Peer-reviewed Article Summaries
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Lancet 2011; 378: 1325–38
Published Online September 23, 2011 DOI:10.1016/S0140- 6736(11)60555-2
See Editorial page 1276
See Comment page 1277
This is the fi rst in a Series of two reports about child development
Tropical Medicine Research Institute, The University of the West Indies, Kingston, Jamaica (Prof S P Walker PhD, H Baker-Henningham PhD, S M Chang PhD, C A Powell PhD); Department of Psychological Sciences, Purdue University, West Lafayette, IN, USA (Prof T D Wachs PhD); Institute of Child Health, London, UK (Prof S Grantham-McGregor MD); Department of Pediatrics, University of Maryland, College Park, MD, USA (Prof M M Black PhD); Children’s Hospital Boston/Harvard Medical School, Boston, MA, USA (Prof C A Nelson PhD); Department of Nutrition, University of California, Davis, CA, USA (S L Huff man ScD); Child Development Unit, ICDDR,B, Dhaka, Bangladesh (J D Hamadani PhD); Center for Human Growth and Development, Department of Pediatrics, University of Michigan, Ann Arbor, MI, USA (Prof B Lozoff MD); Caribbean Child Development Centre, The University of the West Indies, Open Campus, Jamaica (Prof J M Meeks Gardner PhD); Institute of Psychology, Health, and Society, University of Liverpool, Liverpool, UK (Prof A Rahman PhD); and Human Sciences Research Council & University of the Witwatersrand, South Africa (Prof L Richter PhD)
Child Development 1
Inequality in early childhood: risk and protective factors for early child development Susan P Walker, Theodore D Wachs, Sally Grantham-McGregor, Maureen M Black, Charles A Nelson, Sandra L Huff man, Helen Baker-Henningham, Susan M Chang, Jena D Hamadani, Betsy Lozoff , Julie M Meeks Gardner, Christine A Powell, Atif Rahman, Linda Richter
Inequality between and within populations has origins in adverse early experiences. Developmental neuroscience shows how early biological and psychosocial experiences aff ect brain development. We previously identifi ed inadequate cognitive stimulation, stunting, iodine defi ciency, and iron-defi ciency anaemia as key risks that prevent millions of young children from attaining their developmental potential. Recent research emphasises the importance of these risks, strengthens the evidence for other risk factors including intrauterine growth restriction, malaria, lead exposure, HIV infection, maternal depression, institutionalisation, and exposure to societal violence, and identifi es protective factors such as breastfeeding and maternal education. Evidence on risks resulting from prenatal maternal nutrition, maternal stress, and families aff ected with HIV is emerging. Interventions are urgently needed to reduce children’s risk exposure and to promote development in aff ected children. Our goal is to provide information to help the setting of priorities for early child development programmes and policies to benefi t the world’s poorest children and reduce persistent inequalities.
Introduction In a 2007 Series in The Lancet we estimated that more than 200 million children younger than 5 years from low-income and middle-income countries were not attaining their developmental potential, primarily because of poverty, nutritional defi ciencies, and inadequate learning opportunities.1,2 Economic reces- sion and climate change will probably increase the number of children aff ected.3,4 Biological and psycho- social risk factors associated with poverty lead to inequalities in early child development, which undermine educational attainment and adult product- ivity, thereby perpetuating the poverty cycle.5 In this Series, we review new evidence on the mechanisms and
causes of developmental inequality and economic implications and strategies to promote early child development. In this report we summarise evidence from developmental neuroscience on how experiences in early life aff ect the structure and functioning of the brain, and subsequent child development. We review evidence on risks and protective factors for development, updating evidence on previously identifi ed risks (panel 1),1 and highlight risks not previously identifi ed. Our focus is on modifi able risks that aff ect large numbers of children younger than 5 years in low- income and middle-income countries.
Search strategy and selection criteria
We searched relevant databases (eg, PubMed, PsychInfo, Cochrane Review) with multiple search terms for articles published since 2005. The search terms we used were linked to each of the risk or protective factors: “child development”, “child behaviour”, “infant behaviour”, “cognition”, “social”, “emotional”, “intelligence”, “language”, and “motor development”. We searched citation lists of articles retrieved and review articles published since the last Series for further references. We included earlier key publications in which the risk or protective factor was not reviewed in the previous Series. We include only risk and protective factors that can be modifi ed by interventions or public policy and which aff ect large numbers of children younger than 5 years in low-income and middle-income countries. We consider exposures in utero to age 5 years and focus on research done in low-income and middle-income countries. Although many of the risk and protective factors we considered are also relevant to children’s health outcomes, we focus on children’s cognitive, motor, and social–emotional development.
Key messages
• Exposure to biological and psychosocial risks aff ects the developing brain and compromises the development of children
• Inequalities in child development begin prenatally and in the fi rst years of life
• With cumulative exposure to developmental risks, disparities widen and trajectories become more fi rmly established
• Reducing inequalities requires early integrated interventions that target the many risks to which children in a particular setting are exposed
• The most eff ective and cost-effi cient time to prevent inequalities is early in life before trajectories have been fi rmly established
• Action or lack of action will have lifetime consequences for adult functioning, for the care of the next generation, and for the wellbeing of societies
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Correspondence to: Prof Susan P Walker, Tropical Medicine Research Institute, Epidemiology Research Unit,
The University of the West Indies, Mona, Kingston, 7, Jamaica susan.walker@uwimona.
edu.jm
Risk, stress, and brain development The foundations of brain architecture are laid down early in life through dynamic interactions of genetic, biological, and psychosocial infl uences, and child behaviour. Biological and psychosocial infl uences aff ect the timing and pattern of genetic expression, which can alter brain structure and function,6 and behaviour.7 Through bidirectional eff ects, children’s behaviour aff ects brain development directly and by modifying the eff ects of biological and psychosocial infl uences.8
Childhood risks associated with poverty, such as lack of stimulation or excessive stress, aff ect brain development, result in dysregulation of the hypothalamic–pituitary– adrenocortical system,9 and change electrical activity of the brain related to effi ciency of cognitive processing.10 The infl uence of risks can begin prenatally because the fetal brain can be infl uenced by exogenous factors that produce maternal stress.11 At present there is insuffi cient evidence from research in human beings to establish if the eff ects on hypothalamic–pituitary–adrenocortical regulation are reversible.12
Three translational processes infl uence how risk factors and stress aff ect brain and behavioural development: the extent and nature of defi cits depend on timing, co-occurring and cumulative infl uences, and diff erential reactivity (fi gure 1 and table 1). Risks often co-occur and persist, leading to exposure to multiple and cumulative risks. For example, maternal depression increases risk of low birthweight (LBW; additional references in web appendix pp 1–5), stunting,13 and insecure attachment.14 Because of diff erential reactivity, the eff ect of risks on behaviour might vary by individual or environmental characteristics.
Maternal nutrition There is maternal undernutrition (body-mass index <18·5 kg/m²) in 10–19% of women in most low-income and middle-income countries, with higher prevalence in sub-Saharan Africa and south Asia. Maternal pre- pregnancy body-mass index and weight gain during pregnancy predict birthweight, and balanced energy– protein supplementation benefi ts birthweight and reduces births that are small for their gestational age. However, there is little information on associations between maternal nutritional status and child develop- ment. Pre-pregnancy weight and weight gain in Jamaican women that were mostly adequately nourished were not
associated with child cognition at age 7 years.15 In Bangladesh, infants of undernourished mothers had poorer problem-solving ability at 7 months,16 and ability was better in infants of mothers given food supplements early rather than later in pregnancy. By age 18 months, no eff ects of maternal undernutrition or supplementation were identifi ed.17 Analyses of the Dutch (1944–45) and Chinese (1959–61) famines suggest that prenatal nutritional defi cits might have long-term eff ects on adult mental health. There is a need for research on the eff ect of food supplementation before and during pregnancy on child development.
About 42% of pregnant women in low-income and middle-income countries are anaemic, and, of these, 60% are iron defi cient; however, there is little information on perinatal iron defi ciency and child development. Lower maternal haemoglobin and neonatal ferritin predicted lower intra-individual variability in temperament-like behaviours in Peruvian infants that suggested diminished responsiveness.18 In South Africa, maternal iron- defi ciency anaemia at 6–10 weeks post partum was associated with lower maternal sensitivity and child responsiveness.19 Although both disorders improved after treatment with iron, infant development was delayed at age 9 months.20
Meta-analyses of 12 randomised controlled trials from low-income and middle-income countries show that supplementation with multiple micronutrients in pregnancy leads to increased birthweight. Trials of supplementation with multiple micronutrients during pregnancy in Bangladesh and in pregnant women in Tanzania infected with HIV suggest small benefi ts to infants’ motor development,16,21 and to mental develop- ment in China,22 compared with iron and folic acid alone. In Peru, zinc supplementation during pregnancy had no eff ect on children’s cognitive, social, or behavioural development at ages 4–5 years.23 In Nepal, children whose mothers received iron and folate during pregnancy had better intelligence quotient (IQ), executive, and motor functioning than the placebo group at ages 7–9 years;24 provision of multiple micronutrients or iron plus folate plus zinc had no benefi ts, possibly because of zinc inhibition of iron absorption.
Inadequate intakes of ω3 fatty acids (including α-linoleic acid, docosahexaenoic acid [DHA], eicosapentaenoic acid) have been reported in pregnant women in some low-income and middle-income countries. In high- income countries, trials of fi sh oil, DHA, or DHA and eicosapentaenoic acid showed that infants born to supplemented mothers had improvements in visual acuity,25 attention,26 and aspects of cognitive perfor- mance.27 Supplementation with ω3 fatty acids and micro- nutrients benefi ted birthweight and length and reduced very early preterm births in Chile. In Mexico, supple- mentation with ω3 fatty acids benefi ted birthweight and head size in primigravid women only. Information is needed on possible benefi ts to infant development.
Panel 1: Previously identifi ed priority risk factors
• Key risks: inadequate cognitive stimulation, linear growth retardation (stunting), iodine defi ciency, and iron-defi ciency anaemia
• Other priority risks: intrauterine growth restriction, malaria, lead exposure, maternal depressive symptoms, and exposure to violence
See Online for webappendix
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Infant and child nutrition In low-income and middle-income countries, 16% of births are LBW with rates as great as 27% in south Asia, most of these births being intrauterine growth restriction (IUGR)-LBW. A Guatemalan study28 showed associations between birth size adjusted for gestational age and development at 6 and 24 months, supporting earlier conclusions that IUGR is associated with early developmental risk.1
Evidence for longer-term eff ects of IUGR is less consistent. Signifi cant eff ects of birthweight unadjusted for gestational age were identifi ed on IQ at age 5 years29 and on highest school grade achieved.30 However, contributions of prematurity cannot be estimated. No signifi cant diff erences were identifi ed between term LBW and normal birthweight children in IQ or parent- reported behaviour at 6 years in Jamaica,31 or at 8 years in Brazil,32 and no diff erence in self-reported behaviour at 12 years in South Africa.33 By contrast, a large study in Taiwan34 reported signifi cant small defi cits in academic achievement of term LBW at 15 years. More evidence is needed on long-term eff ects of IUGR in low-income and middle-income countries on IQ, and specifi c cognitive and social skills.
About 39% of infants aged 0–6 months in low-income and middle-income countries are exclusively breastfed, with wide variations in duration of exclusive breastfeeding between countries. In a large cluster-randomised trial in Belarus,35 clinics were assigned to breastfeeding pro- motion or usual care. Intervention increased exclusive breastfeeding at 3 months and any breastfeeding up to 12 months. At age 6·5 years, intervention children had signifi cantly higher scores on verbal and full-scale IQ and teacher ratings for reading and writing. No benefi ts were identifi ed for child behaviour.36 In Brazil, boys breastfed for at least 9 months attained 0·5–0·8 school grades more by 18 years than boys breastfed for less than 1 month. Regression of grade level attained on adult income in this population suggests this diff erence corresponds to a 10–15% diff erence in income.37 These fi ndings strengthen the evidence for benefi ts of breastfeeding to development and educational attainment.
In high-income countries, formula-fed infants given DHA supplemented formula had better visual acuity, with greater benefi ts for preterm infants. There is little information on essential fatty-acid intake or the develop- mental eff ect in infants and children from low-income and middle-income countries. In Turkey, improve ments in brainstem auditory evoked potentials were noted in infants randomly assigned to receive DHA-supplemented formula compared with infants receiving non-supple- mented formula.38 Consumption of comple mentary foods fortifi ed with micronutrients and essential fatty acids was associated with improved motor development in Ghana and China.39,40 Although it is unclear which nutrients were responsible for the benefi ts, supplementation with essential fatty acids and micronutrients resulted in earlier
walking compared with micronutrients alone;39 however, the groups also diff ered in energy intake.
Linear growth retardation or stunting is estimated to aff ect 34% of children younger than 5 years in low-income and middle-income countries. Consistent with previous evidence, new longitudinal studies from Brazil, India, Peru, and Vietnam show associations between early height-for-age and cognitive or language ability at 5 years.
Height before 6 years was related to age at school enrolment and grades attained by late adolescence in Zimbabwe.41 New information also extends the long-term outcomes associated with stunting, including reduced likelihood of formal employment at age 20–22 years in the Philippines42 and poorer psychological functioning in Jamaican adolescents.43
Timing of growth faltering seems important. In Guatemala, growth and development were related up to age 24 months but not from 24 to 36 months.28 Pooled analyses of fi ve longitudinal studies identifi ed that a 1 SD increase in weight gain from birth to 24 months was associated with increased schooling (0·43 years) and inversely related to grade failures, whereas growth from
Figure 1: Pathways linking poverty to developmental inequities (A) Timing, dose, and diff erential reactivity infl uence how individual exposure to risk and protective factors translate into individual diff erences in brain function and structure. (B) Brain structure and function infl uence the degree of diff erential reactivity shown. (C) Timing and dose of exposure, and diff erential reactivity moderate the eff ect of risk and protective factors upon child development.
Risks
Translational processes: timing, dose, differential reactivity
Protective factors
Family poverty
CNS, neurotransmitters, stress-linked autonomic and hormonal endocrine systems
Child developmental inequalities
(A)
(B)
(C)
(C)
+
–
+
–
Examples*
Timing: extrinsic and environmental infl uences have maximum eff ect on brain and behavioural development during specifi c ages (sensitive periods)
The infant–caregiver relationship depends on the quality and availability of caregiving early in life, the same period that is sensitive to the eff ect of iron defi ciency on myelination and density of dopamine receptors
Co-occurring or cumulative infl uences (dose): risk and protective factors that cumulate during a sensitive period or over time are potent adverse (risk) or facilitative (protective) infl uences on biological and behavioural development
When stress is cumulative or severe, the risk of adverse long-term physiological and behavioural consequences is substantially increased; early cumulative exposure to stress might compromise children’s ability to benefi t from supportive environments, or increase their susceptibility to later stressors
Diff erential reactivity: the eff ect of risk and protective factors on brain and behavioural development can be moderated by child and contextual characteristics
Reactivity to risks varies depending on the presence or absence of specifi c alleles, child characteristics such as temperament, and contextual characteristics such as social support
*References in the webappendix p 1.
Table 1: Translational processes underlying the eff ect of risk exposure on brain and behavioural development
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2 to 4 years had little aff ect.30 Duration might also change the eff ect because Peruvian children stunted at age 6–18 months, but not at 4·5–6 years, did not diff er from children who were not stunted at either age in vocabulary and quantitative test scores at 4·5–6 years. Children stunted at both ages had signifi cantly lower scores. The timing of catch-up growth is unknown and might have happened within the fi rst 2 years of life.44
Previous randomised controlled trials of macronutrient supplementation to promote better growth consistently showed concurrent developmental benefi ts.1 Follow-up of a cluster-randomised trial in Guatemala showed benefi ts to reading comprehension and reasoning at 25–42 years in participants supplemented from birth to 24 months, but not those supplemented later.45 Men supplemented throughout the fi rst 3 years earned higher hourly wages.46 These fi ndings highlight the importance of adequate nutrition early in life.
Several studies reported previously unrecognised behavioural or neurophysiological alterations with iron- defi ciency anaemia in infancy (webappendix pp 9–28). Studies in Chile, India, and Mexico identifi ed electro- physiological evidence of delayed brain maturation in infants with iron-defi ciency anaemia. Sleep duration improved with iron plus folic acid or zinc supplementation, but not both, in trials in Zanzibar and Nepal.47 However, sleep-state organisation was altered in Chilean children aged 4 years despite treatment for iron-defi ciency anaemia in infancy.48 Additional evidence from studies in Chile, India, Mexico, and Zanzibar showed poorer cognitive, motor, and social–emotional development associated with iron-defi ciency anaemia in infancy, or the preschool period. Social–emotional development improved in Chilean infants with iron-defi ciency anaemia who received home visitation to promote development, but remained lower than that of non-anaemic infants. Without home visitation social–emotional development declined in infants with iron-defi ciency anaemia.49
Costa Rican adolescents who had chronic, severe iron defi ciency with or without anaemia in infancy showed no catch-up in motor development despite iron therapy in infancy,50 poorer executive functioning and recognition memory at age 19 years,51 and more internalising and externalising behaviour problems in childhood and adolescence.52 A study of fortifi cation of complementary feeding in China noted infants whose anaemia did not correct within 6 months had lower IQ at age 6 years than those whose anaemia resolved.40
In addition to iron, many other micronutrients are defi cient in children in low-income and middle-income countries including zinc, vitamins A, B12, D, E, ribofl avin, and iodine in some regions. Six randomised and one non-randomised trial of supplementation with multiple micronutrients or fortifi cation included three or more micronutrients and assessed development in children younger than 5 years (webappendix pp 29–37). Five of seven studies showed benefi ts to motor development.
Studies from Bangladesh and India assessing mental development did not identify any benefi ts,53,54 and one from China identifi ed small benefi ts for mental development at 24 months and for IQ at 6 years.40 There are insuffi cient data to establish whether supplementation with multiple micronutrients is more eff ective than iron alone in improving development.
Infectious diseases Previous evidence of the eff ect of diarrhoea on child development was inconclusive. Additional studies in Brazil noted associations between the number of diarrhoea episodes before age 2 years, late school entry,55 defi cits in semantic fl uency, and verbal learning,56 adjusting for socioeconomic status and present nutritional status. Adjustment for stunting before age 2 attenuates the association between diarrhoea and intellectual performance.29 A multicountry study showed that each episode of diarrhoea in the fi rst 2 years of life contributes to stunting,57 suggesting that associations between diarrhoea early in life and school-age performance might be through the same processes that cause stunting.
1·2 billion people are at risk of malaria, with children younger than 5 years at greatest risk. Cerebral or severe malaria can have serious neurological sequelae including seizures, and language and cognitive defi cits.1,58 In Uganda, cognitive training interventions improved the function of aff ected children.59
New evidence suggests that repeated uncomplicated attacks and asymptomatic parasitaemia (experienced by millions of children annually) also aff ect children’s development. In a cross-country analysis controlling for education quality and other confounders, grade repetition and primary school completion rates were related to malaria exposure.60 Longitudinal studies with school- aged children from Brazil and Mali have shown associations between attacks of clinical malaria or asymptomatic parasitaemia and poorer cognitive scores and academic performance. Randomised clinical trials of chemoprophylaxis in schoolchildren showed signifi cant benefi ts to language, mathematics, and attendance in Sri Lanka,61 and to attention in Kenya.62
There are fewer studies with children younger than 5 years. A history of malaria attacks was associated with poorer cognitive function at school entry in Sri Lanka,63 and there were inconsistent associations between parasitaemia and activity and exploration in toddlers in Zanzibar.64 Chemoprophylaxis in young children in The Gambia had later benefi ts for grades attained65 but not cognitive function, although duration of intervention was related to cognitive function. Although most data come from studies of school-aged children, malaria attacks are more common and severe in younger children, and cognitive eff ects might be worse. Despite progress in control programmes, in 18 African countries surveyed only 23% of children younger than 5 years and
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27% of pregnant women were sleeping under insecticide- treated nets.
Most studies investigating other parasitic infections and child cognitive or social–emotional performance involve school-age children. The few studies with young children are inconclusive.1 Although one additional study from Brazil29 showed an association between the number of parasitic infections at 1–3 years and lower IQ at 5 years, fi ndings were not signifi cant after covariate control. Evidence is insuffi cient to establish if early parasitic infections aff ect child development.
An estimated 2·1 million children younger than 15 years are living with HIV; however, only 28% of children in low-income and middle-income countries who need antiretroviral drugs receive them. HIV infection aff ects brain development, leading to cognitive impairments.66 Detrimental eff ects of HIV infection on neurocognitive development were identifi ed in 36 of 43 studies from low-income, middle-income, and high- income countries.67 We summarise in the webappendix (pp 33–37) studies of the development of children younger than 5 years infected with HIV from low-income and middle-income countries. Compared with uninfected children, children infected with HIV had signifi cantly lower motor and mental development scores in most studies. Eff ects are accentuated by associated illnesses, poor nutritional status, and adverse living conditions, including caregiver stress, illness, and death (co- occurrence or cumulative infl uences).
In US studies, highly active antiretroviral therapy (HAART) has led to reduced rates of progressive HIV encephalopathy68 and some benefi ts to development.69 Cognitive function did not change after short-term treatment (6 months) in South African children;70 however, benefi ts to motor and cognitive development were noted after 1 year in the Democratic Republic of the Congo with greater benefi ts in younger children.71 There is an urgent need for increased access to treatment for infected children in low-income and middle-income countries and further assessment of the eff ect of early treatment on development.
Cognitive and motor defi cits have been reported in HIV-exposed uninfected children in low-income and middle-income countries including the Democratic Republic of the Congo72 and Thailand.73 However, co- varying risks such as family poverty and non-parental caregivers were also increased and other studies have not identifi ed defi cits (webappendix pp 33–37). Many uninfected children are aff ected by parental HIV, which can increase exposure to developmental risks such as poverty,74 disrupted caregiving,75 and abandonment.76 In South Africa, young children in aff ected households with caregiver illness or death were at risk for bullying, mental health problems,77 and abuse,74 and in Rwanda for emotional and behavioural problems.78 The restricted fi nancial and social support available to non-parental caregivers further challenges the wellbeing of orphans.79
Environmental toxins Children might be exposed to environmental toxins prenatally—through maternal exposure—and post- natally— through breastmilk, food, water, house dust, or soil. We previously identifi ed lead as a risk factor for young children from low-income and middle-income countries.1 Recent evidence from Poland has shown that prenatal exposure to very low concentrations of lead (<5 μg/dL) can result in poor mental development in young children.80
Evidence from low-income and middle-income countries on the eff ect of other toxins on early child development is inconsistent or sparse (webappendix pp 38–39). Evidence from China shows that arsenic exposure can compromise cognition in older children;81 however, studies from Bangladesh have not identifi ed signifi cant associations between arsenic exposure and mental development up to age 2 years.17 Prenatal exposure to mercury has been linked to low cognitive performance in infancy and early childhood in Brazil,82 but studies from the Seychelles report weak or inconsistent eff ects,83 or no eff ects.84 In Ecuador, prenatal exposure to pesticides was signifi cantly associated with poor communication and motor skills;85 however, associations with later development were weaker,85 or non-signifi cant in Mexico.86 Prenatal exposure to polycyclic aromatic hydrocarbons was associated with slower language and cognitive development up to age 2 years in China87 and intelligence at age 5 years in Poland.88
Comparison of fi ndings is diffi cult because of variability in exposure duration, timing, and outcome measures.83 Inconsistent fi ndings might also relate to diff erential reactivity, in which eff ects are modifi ed by risk factors, such as low birthweight or malnutrition.85 Alternatively, the eff ect of toxins might be reduced when exposure is associated with protective infl uences, such as poly- unsaturated fatty acids in mercury contaminated fi sh, or better health care for children of mothers employed on farms. Further evidence is needed of the eff ects of toxins on early child development as well as further assessment of interactions with other exposures.
Disabilities In a survey of disability in 18 low-income and middle- income countries, 23% of children aged 2–9 years had, or were at risk for, disabilities. Besides being a marker for compromised development, childhood disabilities can reduce access to school or health services, and increase risk of caregiver stress and depression89,90 (webappen- dix p 40). Studies from south Asia suggest that learning and social integration is also limited by social stigma89 and overprotection by parents.90
Although interventions can promote better function in children with disabilities, few have been assessed in low- income and middle-income countries. Randomised trials suggest more positive attitudes after interactive group therapy in parents of children with intellectual disabilities
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in India,91 and benefi ts from mother–child group inter- vention or parent training to child develop ment and maternal adaptation for children with cerebral palsy in Bangladesh.92 Quasiexperimental studies of parent-training programmes have shown some benefi ts to child develop- ment and maternal behaviour (webappendix p 40).
Evidence on availability of services is scarce but studies from Pakistan and South Africa report that few children receive adequate services.89,93 Identifying barriers to accessing services is an important priority for children with disabilities. Community-based approaches to pro- vision of services are discussed in the second paper in this Series.
Psychosocial factors Early learning and caregiver–child interaction Learning opportunities that facilitate early cognitive development include caregiver activities and materials
that promote age-appropriate language and problem- solving skills. Caregiver–child interactions that facilitate early social–emotional development include caregiver positive emotionality, sensitivity, and responsiveness toward the child, and avoidance of harsh physical punishment. Lack of early learning opportunities and appropriate caregiver–child interactions contribute to loss of developmental potential.1 We review new studies that assess the eff ect of interventions to increase learning opportunities and improve caregiver–child interaction (table 2 and webappendix pp 41–45). The second paper in the Series discusses the eff ectiveness of interventions that are, or could be, implemented at scale.
Studies from Bangladesh, China, India, and South Africa have shown that interventions to enhance mother–child interactions and increase developmentally facilitative activities benefi t cognitive development when delivered through home visits,98 individual parent
Sample and intervention Findings Comments
Chile49 Children aged 6 and 12 months with iron-defi ciency anaemia or who were non-anaemic were randomly assigned to intervention or surveillance groups for 1 year (n=277); infants were given oral iron for 1 year (6-month group) or 6 months (12-month group); surveillance groups received weekly visits to monitor feeding and health, intervention groups received weekly home visits by professional educators to promote development through improving the mother–child relationship
Signifi cant benefi t of intervention to cognitive and social–emotional scores of infants with iron-defi ciency anaemia; intervention group of infants with iron- defi ciency anaemia did not diff er from non-anaemic infants in cognitive and motor trajectories, but their social–emotional development was delayed; in surveillance group infants with iron-defi ciency anaemia social–emotional behaviour declined
No diff erence in cognitive and motor scores between infants with iron-defi ciency anaemia and non-anaemic infants at baseline; infants with iron-defi ciency anaemia had lower scores than non-anaemic infants on socio–emotional development; no intervention benefi ts to non-anaemic infants
South Africa14 Women recruited in late pregnancy from two periurban settlements; randomly assigned to intervention (n=220) or control group (n=229); caregivers were taught in a home stimulation programme to encourage sensitive, responsive interactions with infant, sensitise mother to her infant’s abilities; 16 visits antenatal to 5 months
Intervention mothers more sensitive and less intrusive at 6 and 12 months (d=0·24–0·26); infants more securely attached at 18 months
Maternal sensitivity not signifi cantly associated with infant attachment
China94 100 families with a child younger than 2 years from seven randomly selected villages; families randomly allocated to intervention (n=50) or control (n=50) groups; intervention was two 30–60 min counselling sessions with the WHO Care for Development guidelines, one on enrolment and one within 6 months; mothers were given a card with age-specifi c messages; counselling sessions included demonstration of play activities and practice, discussion of obstacles to implementation and problem solving
Signifi cant benefi ts after 6 months to Gesell quotients in adaptive (d=0·49), language (d=0·52), and social (d=0·17) development; no benefi ts to motor development
Children’s group not masked from tester; not clear where sessions were done but seems fi rst was at health centre and second at home
India95 800 infants admitted to special-care nursery randomly assigned to intervention or control groups; 27% preterm, 50% LBW; 665 infants tested at 1 year, 735 at 2 years; mothers trained individually and in groups to give stimulation and to continue at home; compliance assessed at monthly home visits; intervention given for 1 year
Benefi ts to Bayley mental developmental index and psychomotor developmental index scores at 1 year (eff ect size mental developmental index 0·38, psychomotor developmental index 0·40); eff ect size at 2 about half that at 1 year; benefi ts for VLBW, LBW, and NBW infants
Number of training sessions for mothers not given; not clear if intervention was reinforced at home visits or only monitored compliance
South Africa96 122 HIV-positive children aged <30 months randomly assigned to intervention or control groups (institutionalised children excluded); caregivers taught through home stimulation programmes individualised for their child at usual clinic visit every 3 months; structured around daily activities and developmentally appropriate play; caregivers given a picture book and asked to spend time with child looking at and talking about pictures daily
Signifi cant improvement after 12 months in intervention group compared with control in Bayley mental developmental index (d=0·27) and psychomotor developmental index (d=0·19)
Severe developmental delay in both groups; despite improvement, intervention group remained severely delayed
Jamaica97 Five inner-city preschools randomly assigned to intervention or control; children aged 3–5 years nominated by their teacher as having a behaviour diffi culty were assessed (intervention n=69, control=66); intervention based on Incredible Years teacher training programme (seven full-day teacher workshops and monthly classroom consultations) and 14 child lessons on social and emotional skills in each class; control schools received educational materials only
Intervention children had reduced conduct problems (d=0·26), hyperactivity (d=0·36), and peer problems (d=0·71) by teacher report; no signifi cant benefi ts to prosocial behaviour or emotional problems
Small sample size and small number of schools
d=eff ect size, Cohen’s d. LBW=low birthweight. VLBW=very low birthweight. NBW=normal birthweight.
Table 2: Eff ects of early interventions on cognitive and social–emotional development
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counselling delivered at health centres,94,96 or combined approaches.95 Benefi ts have been shown in children with risk conditions such as severe malnutrition,98 LBW,95 iron-defi ciency anaemia,49 or HIV infection.96 Group parenting education benefi ted mental development in one of three studies (webappendix p 41–45).
In Chile and South Africa, early interventions to improve mother–child interaction promoted attachment14 and social–emotional development,49 although gains were not identifi ed in Bangladesh.98 A preschool intervention in Jamaica to promote social–emotional development reduced child-behaviour problems.97
Sustained intervention benefi ts to cognitive function at age 18 years have previously been reported.1 Studies from Jamaica and Turkey show benefi ts to college attendance,99 psychological functioning,100 and cognition and behaviour at age 6 years.31
Maternal depression A recent study from Bangladesh provides further evidence of the high incidence of maternal depressive symptoms in many low-income and middle-income countries. Maternal depressive symptoms are negatively associated with early child development and quality of parenting across diff erent cultures and socioeconomic groups.101 In Bangladesh, maternal depressive symptoms were associated with infant stunting, perhaps related to unresponsive caregiving13 (webappendix p 46). Risk factors for maternal depression, such as poverty, low education, high stress, lack of empowerment, and poor social support101 are also risk factors for poor child development, suggesting that the relation between maternal depression and compromised early child development is multilevel and cumulative.
Availability of mental health care is restricted in many low-income and middle-income countries. In Pakistan
and South Africa, interventions delivered by community health workers have reduced maternal depressive symptoms,12,102 and improved maternal sensitivity and infant attachment,14 infant health, and time spent playing with infants.102 Evidence that symptoms of maternal depression can be eff ectively treated in low- income and middle-income countries, often with restricted resources and community health workers, emphasises the need for early identifi cation and com- munity programmes to reduce the risk of adverse consequences for mothers and children.
Exposure to violence Estimates suggest that 300 million children younger than 5 years have been exposed to societal violence. New studies further show the adverse consequences of exposure to violence in young children (webappendix p 47). Although domestic violence and child abuse happen in countries of all incomes, we focus here on societal or community violence that might be particularly common in low-income and middle-income countries.
Young children exposed to societal violence show insecure attachments,103 increased risk of behaviour problems,104 reduced levels of prosocial behaviour, and increased aggressive behaviour.105 The adverse conse- quences might result from disruptions to family structure and function106 that compromise the adequacy of maternal childrearing skills,103 and reduce children’s ability to regulate their own emotions.105
Studies from Israel and Palestine identifi ed intervention strategies that can reduce stress reactions for young children.107,108 The eff ect of exposure to violence can be reduced by supportive parental reactions and positive family routines; however, violence can disrupt the quality of parenting, thereby reducing families’ ability to protect young children exposed to violence.107
Sample and method Findings Clinical implications
Metabolic function Romanian children institutionalised early in life, adopted, and followed up at mean age of 8·8 years
PET scan revealed signifi cantly reduced brain metabolism in the prefrontal cortex and temporal lobe, compared with non-institutionalised children
Reduced brain metabolism has several underlying causes; might be important to assess head growth after adoption
Brain structure Romanian children institutionalised early in life, adopted, and followed up at adolescence
MRI scans showed signifi cantly reduced grey-matter and white-matter volume and an enlarged amygdala, compared with non-institutionalised children
Although individuals vary, structural fi ndings such as enlarged amygdala tend to correlate with reduced eye contact and perhaps emotional diffi culties; screening for quasi-autism or anxiety symptoms might be indicated
Brain neurochemistry Cohort of internationally adopted children
Children adopted from poor institutional care might exhibit raised cortisol concentrations years after adoption
Dysregulation of the hypothalamic–pituitary– adrenocortical axis might aff ect stress response and emotional regulation; it might be advisable to encourage or help parents, care providers, and teachers to teach skills in regulating emotions and strategies to manage stress
Brain electrophysiology Bucharest Early Intervention Project, a randomised controlled trial of foster care as an intervention for early institutionalisation
Institutionalised children showed reduced amplitude in event related potential components, compared with non-institutionalised children
See metabolic function
References in the webappendix p 4.
Table 3: Neural consequences of institutionalisation
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Institutionalisation At least 2 million children are institutionalised in non- parental-group residential care. This is probably an underestimate because of under-reporting and lack of information for some regions. Use of orphanages and other institutional care seems to be increasing. Although children’s response to institutionalisation varies, many show long-term developmental defi cits.109 Institutional rearing starting early in life increases children’s risk for adverse outcomes including poor growth, ill-health, attachment disorders, attention disorders, poor cogni- tive function, anxiety, and autistic-like behaviour109,110 (webappendix p 48).
Recent studies of institutionalised children show the eff ect of early experiences on brain development. Institu- tional rearing has been associated with reduced metabolism in the temporal and frontal cortices, reductions in white-matter connectivity, reductions in brain electrical activity, dysregulation of the hypo- thalamic–pituitary–adrenocortical system, and changes in brain volume (particularly the amygdala; table 3 and web appendix p 48). Illustrating the translational processes of timing and cumulative exposure (table 1), children experiencing longer institutional place ment show larger reductions in left amygdala volume111 and greater dysregulation of the hypothalamic–pituitary–adreno- cortical axis,112 whereas children adopted from institutions before the second year of life have more normalised amygdala volume113 and brain electrical activity.114 Adverse neural consequences underlie the behavioural sequelae of early institutionalisation.115
Improving the institutional environment (eg, training staff in sensitive responsive caregiving; increasing caregiver stability and the caregiver-to-child ratio) results in signifi cant benefi ts to child cognitive and social– emotional competence.116 Foster placement and adoption are preferable alternatives to institutionalisation,109,117 particularly if foster and adoptive families receive adequate support.
Protective infl uences Protective factors attenuate adverse consequences of risk factors. Although risk and protective factors are conceptually distinct, many protective factors are the inverse of risk factors (eg, insecure attachment vs secure attachment). Studies in high-income countries have identifi ed biological, psychosocial, and behavioural protective factors for young children, but there are few studies from low-income and middle-income countries. The protective eff ects of breastfeeding and early cognitive and social–emotional stimulation were reviewed in previous sections. Maternal education also can act as a protective factor, reducing child mortality and promoting early child development (webappendix pp 49–50).
Young children of educated mothers have higher levels of cognitive development than children of less educated mothers.118–120 Similarly, high-risk infants121 and young
Panel 2: Protective mechanisms associated with more maternal education*
Less maternal depression • Lower risk of maternal depression and non-depressed
mothers provide a more optimum rearing environment for their children
Child nutritional status • Infants and young children with better nutritional
status
Quality of child-rearing environment • Greater knowledge about child development • More likely to use developmentally appropriate
child-rearing strategies and provide more stimulating home environments
• Possess a wider variety of child-rearing strategies • More sensitive to individual diff erences in children’s
developmental trajectories • Have higher educational aspirations for their children
Ability to access and benefi t from interventions • More likely to make use of available intervention services;
are more likely to be involved in and comply with intervention programmes
• Better able to comprehend intervention material (eg, growth charts)
• Have greater recall of intervention material
References in the webappendix pp 4–5. *Maternal education is a unique protective factor, even after adjusting for family economics.123
Figure 2: Diff ering trajectories of brain and behavioural development as a function of exposure to risk and protective factors The cumulative eff ect is illustrated by the progressive strengthening (darker lines) of the trajectories over time.
Below potential
Optimum
Br ai
n fu
nc ti
on Be
ha vi
ou ra
l c om
pe te
nc e
tr aj
ec to
rie s
Age Prenatal Birth Early childhood Adolescence Adulthood
Reduction in risk factors, increase in protective factors, or intervention during a sensitive period
Risk factors > protective factors
Protective > risk factors
Optimum Recovery Below potential
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children122 show better developmental trajectories when their mothers have higher levels of education.
In panel 2 we show the protective mechanisms linking maternal education and early child development. Children of less-educated mothers are likely to have greater exposure to developmental risks and less access to interventions than children of more-educated mothers, suggesting that low maternal education identifi es families in need of intervention.118 However, poorly educated women might benefi t less from participation in parent-focused programmes than better-educated women124 (diff erential reactivity), emphasising the need
for strategies to increase their participation and learning in early child-development interventions.
Conclusions Major advances in neuroscience show how exposure to biological and psychosocial risk factors, prenatally and during early childhood, aff ects brain structure and function and compromises children’s development and subsequent developmental trajectory. We summarise in fi gure 2 how risk and protective factors encountered before age 5 years compromise children’s development. The greater the exposure to cumulative risks the greater
Recent evidence Implications
Risk factors
Inadequate stimulation and opportunities for learning
Increased evidence of intervention benefi ts for social–emotional outcomes (ES* 0·24–0·71) and further evidence of benefi ts to cognitive outcomes (ES 0·27–0·85; table 2 and webappendix pp 41–45)
Need for eff ective strategies for scaling up of programmes that promote early stimulation and learning opportunities and integration with health and nutrition services for young children
Stunting (linear growth retardation)
Evidence of eff ect on ability at age 5 years (ES 0·2 for stunting at age 1 year) and long-term outcomes such as educational attainment, increased formal employment (ES 0·2 for 1 SD change in height for age at age 2) and psychological functioning (ES 0·4–0·5 comparing stunted and non-stunted)
Results further emphasise the importance of adequate nutrition in the fi rst 2 years; stimulation should be an integral part of intervention for stunted children
Iodine defi ciency We did not discuss this in view of previous conclusive fi ndings;1 for recent supporting studies see webappendix p 51
Need for continued attention to expanding and ensuring quality control of fortifi cation programmes
Iron-defi ciency anaemia Evidence for neurophysiological changes and neural mechanisms leading to developmental defi cits; ES medium to large; increased evidence of long-term cognitive and behavioural eff ects of early iron-defi ciency anaemia; ES small to large (webappendix pp 9–28)
Results emphasise the importance of prevention of iron defi ciency early in life
IUGR Consistent evidence for lower developmental levels in early childhood; evidence for long-term eff ects mixed (ES 0·19–0·31)
IUGR infants likely to benefi t from early interventions to promote development; need for increased strategies to reduce IUGR including better maternal nutrition
Malaria Increased evidence for long-term defi cits due to cerebral and severe malaria; less information for children younger than 5 years but longitudinal studies suggest uncomplicated attacks are associated with reduced ability at school entry (reading and language one to four attacks ES0·37–0·47; greater than four attacks 0·57–0·92) and fewer attacks with better subsequent educational achievement (ES 0·22–0·62)
Need for expansion of prevention programmes (eg, insecticide-treated bednets)
Lead exposure Evidence for adverse eff ects of low concentrations of prenatal exposure for child development (ES 0·19–0·27)
Continued attention to prevention of exposure to lead (eg, through removal of lead in paint, gasoline)
Maternal depression Further evidence for adverse eff ects of maternal depressive symptoms on early child development and quality of parenting; community-based interventions with para-professionals eff ective in reducing depressive symptoms (ES 0·21–0·62)
Increased emphasis on early identifi cation of women who are depressed; programmes to reduce maternal depressive symptoms and reduce risks for depression will probably benefi t early child development
Exposure to violence Exposure to violence detrimentally aff ects social–emotional development of young children (ES medium to large) and compromises primary caregiver child-rearing capabilities; some evidence that interventions can reduce stress reactions in young children (ES 0·56–0·91)
Need for interventions that can strengthen families exposed to societal violence and help caregivers reduce eff ect of exposure on young children
HIV infection† Substantial evidence that development of infected children is delayed (ES usually medium to large; webappendix pp 33–37); US studies show developmental benefi ts from HAART, less evidence from low-income and middle-income countries; aff ected children might also have cognitive defi cits and mental health problems
Need for increased coverage with HAART starting children on treatment in the fi rst year of life, and for assessment of eff ect of treatment on developmental outcomes
Institutionalisation† Recent evidence has documented adverse neural, cognitive, and behavioural eff ects for institutionalised children (ES for IQ 1·10, compared with family reared); improving quality of caregiving in institutions benefi ts cognitive and social–emotional competence (ES 0·43–0·84)
Strategies are needed to support foster and adoptive families to prevent children being placed in institutions; where children are institutionalised, strategies shown to improve early child development should be implemented
Protective factors
Breastfeeding† Stronger evidence for benefi cial eff ects of exclusively breastfed and longer duration of breastfeeding (ES for IQ 0·38; grades attained 0·22–0·35)
Benefi ts to development add to existing reasons for promotion of breastfeeding
Maternal education† Growing evidence on mechanisms linking maternal education to children’s development (ES medium Cohen’s h=0·73 to large Cohen’s h=0·82, d=1·59)
Increased emphasis on educating women as part of an overall intervention package; ensure interventions are appropriate for women with little education
IUGR=intrauterine growth restriction. ES=eff ect sizes. HAART=highly active antiretroviral therapy. IQ=intelligence quotient. *ES are for studies reviewed in this paper that reported them or with suffi cient information to compute; where specifi c ES are given, these are Cohen’s d unless otherwise specifi ed (previously reported eff ect sizes from earlier studies are reported in Walker and colleagues1).†Not reported as a high priority risk or protective factor in the previous Series in The Lancet.
Table 4: High priority developmental risk and protective factors
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the inequality, suggesting that early interventions that prevent inequality are more eff ective than later interventions, which attempt to remedy cumulative defi cits. Risk factors are likely to co-occur, emphasising
the importance of integrated interventions involving the simultaneous reduction of multiple risks. The second paper in the Series discusses integrated interventions.
Inequalities in low-income and middle-income countries are established in early childhood and contribute to lifetime diff erences. Accumulated developmental defi cits in early childhood place children on a lower life- time trajectory with negative implications for adult cognitive and psychological functioning, educational attainment, and subsequent income, thus contributing to continued inequalities in the next generation.
In table 4, we list the risk and protective factors with suffi cient evidence to be priorities for intervention and summarise the evidence reviewed. Previously identifi ed key risks (inadequate stimulation, stunting, iodine defi ciency, iron-defi ciency anaemia) remain in need of urgent intervention to prevent the loss of developmental potential in millions of young children. Although there has been recent attention to the eff ect of early nutrition on development and health,125 substantial progress in improving development is unlikely to be made without also increasing early learning opportunities.126 A meta- analysis of non-US intervention studies127 showed that cognitive benefi ts were greater when interventions included stimulation or education components com- pared with those comprising nutrition or economic assistance only. This strengthens the case for integra- tion of stimulation with economic, nutrition, and health interventions.
New research strengthens the evidence for prioritisation of interventions to reduce the levels of IUGR, malaria, maternal depression, institution al- isation, and exposure to societal violence and to promote development in aff ected children. New research also suggests the adverse consequences for children infected with HIV or whose parents are infected. We highlight the importance of protective factors such as breastfeeding and higher maternal education, which can reduce the eff ect of risks. Knowledge of risk and protective factors can inform priorities for programmes and funding to promote early child development. This knowledge, plus increased understanding of the neural consequences of risks, provides persuasive data for advocacy and the design of early intervention programmes to reduce developmental inequalities.
Although eff ective interventions exist for some identifi ed risks, further research is needed to increase our ability to promote early child development in low- income and middle-income countries. We list research priorities in panel 3. There has been little progress in some previously identifi ed research priorities (eg, supple- mentation with multiple micronutrients, prenatal iron defi ciency, and exposure to toxins). Additional research questions include the eff ect of prenatal maternal nutrition and stress on development, assessment of the eff ect of interventions to reduce maternal depression on child development, and assessment of strategies to reduce the
Panel 3: Priorities for future research to reduce developmental inequalities in infants and young children from low-income and middle-income countries
Maternal nutrition • Eff ect of food supplementation before and during pregnancy on development of
infants and young children. • Eff ect of prenatal iron defi ciency on postnatal cognitive and social–emotional
development. • Eff ect of supplementation with multiple micronutrients in pregnancy on child
development by comparison with iron and folic acid alone. • Eff ect of maternal supplementation with ω3 fatty acids on infant development. • Long-term eff ects of IUGR on cognitive and social–emotional outcomes.
Child nutrition • Eff ect of improving infant intake of essential fatty acids on development. • Eff ect of supplementation with multiple micronutrients on development and
comparison with eff ects of iron only. • How to integrate nutrition and psychosocial stimulation programmes at scale.
Infections • Eff ect of malaria prevention strategies on early child development. • Eff ect of antiretroviral treatment on cognitive and behavioural outcomes and eff ect of
non-medical interventions to promote development in children infected with HIV. • Extent of mental health problems for infants and young children orphaned because of
AIDS. Assessment of interventions to support caregivers and promote development of children aff ected by HIV.
Toxins • Evidence on eff ect of toxins is inconsistent possibly because of interactions with other
exposures. Longitudinal studies are needed to assess potential moderating variables (eg, nutrition).
Disabilities • Assessment of the eff ect of interventions for children with disability and their families. • Identifi cation of barriers to accessing general services (eg, primary health care) as well
as specialist services.
Learning opportunities and stimulation • Modifi cation of interventions to facilitate expansion, and assessment of eff ectiveness
of programmes at scale. • More evidence on the eff ect of early interventions on social and emotional
development.
Maternal depression • Assessment of eff ect of interventions to reduce depressive symptoms on child
development and identifi cation of strategies to expand access.
Violence • Evidence needed on the neural and developmental eff ect of violence exposure on
children younger than 5 years and on eff ective treatment strategies for young children exposed to violence.
Protective factors • Need to identify additional protective factors for outcomes related to early child
development in low-income and middle-income countries.
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developmental consequences for children aff ected by violence and for children in families aff ected by HIV. Research is also needed to develop strategies to include children with disabilities in early child development programmes and provide them with specialist services, and to identify additional protective factors in low-income and middle-income countries.
Without the threats of biological and psychosocial risks, and with a caregiving environment that supports cognitive and social–emotional development, children experience healthy brain development that enables them to reach toward their developmental potential. With this strong foundation, they build lifespan developmental trajectories that enable them to benefi t from family, community, and educational opportunities (fi gure 2). Eff ective interventions to promote early child development in low-income and middle-income countries exist either at scale or are potentially scalable. Interventions to reduce risks and support early child development will yield lifetime gains that contribute to the achievement and sustainability of improved development in the next generation. By investing in early child development programmes, we have an opportunity to break the cycle of inequities that has dominated the lives of millions of children and families in low-income and middle-income countries.
Contributors All authors participated in the review of published work, and drafting
and review of the report. SPW and TDW are the lead authors of this
report and were responsible for the fi nal draft and the decision to
submit for publication. SG-M and MMB provided critical revision of
the text. Reviews and drafting of individual topics were as follows:
Brain development CAN and TDW; maternal undernutrition SG-M;
micronutrients SG-M and MMB; essential fatty acids SLH; IUGR SPW;
breastfeeding CAP; stunting SG-M; iron defi ciency BL; diarrhoea
MMB; malaria SG-M; other parasitic infections TDW; HIV JMM and
LR; toxins JDH; disabilities HB-H; early learning opportunities SPW,
SMC, and HBH; maternal depression AR; violence JMM and TDW;
institutionalisation CAN, SG-M, and LR; and protective factors TDW.
The steering committee of the Global Child Development Group
coordinated the writing of the report in this Series.
Confl icts of interest We declare that we have no confl icts of interest.
Acknowledgments We thank Amika Wright for assistance with referencing and Anna
Quigg for assistance with fi gure 2. A meeting of all authors to discuss
review fi ndings and coordinate the report was held in Jamaica in
December, 2009, with the support of the Global Alliance for Improved
Nutrition (GAIN), UNICEF, the Bernard van Leer Foundation, and the
University of the West Indies. A follow-up steering committee meeting
was held in May, 2010, with the support of UNICEF, the Bernard van
Leer Foundation, and the Child Health and Nutrition Research Initiative.
The sponsors had no role in the design and conduct of the review,
interpretation and writing or the decision to submit for publication.
HBH was supported by a Wellcome Trust Fellowship (# 080534/Z/06/Z).
We thank the Global Child Development Group Secretariat for
coordinating the meetings.
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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission.
- Inequality in early childhood: risk and protective factors for early child development
- Introduction
- Risk, stress, and brain development
- Maternal nutrition
- Infant and child nutrition
- Infectious diseases
- Environmental toxins
- Disabilities
- Psychosocial factors
- Early learning and caregiver–child interaction
- Maternal depression
- Exposure to violence
- Institutionalisation
- Protective influences
- Conclusions
- Acknowledgments
- References