Growth potential in preschool children is similar across countries,59,60 and stunting in early childhood is caused by poor nutrition and infection rather than by genetic differences. Patterns of growth retardation are also similar across countries.61 Faltering begins in utero or soon after birth, is pronounced in the first 12–18 months,62 and could continue to around 40 months, after which it levels off. Some catch-up might take place,63 but most stunted children remain stunted through to adulthood.

There are multiple approaches to measuring poverty.64 One assessment used measures of deprivation of basic needs, availability of services, and infrastructure,65 and surveys in 45 developing countries reported that 37 % of children lived in absolute poverty, more so in rural areas. We use the percentage of people having an income of less than US$1 per day, adjusted for purchasing power parity by country66 because this information is available for the largest number of countries. This indicator is considered the best available despite excluding important components of poverty,67 and is more conservative than measures based on deprivation65 since it identifies only the very poorest families.

Poverty is associated with inadequate food, and poor sanitation and hygiene that lead to increased infections and stunting in children. Poverty is also associated with poor maternal education, increased maternal stress and depression,12,68,69 and inadequate stimulation in the home.70 All these factors detrimentally affect child development (figure 2).12,70 Poor development on enrolment leads to poor school achievement, which is further exacerbated by inadequate schools and poor family support (due to economic stress, and little knowledge and appreciation of the benefits of education).

Figure 2.

Hypothesised relations between poverty, stunting, child development, and school achievement

Risk factors related to poverty frequently occur together, and the developmental deficit increases with the number of risk factors.15,33,71 Deficits in development are often seen in infancy31,72 and increase with age.71,73,74 For example, a cross sectional study in Ecuador reported that the language deficit in poor children increased from 36 to 72 months of age compared with wealthier children (figure 3).70

Figure 3.

Vocabulary scores of Ecuadorian children aged 36 to 72 months by wealth quartiles

TVIP=Test de Vacabulario en Imagenes Peabody. Reproduced with permission from the authors.70

As a first step to examining the use of poverty and stunting as indicators, we did regression analyses of the relation between the percentage of children completing primary school44 and poverty and stunting, with data from developing countries (defined as the non-industrialised countries in UNICEF classification).75 Stunting prevalence was based on the WHO Global Database on Child Growth and Malnutrition,76 and absolute poverty prevalence came from UNICEF.75 In 79 countries with information on stunting and education, the average prevalence of stunting was 26·0%. For every 10% increase in stunting (less than −2 SD), the proportion of children reaching the final grade of primary school dropped by 7·9% (b=−0·79, 95% CI −1·03 to −0·55, R2=36·2%, p<0·0001). In 64 countries with information on absolute poverty, the average prevalence was 20%; for every 10% increase in the prevalence of poverty there was a decrease of 6·4% (b=−0·64, 95% CI=−0·81 to −0·46, R2=46·3%, p<0·0001) of children entering the final grade of primary school**.**

To establish whether stunting and absolute poverty were useful predictors of poor child development in individual studies, we searched the published papers and identified all observational studies that related stunting and poverty in early childhood to concurrent or later child development or educational outcomes. We also identified all studies that related stunting at school age to cognition or education, based on the assumption that stunting developed in early childhood. We selectively reviewed studies of older children that linked economic status to school achievement or cognition, choosing examples with international or nationally representative samples. We assessed whether measurements of the risk factors and developmental outcome were clearly reported, and the relation between them (adjusted or unadjusted) was examined. We did not assess causality.

Stunting and poor development

Cross-sectional studies

Many cross-sectional studies of high-risk children have noted associations between concurrent stunting and poor school progress or cognitive ability. Stunted children, compared with non-stunted children, were less likely to be enrolled in school (Tanzania77), more likely to enrol late (eg, Nepal,78 and Ghana and Tanzania79), to attain lower achievement levels or grades for their age (Nepal,78 China,80 Jamaica,81,82 India,83 Philippines,84–86 Malaysia,87 Vietnam,88 Brazil,89 Turkey,90 Guatemala [only in boys]91), and have poorer cognitive ability or achievement scores (Kenya,92 Guatemala,93 Indonesia,94 Ethiopia, Peru, India, and Vietnam,95 and Chile96). Only three studies97–99 reported no significant relation between stunting and poor school progress. In the Philippines, associations were recorded with weight-for-height,99 and in Ghana98 stunted children enrolled in school late but taller children left school early to earn money or help with family farming.

There are fewer studies with younger children. In Guatemala,100 Jamaica,101 Chile,102 and Kenya,103 associations between height and child development measures were reported. Age of walking was related to height-for-age in Zanzibarian104 and Nepalese children,105 but height was not related to motor development in Kenyans at 6 months of age.106 Weight-for-age, which indicates a combination of weight-for-height and height-for-age, has often been used instead of stunting to measure nutrition in young children. Weight-for-age was associated with child development in India,107 Ethiopia,108 and Bangladesh.109,110

Longitudinal studies

In Pakistan111 and Guatemala,112 growth retardation in infancy predicted age of walking. Excluding studies of children hospitalised for severe malnutrition, four published longitudinal studies showed that early stunting predicted later cognition, school progress, or both. Stunting at 24 months was related to cognition at 9 years in Peru113 and, in the Philippines to intelligent quotient (IQ) at 8 and 11 years, age at enrolment in school, grade repetition, and dropout from school.35,36 In Jamaica, stunting before 24 months was related to cognition and school achievement at 17–18 years and dropout from school.37 In Guatemala, height at 36 months was related to cognition, literacy, numeracy, and general knowledge in late adolescence,114 and stunting at 72 months was related to cognition between 25–42 years.115 In Indonesia,116 weight-for-age at 1 year of age did not predict scores on a cognitive test at 7 years, whereas growth in weight between 1 and 7 years did.

To assess the size of the deficit in later function associated with a loss of 1 SD in height in early childhood, we reanalysed the data from Philippines,36 Jamaica, 37 Peru,113 and Indonesia 116 (Guatemala had too few well-nourished children to be included). We added two other longitudinal studies, from Brazil38 and South Africa,117 that had not previously analysed the effect of stunting (table 2). In these studies, stunting between 12 and 36 months was related to later measures of cognition117 or grade attainment.38 Being moderately or severely stunted compared with not stunted (height-for-age greater than −1 SD) was associated with scores for cognition in every study, and the effect size varied from 0·4 to 1·05 SD. Stunting was also associated with attained grades. The consistent relation between early childhood stunting and poor child development, with moderate to large effects, justifies its use as an indicator of poor development.

Table 2.

Descriptive summary of follow-up studies showing associations between stunting in early childhood and later scores on cognitive tests and school outcomes

Poverty and poor development

Cross-sectional studies

Nationally representative studies from many countries have seen relations between household wealth and school enrolment, early dropout, grades attained, and achievement.46–57,95,121–123 Gaps in mean attained grades between the richest and poorest children were particularly large in western and central Africa and south Asia, reaching as high as ten grades in India.123 In Zambia, poor children were four times more likely to start school late than the richest children, and in Uganda the difference was ten times. Representative surveys in 16 Latin American countries124 also reported that family income predicted the probability of completing secondary schooling. Rural children were worse off in most studies.123

There are fewer studies on wealth and development in preschool children. In 3668 Indian children under 6 years, paternal occupation was associated with developmental milestones.107 In Ecuador, wealth was related to vocabulary scores of children from 3 to 6 years of age.70 In Jamaica, 71·4% of 3887 children from more affluent families entering fee-paying preparatory schools had mastery of all four school-readiness subjects tested, compared with 42·7% of 22 241 children entering free government primary schools.125 An association between poverty and child development was recorded at as early as 6 months of age in Egypt,126 12 months in Brazil,127 10 months in India,128 and 18 months in Bangladesh.68 In another Brazilian study, preschool children's language scores were associated with maternal working but not income.129

Longitudinal studies

Several longitudinal studies have assessed the association between wealth at birth and later educational and cognitive attainment. Socioeconomic status in infancy was associated with children's cognition at 5 years of age in Kenya.130 In Brazil, parental income at birth was associated with poor performance on a developmental screening test at 12 months in 1400 infants, and with school grades attained at 18 years in 2222 men on army enlistment.38 In Guatemala,131 socioeconomic status at birth was associated with school attainment and cognition in 1469 adults. We analysed data from three other longitudinal studies (table 3). Wealth quintiles at birth were related to IQ at 8 years in the Philippines,36 and to cognitive scores at 7 years in South Africa117 and 9 years in Indonesia.116 The effect size in all these studies was substantial, ranging from 0·70 to 1·24 SD scores between the top and bottom quintiles in children from varied socioeconomic backgrounds, and from 0·45 to 0·53 SD scores in Guatemala where all study children were poor. We had to use wealth quintiles rather than the cutoff of US$1 per day because of limitations in the data. Poor children consistently had considerable developmental deficits compared with more affluent children. Thus poverty can be used as an indicator of poor development.

Table 3.

Descriptive summary of follow-up studies showing association between wealth quintiles in early childhood, and later cognitive and school outcomes

Estimate of number of children who are stunted or living in poverty

We estimated the prevalence of children under 5 years who are stunted or living in absolute poverty in developing countries. Data for the number of children in 2004 and percent living in poverty were obtained from UNICEF75 and data for stunting obtained from WHO.76 Of the 156 countries analysed, 126 have a known stunting prevalence and 88 have a known proportion living in absolute poverty (table 4). We replaced missing country values of stunting and poverty with the average prevalence of the region for the purpose of estimating the proportion and number of disadvantaged children. Sensitivity analysis based on imputing stunting by poverty and imputing poverty by stunting through regression analysis gave similar results to using the regional average (webappendix). The most recent poverty data we obtained was up to year 2003, with median 2000 and inter-quartile range of 4 years. The most recent stunting data were up to year 2004, with median 2000 and inter-quartile range of 3 years. We extrapolated all the stunting and poverty data to the year 2004 (table 4).75,76,132,133

Table 4.

Prevalence and number (in millions) of disadvantaged children under 5 years by region in 2004

There are 559 million children under 5 years in developing countries, 156 million of whom are stunted and 126 million are living in absolute poverty (table 4). To avoid the double-counting of children who are both stunted and living in poverty, we estimated the prevalence of stunting among children in poverty in countries with both indicators available, and calculated the numbers of stunted children plus the number of non-stunted children living in poverty. We refer to these children as disadvantaged.

The relation between prevalence of stunting and poverty at the country level is non-linear and can be captured by a regression line of percentage stunted=7·8+4·2×√%poverty (using the 82 countries with available data; R2=40·9%). Extrapolation of this regression line gives an estimate of the prevalence of stunting in people living in poverty to be 50%. Hence, the number of children stunted or living in poverty is the sum of the total number of stunted children (156 million) plus 50% of children living in poverty (63 million) making a total of 219 million disadvantaged children, or 39% of all children under 5 in developing countries.

An alternative estimate of the prevalence of stunting in children in poverty was obtained by analysis of micro-level data from 13 Multiple Indicator Cluster Surveys134 in developing countries with data for both stunting and a wealth index. A meta-analysis of the datasets showed that 43% of children below the poverty line were stunted. Based on this estimate, the total number of disadvantaged children is 227 million. Although the estimate of 219 million is inevitably crude, it is more conservative than the alternative estimate of 227 million; we use the lower estimate in the rest of the paper.

Figure 4 shows the numbers of disadvantaged children in millions by region. Most disadvantaged children (89 million) are in south Asia. The top ten countries with the largest number of disadvantaged children (in millions) are: India 65, Nigeria 16, China 15, Bangladesh 10, Ethiopia 8, Indonesia 8, Pakistan 8, Democratic Republic of the Congo 6, Uganda 5, and Tanzania 4. These ten countries account for 145 (66%) of the 219 million disadvantaged children in the developing world.

Figure 4.

Regional distribution of the number of children under 5 years in millions

(A) stunted, (B) living in poverty, and (C) disadvantaged (either stunted, living in poverty, or both) in year 2004.

Figure 5 shows the prevalence by country. Sub-Saharan Africa has the highest prevalence of disadvantaged children under 5 years, 61% (table 4), followed by south Asia with 52%.

Figure 5.

Percentage of disadvantaged children under 5 years by country in year 2004

Limitations of the estimate of numbers of disadvantaged children

More than 200 million disadvantaged children is an exceedingly large amount. However, limitations in the data suggest that the estimate is conservative. We assumed that the percentage of people in absolute poverty was equal to the percentage of children in absolute poverty. This assumption probably underestimates the number of children because poverty is associated with higher fertility levels and larger household size. Furthermore, less than US$1 per day is an extreme measure of poverty, and children in slightly better off households are probably also at risk. Also, we did not take into account many other risk factors for poor development, such as maternal illiteracy, unstimulating homes, and micronutrient deficiencies.

WHO recently produced new growth standards,135 and the −2 SD curves for length and height-for-age are slightly higher than the −2SD curves of the previous standards in certain age ranges under 60 months. Therefore, if we used the new growth standards our estimate of prevalence of stunting and disadvantaged children would be slightly higher.

The precision of the estimate of disadvantaged children would be improved with internationally comparable data for maternal education and stimulation in the home. We also need data to establish which cutoff for income and poverty is best for identifying children at high risk. Internationally comparable and feasible measures of child development would produce the best estimate of disadvantaged children, and there is an urgent need to develop such measures both to more accurately assess the problem and to assess interventions.

Some of the disadvantaged children would have IQs of less than −2 SD, the level used to diagnose mild mental retardation (IQ 50–69).136 However, a deficit in adaptive behaviour is usually needed to make the diagnosis and these data are not available, although most would have learning problems in school and restricted employment opportunities. We are concerned in this series about the loss of potential across the whole range of cognitive ability.

Economic implications of poor child development

Disadvantaged children in developing countries who do not reach their developmental potential are less likely to be productive adults. Two pathways reduce their productivity: fewer years of schooling, and less learning per year in school. What is the economic cost of one less year of schooling? Studies from 51 countries show that, on average, each year of schooling increases wages by 9·7%.137 Although some of the studies had methodological weaknesses, this average matches another more rigorous study,138 which reported that each year of schooling in Indonesia increased wages by 7–11%.

Both stunting and poverty are associated with reduced years of schooling. Table 5 presents data for school grades attained in 18-year-old Brazilian men,38 by income quintile at birth and stunting status in the first 2 years. We estimate from these data that the deficit attributed to being stunted (height-for-age less than −2 z scores compared with non-stunted greater than −1 z scores), stratified for income quintiles was 0·91 grades, and the deficit from living in poverty (first vs third quintile of income) stratified for stunting status was 0·71 grades. Furthermore, the deficit from being both stunted and in poverty (first income quintile) compared with being non-stunted and in the third income quintile was 2·15 grades.

Table 5.

Attained grades in 18-year-old Brazilian men, by income level, and stunting status in early childhood*

Stunted children also learn less per year in school. Data from the Philippines has shown that, controlling for years of schooling and income, the combined reading and math test score of stunted children was 0·72 SD below that of non-stunted children. This reduction was equivalent to 2·0 fewer years of schooling.86 Regression analysis with Jamaican data37 corroborate this finding; controlling for wealth and grade level, stunted children's combined math and reading test score was 0·78 SD below those of non-stunted children. Controlling for stunting, poor children almost certainly learn less per year in school, but we know of no studies that convincingly estimate the deficit.

Assuming that every year of schooling increases adult yearly income by 9%,137,138 we estimate that the loss in adult income from being stunted but not in poverty is 22·2%, the loss from living in poverty but not being stunted is 5·9% and from being both stunted and in poverty is 30·1% (table 6). Taking into account the number of children who are stunted, living in poverty, or both (table 6), we calculate the average deficit in adult yearly income for all 219 million disadvantaged children to be 19·8%. This estimate is limited by the scarcity of data for the loss of learning ability of children in poverty, and almost certainly underestimates the true loss.

Table 6.

Deficit associated with stunting, poverty (first vs third quintile of wealth), and both, in schooling and percentage loss in yearly income in developing countries

Clearly, disadvantaged children are destined not only to be less educated and have poorer cognitive function than their peers but also to be less productive. In consideration of the total cost to society of poor early child development, we need to take into account that the next generation will be affected, sustaining existing inequities in society with their attendant problems.67 Where large numbers of children are affected, national development will also be substantially affected. These costs have to be weighed against those of interventions.

Conclusion

Many children in developing countries are exposed to multiple risks for poor development including poverty and poor health and nutrition. There are few national data for children's development but our conservative estimate is that more than 200 million children under 5 years of age in developing countries are not developing to their full potential. Sub-Saharan African countries have the highest percentage of disadvantaged children but the largest number live in south Asia. The children will subsequently do poorly in school and are likely to transfer poverty to the next generation. We estimate that this loss of human potential is associated with more than a 20% deficit in adult income and will have implications for national development. The proximal causes of poor child development are analysed in the second paper in this series.

The problem of poor child development will remain unless a substantial effort is made to mount appropriate integrated programmes. There is increasing evidence that early interventions can help prevent the loss of potential in affected children and improvements can happen rapidly (see third paper in this series). In view of the high cost of poor child development, both economically and in terms of equity and individual well-being, and the availability of effective interventions, we can no longer justify inactivity.

Search strategy and selection criteria

The following databases were searched for studies in developing countries reported in English from 1985, to February, 2006: BIOSIS via ISI web of science, PubMed, ERIC, PsychInfo, LILACS, EMBASE, SIGLE, and Cochrane Review, along with published documents from the World Bank, UNICEF, and UNESCO's International Bureau of Education. References in retrieved papers were examined and further information sought from experts in the field. Keywords used for search 1 were: “developing countries” or “developing nations” or “third world” and “child development” or “cognitive development” or “language development” or “cognition” or “education” or “school enrolment”, “school dropout”, “grade retention”, “grade attained”, “educational achievement”. For search 2 we also used stunting or malnutrition or undernutrition, and for search 3 we used search 1 keywords and poverty or income or economic status.

Acknowledgments

Acknowledgments

UNICEF provided funding for a working group meeting for all of the authors with assistance from the Bernard van Leer Foundation. The UNICEF Innocenti Centre in Florence, Italy, hosted the meeting. Deanna Olney provided research assistance. Cesar Victora, Fernando Barros, Magda Damiani, Rosangela Lima, Denise Gigante, and Bernardo Horta assisted with the Brazilian data, Andres Lescano analysed Peruvian data, Shane Norris assisted with the South African data, and Tanya Abramsky analysed the Young Lives data. The sponsor of the study had no role in study design, data collection, data analysis, data interpretation, or writing of the report.

_International Child Development Steering Group—_Sally Grantham-McGregor, Patrice Engle, Maureen Black, Julie Meeks Gardner, Betsy Lozoff, Theodore D Wachs, Susan Walker.

Conflict of interest statement

We declare that we have no conflict of interest.

Web Extra Material

Webtable

Achievement in reading for sixth grade students in 12 African countries

Webappendix

References

• 1.Jones G, Steeketee RW, Black RE, Bhutta ZA, Morris S, the Bellagio Child Survival Study Group How many deaths can we prevent this year? Lancet. 2003;362:65–71. doi: 10.1016/S0140-6736(03)13811-1. [DOI] [PubMed] [Google Scholar]
• 2.Maitra P. Effect of socioeconomic characteristics on age at marriage and total fertility in Nepal. J Health Pop Nutr. 2004;22:84–96. [PubMed] [Google Scholar]
• 3.Lam D, Duryea S. Effects of schooling on fertility, labor supply, and investments in children, with evidence from Brazil. J Hum Res. 1999;34:160–192. [Google Scholar]
• 4.Frankenberg E, Mason W. Maternal education and health-related behaviors: a preliminary analysis of the 1993 Indonesian Family Life Survey. J Pop. 1995;1:21–44. [Google Scholar]
• 5.Hatt LE, Waters HR. Determinants of child morbidity in Latin America: a pooled analysis of interactions between parental education and economic status. Soc Sci Med. 2006;62:375–386. doi: 10.1016/j.socscimed.2005.06.007. [DOI] [PubMed] [Google Scholar]
• 6.Psacharopoulos G. The determinants of early age human capital formation: evidence from Brazil. Econ Dev Cult Change. 1989;37:683–708. [Google Scholar]
• 7.Rosenzweig MR, Wolpin KI. Are there increasing returns to the intergenerational production of human capital—maternal schooling and child intellectual achievement. J Hum Res. 1994;29:670–693. [Google Scholar]
• 8.UN . Road map toward the implementation of the United Nations Millennium Declaration. United Nations; New York: 2002. United Nations General Assembly Document A56/326. [Google Scholar]
• 9.Victora CG, Wagstaff A, Schellenberg JA, Gwatkin D, Claeson M, Habicht JP. Applying an equity lens to child health and mortality: more of the same is not enough. Lancet. 2003;362:233–241. doi: 10.1016/S0140-6736(03)13917-7. [DOI] [PubMed] [Google Scholar]
• 10.Wachs TD. Necessary but not sufficient: the respective roles of single and multiple influences on individual development. American Psychological Association; Washington DC: 2000. [Google Scholar]
• 11.Brooks-Gunn J, Duncan GJ. The effects of poverty on children. Future Child. 1997;7:55–71. [PubMed] [Google Scholar]
• 12.Bradley R, Corwyn R. Socioeconomic status and child development. Ann Rev Psychol. 2002;53:371–399. doi: 10.1146/annurev.psych.53.100901.135233. [DOI] [PubMed] [Google Scholar]
• 13.Mistry RS, Biesanz JC, Taylor LC, Burchinal M, Cox MJ. Family income and its relation to preschool children's adjustment for families in the NICHD study of early child care. Dev Psychol. 2004;40:727–745. doi: 10.1037/0012-1649.40.5.727. [DOI] [PubMed] [Google Scholar]
• 14.NICHD Early Child Care Research Network Before Head Start: income and ethnicity, family characteristics, child care experiences and child development. Early Educ Dev. 2001;12:545–576. [Google Scholar]
• 15.Rutter M. Pathways from childhood to adult life. J Child Psychol Psychiatr. 1989;30:23–51. doi: 10.1111/j.1469-7610.1989.tb00768.x. [DOI] [PubMed] [Google Scholar]
• 16.Committee on Integrating the Science of Child Development . From neurons to neighborhoods: the science of child development. National Academy Press; Washington DC: 2000. [Google Scholar]
• 17.Thompson RA, Nelson CA. Developmental science and the media: early brain development. Am Psychol. 2001;56:5–15. doi: 10.1037/0003-066x.56.1.5. [DOI] [PubMed] [Google Scholar]
• 18.Black J, Jones T, Nelson C, Greenough W. vol 1. Wiley; New York: 1998. pp. 31–53. (Neuronal plasticity and the developing brain. Handbook of child and adolescent psychiatry). [Google Scholar]
• 19.Liu D, Diorio J, Day J, Francis D, Meaney M. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci. 2000;3:799–806. doi: 10.1038/77702. [DOI] [PubMed] [Google Scholar]
• 20.Meaney M. Maternal Care, gene expression, and the transmission of individual differences in stress reactivity across generations. Ann Rev Neurosci. 2001;24:1161–1192. doi: 10.1146/annurev.neuro.24.1.1161. [DOI] [PubMed] [Google Scholar]
• 21.Morgan R, Garavan H, Smith E, Driscoll L, Levitsky D, Strupp B. Early lead exposure produces lasting changes in sustained attention, response initiation, and reactivity to errors. Neurotoxicol Teratol. 2001;23:519–531. doi: 10.1016/s0892-0362(01)00171-4. [DOI] [PubMed] [Google Scholar]
• 22.Rodier P. Environmental causes of central nervous system maldevelopment. Pediatrics. 2004;113:1076–1083. [PubMed] [Google Scholar]
• 23.Webb S, Monk C, Nelson C. Mechanisms of postnatal neurobiological development: implications for human development. Dev Neuropsychol. 2001;19:147–171. doi: 10.1207/S15326942DN1902_2. [DOI] [PubMed] [Google Scholar]
• 24.Wilson MA, Johnston MV, Goldstein GW, Blue ME. Neonatal lead exposure impairs development of rodent barrel field cortex. PNAS. 2000;97:5540–5545. doi: 10.1073/pnas.97.10.5540. [DOI] [PMC free article] [PubMed] [Google Scholar]
• 25.Gunnar M. Stress, nurture and the young brain. Concepts of care: twenty brief papers that point the way toward quality care for infants and toddlers. San Francisco: West Ed (in press).
• 26.Bredy T, Humpartzoomian R, Cain D, Meaney M. Partial reversal of the effect of maternal care on cognitive function through environmental enrichment. Neurosci. 2003;118:571–576. doi: 10.1016/s0306-4522(02)00918-1. [DOI] [PubMed] [Google Scholar]
• 27.Meaney M, Mitchell J, Aitken D. The effects of neonatal handling on the development of the adrenocortical response to stress: implications for neuropathology and cognitive deficits in later life. Psychoneuroendocrinol. 1991;16:85–103. doi: 10.1016/0306-4530(91)90072-2. [DOI] [PubMed] [Google Scholar]
• 28.Rutter M, O'Connor T, English and Romanian Adoptees (ERA) Study Team Are there biological programming effects for psychological development? Findings from a study of Romanian adoptees. Dev Psychol. 2004;40:81–94. doi: 10.1037/0012-1649.40.1.81. [DOI] [PubMed] [Google Scholar]
• 29.Currie J, Thomas D. Early test scores, socioeconomic status and future outcomes. National Bureau of Economic Research; Cambridge: 1999. Working Paper 6943. [Google Scholar]
• 30.Pianta RC, McCoy SJ. The first day of school: the predictive validity of early school screening. J Appl Dev Psychol. 1997;18:1–22. [Google Scholar]
• 31.Feinstein L. Inequality in the early cognitive development of children in the 1970 cohort. Economica. 2003;70:73–97. [Google Scholar]
• 32.Stith AY, Gorman KS, Choudhury N. The effects of psychosocial risk and gender on school attainment in Guatemala. Appl Psychol. 2003;52:614–629. [Google Scholar]
• 33.Gorman KS, Pollitt E. Does schooling buffer the effects of early risk? Child Dev. 1996;67:314–326. [PubMed] [Google Scholar]
• 34.Liddell C, Rae G. Predicting early grade retention: A longitudinal investigation of primary school progress in a sample of rural South African children. Br J Educ Psychol. 2001;71:413–428. doi: 10.1348/000709901158596. [DOI] [PubMed] [Google Scholar]
• 35.Daniels MC, Adair LS. Growth in young Filipino children predicts schooling trajectories through high school. J Nutr. 2004;134:1439–1446. doi: 10.1093/jn/134.6.1439. [DOI] [PubMed] [Google Scholar]
• 36.Mendez MA, Adair LS. Severity and timing of stunting in the first two years of life affect performance on cognitive tests in late childhood. J Nutr. 1999;129:1555–1562. doi: 10.1093/jn/129.8.1555. [DOI] [PubMed] [Google Scholar]
• 37.Walker SP, Chang SM, Powell CA, Grantham-McGregor SM. Effects of early childhood psychosocial stimulation and nutritional supplementation on cognition and education in growth-stunted Jamaican children: prospective cohort study. Lancet. 2005;366:1804–1807. doi: 10.1016/S0140-6736(05)67574-5. [DOI] [PubMed] [Google Scholar]
• 38.Victora CG, Barros FC, Lima RC. The Pelotas birth cohort study, Rio Grande do Sul, Brazil, 1982–2001. Cad Saude Publica, Rio de Janeiro. 2003:1241–1256. doi: 10.1590/s0102-311x2003000500003. [DOI] [PMC free article] [PubMed] [Google Scholar]
• 39.Victora MD, Victora CG, Barros FC. Cross-cultural differences in developmental rates: a comparison between British and Brazilian children. Child Care Health Dev. 1990;16:151–164. doi: 10.1111/j.1365-2214.1990.tb00647.x. [DOI] [PubMed] [Google Scholar]
• 40.Filmer D, Pritchett LH. Estimating wealth effects without expenditure data—or tears: an application to educational enrollments in states of India. Demography. 2001;38:115–132. doi: 10.1353/dem.2001.0003. [DOI] [PubMed] [Google Scholar]
• 41.Pollitt E, Gorman KS, Engle PL, Martorell R, Rivera J. Early supplementary feeding and cognition. Mon Soc Child Dev. 1993;58 [PubMed] [Google Scholar]
• 44.UNESCO . EFA Global Monitoring Report 2005. UNESCO; Paris, France: 2005. [Google Scholar]
• 45.Gonzalez P, Guzman JC, Partelow L. Highlights from the trends in international mathematics and science study TIMSS 2003. US Department of Education; Washington DC: 2004. [Google Scholar]
• 46.Byamugisha A, Ssenabulya F. The SACMEQ II project in Uganda: a study of the conditions of schooling and the quality of education. SACMEQ; Harare, Zimbabwe: 2005. [Google Scholar]
• 47.Chimombo J, Kunje D, Chimuzu T, Mchikoma C. The SACMEQ II project in Malawi: a study of the conditions of schooling and the quality of education. SACMEQ; Harare, Zimbabwe: 2005. [Google Scholar]
• 48.Keitheile M, Mokubung M. The SACMEQ II project in Botswana: a study of the conditions of schooling and the quality of education. SACMEQ; Harare, Zimbabwe: 2005. [Google Scholar]
• 49.Kulpoo D, Soonarane M. The SACMEQ II project in Mauritius: a study of the conditions of schooling and the quality of education. SACMEQ; Harare, Zimbabwe: 2005. [Google Scholar]
• 50.Makuwa D. The SACMEQ II project in Namibia: a study of the conditions of schooling and the quality of education. SACMEQ; Harare, Zimbabwe: 2005. [Google Scholar]
• 51.Moloi M, Strauss J. The SACMEQ II project in South Africa: a study of the conditions of schooling and the quality of education. SACMEQ; Harare, Zimbabwe: 2005. [Google Scholar]
• 52.Mothibeli A, Maema M. The SACMEQ II project in Lesotho: a study of the conditions of schooling and the quality of education. SACMEQ; Harare, Zimbabwe: 2005. [Google Scholar]
• 53.Mrutu AS, Ponera GE, Nkumbi EM. The SACMEQ II project in Tanzania: a study of the conditions of schooling and the quality of education. SACMEQ; Harare, Zimbabwe: 2005. [Google Scholar]
• 54.Nassor SM, Abdalla MS, Salim MM, Said O. The SACMEQ II project in Zanzibar: a study of the conditions of schooling and the quality of education. SACMEQ; Harare, Zimbabwe: 2005. [Google Scholar]
• 55.Onsomu E, Nzomo J, Obiero C. The SACMEQ II project in Kenya: a study of the conditions of schooling and the quality of education. SACMEQ; Harare, Zimbabwe: 2005. [Google Scholar]
• 56.Passos A, Nahara T, Magaza F, Lauchande C. The SACMEQ II project in Mozambique: a study of the conditions of schooling and the quality of education. SACMEQ; Harare, Zimbabwe: 2005. [Google Scholar]
• 57.Shabalala J. The SACMEQ II project in Swaziland: a study of the conditions of schooling and the quality of education. SACMEQ; Harare, Zimbabwe: 2005. [Google Scholar]
• 58.Hamill PV, Drizd TA, Johnson CL, Reed RB, Roche AF. NCHS growth curves for children birth–18 years. United States. Vital Health Stat. 1977;11:1–74. [PubMed] [Google Scholar]
• 59.Bhandari N, Bahl R, Taneja S, de Onis M, Bhan MK. Growth performance of affluent Indian children is similar to that in developed countries. Bull World Health Organ. 2002;80:189–195. [PMC free article] [PubMed] [Google Scholar]
• 60.WHO Multicentre Growth Reference Study Group Assessment of differences in linear growth among populations in the WHO Multicentre Growth Reference Study. Acta Paediatr Suppl. 2006;450:56–65. doi: 10.1111/j.1651-2227.2006.tb02376.x. [DOI] [PubMed] [Google Scholar]
• 61.Shrimpton R, Victoria CG, de Onis M, Lima RC, Blossner M, Clugston G. Worldwide timing of growth faltering: implications for nutritional interventions. Pediatrics. 2001;107:e75. doi: 10.1542/peds.107.5.e75. [DOI] [PubMed] [Google Scholar]
• 62.Martorell R, Schroeder DG, Rivera JA, Kaplowitz HJ. Patterns of linear growth in rural Guatemalan adolescents and children. J Nutr. 1995;125:S1060–S1067. doi: 10.1093/jn/125.suppl_4.1060S. [DOI] [PubMed] [Google Scholar]
• 63.Adair LS. Filipino children exhibit catch-up growth from age 2 to 12 years. J Nutr. 1999;129:1140–1148. doi: 10.1093/jn/129.6.1140. [DOI] [PubMed] [Google Scholar]
• 64.Deaton A. Counting the world's poor: problems and possible solutions. World Bank Res Obs. 2001;16:125–147. [Google Scholar]
• 65.Gordon G, Nandy S, Pantazis C, Pemberton S, Townsend P. Child poverty in the developing world. The Policy Press; Bristol, UK: 2003. [Google Scholar]
• 66.World Bank, World development indicators 2005. World Bank, 2005.
• 67.Chronic Poverty Research Centre . Chronic poverty report 2004–05. University of Manchester; Manchester, UK: 2006. [Google Scholar]
• 68.Hamadani JD, Grantham-McGregor SM. Report of the family care indicators project: Validating the family psychosocial indicators in rural Bangladesh. Report to UNICEF Early Child Development Desk, 2004.
• 69.Baker-Henningham H, Powell C, Walker S, Grantham-McGregor S. Mothers of undernourished Jamaican children have poorer psychosocial functioning and this is associated with stimulation provided in the home. Eur J Clin Nutr. 2003;57:786–792. doi: 10.1038/sj.ejcn.1601611. [DOI] [PubMed] [Google Scholar]
• 70.Schady N, Paxson C. Cognitive development among young children in Ecuador: the roles of health, wealth and parenting. World Bank Policy Research Working Paper 3605, May, 2005. World Bank; Washington DC: 2005. [Google Scholar]
• 71.Richter L, Griesel R, De Wet T. Growing up and going to school: Birth to Ten, children's cognitive and social competence at school entry. In: Richter L, editor. A view of school: preparation for and adjustment to school under rapidly changing social conditions. The Goethe Institute; Johannesburg: 1998. [Google Scholar]
• 72.Espy KA, Molfese VJ, DiLalla LF. Effects of environmental measures on intelligence in young children: growth curve modeling of longitudinal data. Merrill-Palmer Quart. 2001;47:42–73. [Google Scholar]
• 73.Walker SP, Grantham-McGregor SM. Growth and development of West Indian children. Part 2: development. West Indian Med J. 1990;39:12–19. [PubMed] [Google Scholar]
• 74.Lozoff B, Teal SJL. Longitudinal analysis of cognitive and motor effects of iron deficiency in infancy. Pediatr Res. 2004;55:23A. [Google Scholar]
• 75.UNICEF . State of the world's children 2006. UNICEF; New York: 2005. [Google Scholar]
• 76.WHO Global database on child growth and malnutrition. World Health Organization. 2006. http://www.who.int/nutgrowthdb/database/en/ (accessed March 18, 2006)
• 77.Beasley NMR, Hall A, Tomkins AM. The health of enrolled and non enrolled children of school age in Tanga, Tanzania. Acta Trop. 2000;76:223–229. doi: 10.1016/s0001-706x(00)00101-7. [DOI] [PubMed] [Google Scholar]
• 78.Moock PR, Leslie J. Childhood malnutrition and schooling in the Terai region of Nepal. J Dev Econ. 1986;20:33–52. [Google Scholar]
• 79.Brooker S, Hall A, Bundy DAP. Short stature and the age of enrolment in primary school: studies in two African countries. Soc Sci Med. 1999;48:675–682. doi: 10.1016/s0277-9536(98)00382-7. [DOI] [PubMed] [Google Scholar]
• 80.Jamison DT. Child malnutrition and school performance in China. J Dev Econ. 1986;20:299–309. [Google Scholar]
• 81.Clarke N, Grantham-McGregor S, Powell C. Health and nutrition predictors of school failure in Kingston, Jamaica. Ecol Food Nutr. 1990;26:1–11. [Google Scholar]
• 82.Hutchinson SE, Powell CA, Walker SP, Chang SM, Grantham-McGregor SM. Nutrition, anaemia, geohelminth infection and school achievement in rural Jamaican primary school children. Eur J Clin Nutr. 1997;51:729–735. doi: 10.1038/sj.ejcn.1600473. [DOI] [PubMed] [Google Scholar]
• 83.Agarwal DK, Upadhyay SK, Tripathi AM, Agarwal KN. Nutritional status, physical work capacity and mental function in school children. Nutritional Foundation of India, 1987. Scientific Report No. 6.
• 84.Florencio C. Nutrition, health and other determinants of academic achievement and school-related behavior of grades one to six pupils. University of the Philippines; Quezan City, Philippines: 1988. [Google Scholar]
• 85.Steegmann AT, Datar FA, Steegmann RM. Physical size, school performance and visual-motor maturity in the Philippines. Am J Hum Biol. 1992;4:247–252. doi: 10.1002/ajhb.1310040209. [DOI] [PubMed] [Google Scholar]
• 86.Glewwe P, Jacoby HG, King EM. Early childhood nutrition and academic achievement: a longitudinal analysis. J Public Econ. 2001;81:345–368. [Google Scholar]
• 87.Shariff ZM, Bond JT, Johnson NE. Nutrition and educational achievement of urban primary schoolchildren in Malaysia. Asia Pacific J Clin Nutr. 2000;9:264–273. doi: 10.1046/j.1440-6047.2000.00191.x. [DOI] [PubMed] [Google Scholar]
• 88.Partnership for Child Development An association between chronic undernutrtition and educational test scores in Vietnamese children. Eur J Clin Nutr. 2001;55:801–804. doi: 10.1038/sj.ejcn.1601229. [DOI] [PubMed] [Google Scholar]
• 89.Brito GNO, de Onis M. Growth status, behavior and neuropsychological performance. Arquivos Neuro-Psiquiatr. 2004;62:949–954. doi: 10.1590/s0004-282x2004000600004. [DOI] [PubMed] [Google Scholar]
• 90.Ozmert EN, Yurdakok K, Soysal S. Relationship between physical, environmental and sociodemographic factors and school performance in primary schoolchildren. J Trop Pediatr. 2005;51:25–32. doi: 10.1093/tropej/fmh070. [DOI] [PubMed] [Google Scholar]
• 91.Bogin B, Macvean RB. The relationship of socioeconomic-status and sex to body size, skeletal maturation, and cognitive status of Guatemala City schoolchildren. Child Dev. 1983;54:115–128. [PubMed] [Google Scholar]
• 92.Sigman M, Neumann C, Jansen AA, Bwibo N. Cognitive abilities of Kenyan children in relation to nutrition, family characteristics, and education. Child Dev. 1989;60:1463–1474. [PubMed] [Google Scholar]
• 93.Johnston FE, Low SM, de Baessa Y, Macvean RB. Interaction of nutritional and socioeconomic status as determinants of cognitive development in disadvantaged urban Guatemalan children. Am J Phys Anthropol. 1987;73:501–506. doi: 10.1002/ajpa.1330730412. [DOI] [PubMed] [Google Scholar]
• 94.Webb KE, Horton NJ, Katz DL. Parental IQ and cognitive development of malnourished Indonesian children. Euro J Clin Nutr. 2005;59:618–620. doi: 10.1038/sj.ejcn.1602103. [DOI] [PubMed] [Google Scholar]
• 95.Young Lives Justification of the content of the 7·5–8·5 year old questionnaire. Young Lives: an international study of childhood poverty. 2002. http://www.younglives.org.uk/ (accessed March 18, 2006)
• 96.Ivanovic DM, Perez HT, Olivares MD, Diaz NS, Leyton BD, Ivanovic RM. Scholastic achievement: a multivariate analysis of nutritional, intellectual, socioeconomic, sociocultural, familial, and demographic variables in Chilean shool-aged children. Nutrition. 2004;20:878–889. doi: 10.1016/j.nut.2004.06.009. [DOI] [PubMed] [Google Scholar]
• 97.Cueto S. Height, weight, and education achievement in rural Peru. Food Nutr Bull. 2005;26(2 suppl 2):S251–S260. doi: 10.1177/15648265050262S216. [DOI] [PubMed] [Google Scholar]
• 98.Glewwe P, Jacoby H. An economic analysis of delayed primary school enrollment in a low income country: the role of early childhood nutrition. Rev Econ Stat. 1995;77:156–169. [Google Scholar]
• 99.Popkin B, Lim Ybanez M. Nutrition and school achievement. Soc Sci Med. 1982;16:53–61. doi: 10.1016/0277-9536(82)90423-3. [DOI] [PubMed] [Google Scholar]
• 100.Lasky RE, Klein RE, Yarbrough C, Engle PL, Lechtig A, Martorell R. The relationship between physical growth and infant behavioral development in rural Guatemala. Child Dev. 1981;52:219–226. [PubMed] [Google Scholar]
• 101.Powell CA, Grantham-Mcgregor S. The ecology of nutritional status and development in young children in Kingston, Jamaica. Am J Clin Nutr. 1985;41:1322–1331. doi: 10.1093/ajcn/41.6.1322. [DOI] [PubMed] [Google Scholar]
• 102.Monckeberg F. Malnutrition and mental capacity. In: Organization PAH, editor. Nutrition, the nervous system and behaviour, Scientific Publication No 251. PAHO; Washington DC: 1972. pp. 48–54. [Google Scholar]
• 103.Sigman M, Neumann C, Baksh M, Bwibo N, McDonald MA. Relationship between nutrition and development in Kenyan toddlers. J Pediatr. 1989;115:357–364. doi: 10.1016/s0022-3476(89)80832-7. [DOI] [PubMed] [Google Scholar]
• 104.Kariger PK, Stoltzfus RJ, Olney D. Iron deficiency and physical growth predict attainment of walking but not crawling in poorly nourished Zanzibari infants. J Nutr. 2005;135:814–819. doi: 10.1093/jn/135.4.814. [DOI] [PubMed] [Google Scholar]
• 105.Siegel EH, Stoltzfus RJ, Kariger PK. Growth indices, anemia, and diet independently predict motor milestone acquisition of infants in South Central Nepal. J Nutr. 2005;135:2840–2844. doi: 10.1093/jn/135.12.2840. [DOI] [PMC free article] [PubMed] [Google Scholar]
• 106.Bhargava A. Modeling the effects of maternal nutritional status and socioeconomic variables on the anthropometric and psychological indicators of Kenyan infants from age 0–6 months. Am J Phys Anthropol. 2000;111:89–104. doi: 10.1002/(SICI)1096-8644(200001)111:1<89::AID-AJPA6>3.0.CO;2-X. [DOI] [PubMed] [Google Scholar]
• 107.Vazir S, Naidu AN, Vidyasagar P. Nutritional status, psychosocial development and the home environment of Indian rural children. Indian Pediatr. 1998;35:959–966. [PubMed] [Google Scholar]
• 108.Drewett R, Wolke D, Asefa M, Kaba M, Tessema F. Malnutrition and mental development: is there a sensitive period? A nested case-control study. J Child Psychol Psychiatr. 2001;42:181–187. doi: 10.1111/1469-7610.00709. [DOI] [PubMed] [Google Scholar]
• 109.Hamadani JD, Fuchs GJ, Osendarp SJ, Khatun F, Huda SN, Grantham-McGregor SM. Randomized controlled trial of the effect of zinc supplementation on the mental development of Bangladeshi infants. Am J Clin Nutr. 2001;74:381–386. doi: 10.1093/ajcn/74.3.381. [DOI] [PubMed] [Google Scholar]
• 110.Hamadani JD, Fuchs GJ, Osendarp SJ, Huda SN, Grantham-McGregor SM. Zinc supplementation during pregnancy and effects on mental development and behaviour of infants: a follow-up study. Lancet. 2002;360:290–294. doi: 10.1016/S0140-6736(02)09551-X. [DOI] [PubMed] [Google Scholar]
• 111.Cheung YB, Yip PSF, Karlberg JPE. Fetal growth, early postnatal growth and motor development in Pakistani infants. Int J Epidemiol. 2001;30:66–72. doi: 10.1093/ije/30.1.66. [DOI] [PubMed] [Google Scholar]
• 112.Kuklina EV, Ramakrishnan U, Stein AD, Barnhart HH, Martorell R. Growth and diet quality are associated with the attainment of walking in rural Guatemalan infants. J Nutr. 2004;134:3296–3300. doi: 10.1093/jn/134.12.3296. [DOI] [PubMed] [Google Scholar]
• 113.Berkman DS, Lescano AG, Gilman RH, Lopez SL, Black MM. Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet. 2002;359:564–571. doi: 10.1016/S0140-6736(02)07744-9. [DOI] [PubMed] [Google Scholar]
• 114.Martorell R, Rivera J, Kaplowitz J, Pollitt E. Long term consequences of growth retardation during early childhood. In: Hernandez M, Argenta J, editors. Human growth: basic and clinical aspects. Elsevier; Amsterdam: 1992. pp. 143–149. [Google Scholar]
• 115.Behrman JR, Hoddinott J, Maluccio JA, et al. What determines adult cognitive skills? Impacts of pre-school, schooling and post-school experiences in Guatemala. 2005. Working draft October 2005.
• 116.Cheung YB. Growth and cognitive function of Indonesian children: Zero-inflated proportion models. Stat Med. 2006;25:3011–3022. doi: 10.1002/sim.2467. [DOI] [PubMed] [Google Scholar]
• 117.Richter LM, Yach D, Cameron N, Griesel RD, De Wet T. Enrolment into Birth to Ten (BTT): population and sample characteristics. Paediatr Perinat Epidemiol. 1995;9:109–120. doi: 10.1111/j.1365-3016.1995.tb00124.x. [DOI] [PubMed] [Google Scholar]
• 118.Wechsler D. Wechsler adult intelligence scale manual. Psychological Corporation; New York: 1955. [Google Scholar]
• 119.Wechsler D. Wechsler Intelligence Scales for Children-Revised. The Psychological Corporation, Harcourt Brace Jovanovich Inc; San Antonio: 1974. [Google Scholar]
• 120.Raven J, Raven J, Court J. Coloured Progressive Matrices. Information Press; Oxford: 1998. [Google Scholar]
• 121.Alderman H, Behrman JR, Khan S, Ross DR, Sabot R. The income gap in cognitive skills in rural Pakistan. Econ Dev Cult Change. 1997;46:97–122. [Google Scholar]
• 122.Behrman JR, Knowles JC. Household income and child schooling in Vietnam. World Bank Econ Rev. 1999;13:211–256. [Google Scholar]
• 123.Filmer D, Pritchett L. The effect of household wealth on educational attainment: evidence from 35 countries. Pop Dev Rev. 1999;25:85–120. [Google Scholar]
• 124.Aldaz-Carroll E, Moran R. Escaping the poverty trap in Latin America: the role of family factors. Cuadernos Econom. 2001;38:155–190. [Google Scholar]
• 125.Baker-Henningham H, Walker S, Chang-Lopez S. Special education needs study: end of phase 1 report. Department of Educational Studies/Office of the Principal, University of the West Indies; Kingston, Jamaica: 2006. [Google Scholar]
• 126.Kirksey A, Wachs TD, Srinath U. Relation of maternal zinc nutrition to pregnancy outcome and early infant development in an Egyptian village. Am J Clin Nutr. 1994;60:782–792. doi: 10.1093/ajcn/60.5.782. [DOI] [PubMed] [Google Scholar]
• 127.Lima MC, Eickmann SH, Lima ACV. Determinants of mental and motor development at 12 months in a low income population: a cohort study in northeast Brazil. Acta Paediatr. 2004;93:969–975. doi: 10.1111/j.1651-2227.2004.tb18257.x. [DOI] [PubMed] [Google Scholar]
• 128.Black MM, Sazawal S, Black RE, Khosla S, Kumar J, Menon V. Cognitive and motor development among small for gestational age infants: impact of zinc supplementation, birth weight, and caregiving practices. Pediatr. 2004;113:1297–1305. doi: 10.1542/peds.113.5.1297. [DOI] [PMC free article] [PubMed] [Google Scholar]
• 129.Basilio CS, Puccini RF, da Silva EMK, Pedromônico MRM. Living conditions and receptive vocabulary of children aged two to five years. Rev Saude Publica. 2005;39:725–730. doi: 10.1590/s0034-89102005000500005. [DOI] [PubMed] [Google Scholar]
• 130.Sigman M, McDonald MA, Neumann C, Bwibo N. Prediction of cognitive competence in Kenyan children from toddler nutrition, family characteristics and abilities. J Child Psychol Psychiat. 1991;32:307–320. doi: 10.1111/j.1469-7610.1991.tb00309.x. [DOI] [PubMed] [Google Scholar]
• 131.Stein AD, Behrman JR, DiGirolamo A. Schooling, educational achievement and cognitive functioning among young Guatemalan adults. Food Nutr Bull. 2005;26:S46–S54. doi: 10.1177/15648265050262S105. [DOI] [PubMed] [Google Scholar]
• 132.Chen S, Ravallion M. How have the world's poorest fared since the early 1980s? World Bank Policy Research Working Paper (WPS 3341) World Bank; Washington: 2004. [Google Scholar]
• 133.de Onis M, Blossner M, Borghi E, Morris R, Frongillo EA. Methodology for estimating regional and global trends of child malnutrition. Int J Epidemiol. 2004;33:1260–1270. doi: 10.1093/ije/dyh202. [DOI] [PubMed] [Google Scholar]
• 134.UNICEF Multiple indicator cluster surveys 2. UNICEF. 2006. http://www.childinfo.org/MICS2/MICSDataSet.htm (accessed Feb 24, 2006)
• 135.de Onis M, Onyango A, Borghi E, Siyam A, Pinol A. WHO child growth standards: length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: methods and development. World Health Organization; Geneva: 2006. [Google Scholar]
• 136.WHO International statistical classification of diseases and related health problems, 10th revision, version for 2006. World Health Organization. 2006. http://www3.who/int/icd/currentversion/fr-icd.htm (accessed July 18, 2006)
• 137.Psacharopoulos G, Patrinos H. Returns to investment in education: a further update. Educ Econ. 2004;12:111–134. [Google Scholar]
• 138.Duflo E. Schooling and labor market consequences of school construction in Indonesia: evidence from an unusual policy experiment. Am Econ Rev. 2001;91:795–814. [Google Scholar]

Uncited references

• 42.Thorndike RL, Hagen E, Sattler J. Stanford-Binet Intelligence Scale. 4th edn. Riverside Publishing; Itasca: 1986. [Google Scholar]
• 43.Griffiths R. The abilities of young children: a comprehensive system of mental measurement for the first eight years of life. Child Development Research Centre; London, UK: 1970. [Google Scholar]

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Achievement in reading for sixth grade students in 12 African countries

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