Stunting in Developing Countries
Andrew M. Prentice
Although stunting rates in low- and middle-income countries have been declining quite rapidly, with many countries meeting their Millennium Development Goal targets, there remain an estimated 160 million stunted children worldwide. As one of its Nutrition Targets, the World Health Organization (WHO) has set an ambitious goal of a further 40% reduction by 2025. Unfortunately, the rate of reduction in Africa is so slow that it is being more than offset by population growth such that the absolute numbers of stunted children is rising in this region.
In scanning all the papers published on this topic during the year under review, there is a depressing preponderance of descriptive papers that simply summarize the anthropometric statistics by region, country, area or population group with some of these papers including analyses of factors predictive of poor growth. The great problem with such analyses is that the factors associated with growth failure are all generally correlated with poverty and hence – apart from global eradication of poverty – it is hard to navigate through the statistical confounding and pinpoint individual factors that predispose to stunting. Some of these analyses do a much better job than others, and the examples are listed below.
Growth faltering in rural Gambian children after four decades of interventions: a retrospective cohort study
HM Nabwera, AJ Fulford, SE Moore and AM Prentice
Recent estimates suggest that the rate of stunting has declined in many regions. How- ever, it has declined very slowly in sub-Sahara Africa. Due to this very slow decline in the prevalence of stunting, and the growth in population, the absolute number of children with stunting has in- creased. Thus, it is important to identify effective intervention methods.
This was a cohort study using routine growth monitoring data from birth to age 2 years of 3,659 children between 1976 and 2012. The authors analyzed the effect of 36 years of intensive health interventions on growth in infants and young children from three rural Gambian villages. Z scores for weight-for-age, length-for-age, weight-for-length, mid-upper-arm circumference, and head circumference were calculated using the World Health Organization 2006 growth standards. Seasonal patterns of mean Z scores were obtained by Fourier regression.
Secular improvements were noted in all postnatal growth parameters, except weight-for- length, accompanied by declines over time in seasonal variability. The proportion of children who were underweight or stunted at 2 years of age halved during four decades of the study period, from 38.7% (95% CI 33.5–44.0) for underweight and 57.1% (95% CI 51.9–62.4) for stunting. However, despite the unprecedented extent of intervention, postnatal growth faltering persisted, leading to poor nutritional status at 24 months.
A combination of nutrition-sensitive and nutrition-specific interventions has caused a reduction of 50% in undernutrition rates. Yet, considerable growth faltering remains. It is important to learn and understand the causes to growth faltering to be able to develop new interventions.
Handwashing, sanitation and family planning practices are the strongest underlying determinants of child stunting in rural indigenous communities of Jharkhand and Odisha, Eastern India: a cross-sectional study
J Saxton, S Rath, N Nair, R Gope, R Mahapatra, P Tripathy and A Prost
The WHO is aiming to reduce by 40% the number of stunted children worldwide by 2025. Approximately 55 million children affected by stunting live in India, and children from poorest families from Scheduled Caste and Scheduled Tribe communities are the worst affected.
The aim of the study was to identify the strongest factors causing stunting among these children in rural Jharkhand and Odisha in India to find the most relevant intervention methods.
Data were collected in 2010 from 1,227 children aged 6 months to 3 years and their mothers, from 18 clusters of villages in 3 districts with a high proportion of people from the “depressed classes.” The authors measured height and weight of mothers and children, and captured data on various basic, underlying and immediate determinants of undernutrition. Generalized Estimating Equations were used to identify individual determinants associated with children’s height-for-age z-score (HAZ; p < 0.10); the authors included these in a multivariable model to identify the strongest HAZ determinants using backwards stepwise methods.
In the adjusted model, the strongest protective factors for linear growth included cooking out- doors rather than indoors (HAZ +0.66), birth spacing ≥24 months (HAZ +0.40), and handwash- ing with a cleansing agent (HAZ +0.32). The strongest risk factors were later birth order (HAZ–0.38) and repeated diarrhoeal infection (HAZ –0.23). The results suggest multiple risk factors for linear growth faltering in indigenous communities in Jharkhand and Odisha. Interventions that could improve children’s growth include reducing exposure to indoor air pollution, increasing access to family planning, reducing diarrhoeal infections, improving handwashing practices, increasing access to income, and strengthening health and sanitation infrastructure.
Impact of contaminated household environment on stunting in children aged 12–59 months in Burkina Faso
F Fregonese, K Siekmans, S Kouanda, T Druetz, A Ly, S Diabaté and S Haddad
One hundred sixty-five million children worldwide suffer from stunting, which affects their survival and development. Increasing evidence suggests that environmental enteropathy disorder (EED) may play a significant role in children with faltering growth, with a likely contribution of frequent fecal-oral transmission.
The aim of this study was to assess the impact of fecal-oral transmission on stunting in Burkina Faso, where stunting prevalence is very high.
Data were collected from a household panel study that was set up in 2011 as part of the Kaya Health and Demographic Surveillance System. Cohort consisted of children aged 1–5 years in Kaya. Data on household socioeconomic characteristics, food needs, and environmental contamination were collected once, and child growth parameters were measured annually, between 2011 and 2014. The authors used multiple correspondence analysis and 12 questions and observations on water, sanitation, hygiene behaviors, yard cleanliness, and animal proximity, to construct a “contaminated environment” index as a measure of exposure to fecal-oral transmission. Analysis was performed using a generalized structural equation model, adjusting for repeat observations and hierarchical data.
Stunting (<2 SD height-for-age) was found in 29% of 3,121 children (median [interquartile range] age 36 [25–48] months). Environment contamination was highly prevalent, especially in rural and peri-urban areas, and was positively correlated with stunting (prevalence ratio 1.30; p = 0.008), after controlling for sex, age, survey year, setting, mother’s education, father’s occupation, household food security, and wealth. This association was significant for children of all ages (1–5 years) and settings. The effect of lower contamination was comparable to that of higher food security.
This study suggests that environment contamination may play an important part in the pathogenesis of stunting. Interventional programs for prevention of stunting should aim to reduce environmental contamination and fecal-oral transmission.
Female-headed households associated with lower childhood stunting across culturally diverse regions of Pakistan: results from a cross-sectional household survey
H Khalid and EG Martin
The focus on female empowerment created interest in studying how it can also improve child health outcomes, and literature on this topic is plentiful. However, very little has been studied on the relationship between female empowerment and childhood stunting. Early childhood stunting has an adverse effect on long-term cognitive and health outcomes. The authors, therefore, explored this relationship among young children in Punjab, Pakistan, which has both high stunting rates and a considerable proportion of female-headed households. They also tried to assess whether this relationship varied within three provincial regions with differing cultural attitudes towards women’s role in society.
The authors collected data from a cross-sectional household level survey performed in 2011, identifying 13,412 children aged 1–4 from 8,985 two-parent households in three culturally distinct regions in Punjab. Logistic regression models were used to estimate whether stunting was associated with female-headed households, as a reflection of female empowerment, and whether this relationship varied by region. Regressions were controlled for child-and household-level covariates.
Children from female-headed households had 26% lower odds of stunting than children from male-headed households (OR 0.74, 95% CI 0.60–0.90). The interaction term for female-head- ed households and child stunting by provincial region was not statistically significant, suggesting that the relationship is valid across the three culturally distinct regions.
The results of this study suggest that women can improve child outcomes even after adjusting for access to medical care. Moreover, the results showed that with increased level of education for the household head, there is a reduction of stunting among children. Therefore, greater investments in public education and awareness campaigns to improve health literacy are needed for improving the success of existing public health interventions targeting childhood stunting.
Risk factors for childhood stunting in 137 developing countries: a comparative risk assessment analysis at global, regional, and country levels
G Danaei, KG Andrews, CR Sudfeld, G Fink, DC McCoy, E Peet, A Sania, MC Smith Fawzi, M6 Ezzati and WW Fawzi
Many risk factors for stunting have been identified in epidemiological studies, but their relative impact on stunting across developing countries is not known. This study aimed to evaluate the number of stunting cases in children aged 24–35 months and their relationship to 18 risk factors in 137 developing countries.
Methods and Findings
Risk factors were classified into five clusters: maternal nutrition and infection, teenage motherhood and short birth intervals, fetal growth restriction (FGR) and preterm birth, child nutrition and infection, and environmental factors. The authors derived the prevalence of exposure to each risk factor for the year 2010 from published literature and other available surveys, and estimated the prevalence of stunting and the number of stunting cases that were attributable to each risk factor and cluster by country and region. The leading risk factor across all countries studied was FGR (children born at term and small for gestational age), with 10.8 million cases (95% CI 9.1–12.6 million) of stunting (out of 44.1 million). The next most influential factors were unimproved sanitation, with 7.2 million (95% CI 6.3–8.2 million), and diarrhea with 5.8 million (95% CI 2.4–9.2 million). FGR and preterm birth was the leading risk factor cluster in all regions. Environmental risks had the second largest estimated impact on stunting globally and in the developing regions, whereas child nutrition and infection were the second leading cluster of risk factors in other regions.
The analysis is limited to risk factors for which data were available, and also required various approximations and assumptions.
This study found that FGR, unimproved sanitation, and diarrhea are the leading risk factors for stunting globally, with a bigger impact on stunting in developed regions than in other regions. Reducing the burden of stunting requires not only treatment of the affected infants, but also interventions focused on improving nutrition and sanitation for mothers and families.
The first paper by Nabwera et al.  sets the scene for what follows. It describes a 40-year longitudinal analysis of growth data collected in 3 rural Gambian villages that have benefitted from an unprecedented level of health interventions. There is good news and bad news. The good news is that stunting levels in 2-year olds were halved from 57 to 30%. The bad news is that despite the intense interventions that have had a profound effect on mortality, there is still a 30% rate of child stunting. This suggests that there is a very high threshold for interventions before stunting will be eliminated. What do these interventions consist of? This is where we need robust data on the primary etiological factors. The analysis by Saxton et al.  using data from Eastern India observed effect size associations that are unusually strong for this type of study. The strongest protective factors for linear growth included cooking outdoors rather than indoors (HAZ +0.66), birth spacing ≥24 months (HAZ +0.40), and handwashing with a cleansing agent (HAZ+0.32). The strongest risk factors were later birth order (HAZ –0.38) and repeated diarrheal infection (HAZ –0.23).
A somewhat similar study in Burkino Faso attributed stunting to environmental contamination with a prevalence ratio of 1.30 in rural and peri-urban settings after adjusting for the measured potential confounders. As mentioned above there remains a risk of residual confounding in all such studies and the prevalence ratio of 1.3 is not very large. Thus, this and similar studies confirm what we already know about the relationship be- tween poverty, living conditions and stunting, but do not give granular insights.
Khalid and Martin’s study in Pakistan based on an analysis of household surveys showed that the risk of stunting was 24% lower in female-headed houses; from which they concluded that female empowerment and health literacy would be a good investment.
The final paper by Danaei et al.  offers a complex analysis of the impact of 5 clusters of risk factors for stunting in 137 developing countries. The authors acknowledge the limitations of their approach and stress that it only includes factors for which they could find published effect sizes. Nonetheless, they concluded that the leading risk worldwide was FGR, defined as being term and small for gestational age, with 10.8 million cases of stunting attributable to it (about one quarter of the total burden). This was followed by unimproved sanitation, with 7.2 million, and diarrhea with 5.8 million. FGR and preterm birth was the leading risk factor cluster in all regions. Environmental risks had the second largest estimated impact on stunting globally and in the South Asia, sub-Saharan Africa, and East Asia and Pacific regions, whereas child nutrition and infection were the second leading cluster of risk factors in other regions.
The next 3 papers relate to the long-discussed issue of how, and to what extent, EED lie on the causal pathway to stunting. This has been a topic of keen enquiry since the first demonstrations of chronic gut damage in young children in our own and other laboratories well over a quarter of a century ago.
Environmental enteric dysfunction and growth failure/stunting in global child health
V Owino, T Ahmed, M Freemark, P Kelly, A Loy, M Manary and C Loechl
Approximately 25% of the world’s children aged <5 years suffer from stunting, which is associated with increased mortality, cognitive dysfunction, and loss of productivity. The global target is a 40% reduction in the number of stunted children by 2030. The pathogenesis of stunting is not fully understood. EED – a generalized disorder of small intestinal structure, commonly found in children living in unsanitary conditions – has a significant role in stunting. Mechanisms leading to growth failure in EED include increased intestinal permeability, gut inflammation, dysbiosis and bacterial translocation, systemic inflammation, and nutrient malabsorption. Since many causal pathways lead to EED, there is a need for versatile ways to treat it. Potential interventions to reduce EED include: (1) improved water, sanitation, and hygiene; (2) promotion of breastfeeding and diverse complementary nutrition; (3) probiotics and prebiotics; (4) nutrient supplements, including zinc, polyunsaturated fatty acids, and amino acids; (5) antiin-flammatory agents such as 5-aminosalicyclic acid; and (6) antibiotics in the management of acute malnutrition and infection. Improved understanding of the events leading to EED and development of optimal diagnostic tools are still pending. “Omics” technologies (genomics, epigenomics, transcriptomics, proteomics, and metabolomics) and stable isotope techniques (e.g., 13C breath tests) targeted at children and their intestinal microbiota may enhance our ability to successfully identify, manage, and prevent this disorder.
Systemic inflammation, growth factors, and linear growth in the setting of infection and malnutrition
MD DeBoer, RJ Scharf, AM Leite, A Férrer, A Havt, R Pinkerton, AA Lima and RL Guerrant
Recurrent infections are associated with lower growth velocity and stunting in children in developing areas of the world where malnutrition and recurrent infections are common. It is well known that both inflammation and malnutrition can result in growth hormone (GH) resistance, however, the interplay between infection, inflammation, and stunted growth in developing areas is not fully understood.
This study aimed to assess relationships between mild systemic inflammation, growth factors, and anthropometric measures in a case-control cohort of underweight and normal weight children in northern Brazil. The authors’ hypothesis was that even low-grade inflammation would be associated with GH resistance, including lower levels of insulin-like growth factor-1 (IGF-1) and IGF-binding protein-3 (IGFBP-3) and higher levels of GH through lack of feedback.
Data from 147 children ages 6–24 months – evaluated in the MAL-ED case-control study – was assessed following recruitment from a nutrition clinic for impoverished families in Fortaleza, Brazil. Nonparametric tests and linear regression were used to evaluate correlations between symptoms of infections (assessed by questionnaire), systemic inflammation (portrayed by high-sensitivity C-reactive protein [hsCRP]), the GH IGF-1 axis, anthropometric measures. All models were adjusted for age and sex.
Children with recent symptoms of diarrhea, cough, and fever had higher hsCRP levels than children without symptoms; those with recent diarrhea and fever also had lower IGF-1 and higher GH levels. There was a positive association between stool myeloperoxidase and serum hsCR. In turn, hsCRP was positively associated with GH and negatively associated with IGF-1 and IGFBP-3, assumedly reflecting a state of GH resistance. Following adjustment for hsCRP, IGF-1 and IGFBP-3 were positively and GH was negatively associated with z scores for weight and height.
The authors found that even mild inflammation in a cohort of significant poverty may lead to decreased growth, and a state of resistance to GH.
Causal pathways from enteropathogens to environmental enteropathy: findings from the MAL-ED birth cohort study
MN Kosek, et al. for the MAL-ED Network Investigators (159 collaborators)
EED, a state of persistent immune activation and altered permeability stemming from frequent and recurrent enteric infections, has been suggested as a major determinant of growth deficits in children in low- and middle-income countries. A theory-driven systems model to assess pathways by which enteropathogens, gut permeability, and intestinal and systemic inflammation influence child growth was developed within the framework of the Etiology, Risk Factors and Interactions of Enteric Infections and Malnutrition and the Consequences for Child Health and Development (MAL-ED) birth cohort study.
Non-diarrheal stool samples (n = 22,846) from 1,253 children from multiple sites within 8 countries were analyzed for markers of gut inflammation, a panel of 40 enteropathogens and fecal concentrations of myeloperoxidase, alpha-1-antitrypsin, and neopterin. Markers of gut permeability – urinary lactulose:mannitol (L:M; n = 6,363) and plasma alpha-1-acid glycoprotein (n = 2,797) – as well as anthropometric measures were also measured in the same cohort. A specific temporal sampling design was used to evaluate proposed mechanistic pathways leading to stunting in children 0–2 years of age.
In this cohort, frequent enteric infections and high levels of both intestinal and systemic inflammation were found. Higher loads of enteropathogens, especially those known to be entero-invasive or causing mucosal disruption, were linked with increased levels of gut and systemic inflammation markers, and thus indirectly associated with reduced linear and ponderal growth. Evidence supporting the association with impaired linear growth was more robust for systemic inflammation than for gut inflammation, but apparently reduced ponderal growth was more strongly correlated with local than systemic inflammation.
The substantial quantity of empirical data contributing to this analysis supports the conceptual model of EED. The impact of EED on growth faltering in young children was small, but the different analyses performed supported the attribution of growth failure to asymptomatic enteric infections. The strongest evidence for EED was the association between enteropathogens and linear growth mediated via systemic inflammation.
The paper by Owino et al.  reviewed the current knowledge linking EED to stunting and suggested 6 categories of potential interventions. The following 2 papers are among the early results from the multi-centre MAL-ED study funded by the Bill and Melinda Gates Foundation.
DeBoer et al.  describe the results from one of the MAL-ED sites in Brazil. Their results confirm the known links between infections, gut damage and inflammation, and systemic inflammation. They also assessed the GH/IGF-1 axis and found evidence of GH resistance in children with raised levels of systemic inflammation.
The final paper by Kosek et al.  summarizes the integrated results from all the MAL- ED sites, and therefore represents a very important piece of work. They present a he- roic analysis including multiple measures of enteropathogen load in non-diarrheal stools, biomarkers of intestinal permeability and inflammation, and of systemic inflammation, and related these to subsequent growth using acyclic modelling. Again, the findings supported the current thinking with respect to the interconnecting pathways from enteropathogens to EED to systemic inflammation and growth restriction. However, the authors noted that the effect sizes were much smaller than anticipated. This might be a consequence of the renowned imprecision of measures of gut function which will necessarily introduce a high degree of correlation dilution.
The final paper is selected because it had an unusually large effect for an intervention against stunting; achieved by the provision of an egg per day.
Eggs in early complementary feeding and child growth: a randomized controlled trial
LL Iannotti, CK Lutter, CP Stewart, CA Gallegos Riofrío, C Malo, G Reinhart, A Palacios, C Karp, M Chapnick, K Cox and WF Waters
The aim of this study was to assess whether early introduction of eggs – a simple, affordable, and available source of nutrients – during complementary feeding would improve the growth and development of children from a resource-poor population.
This was a randomized controlled trial conducted in Ecuador, in which children aged 6–9 months were randomly assigned to intervention (an egg per day for 6 months [n = 83]) and control (no intervention [n = 80]) groups. Both arms received messages encouraging them to take part in this project. Household visits were performed once a week to monitor morbidity symptoms, distribute eggs, and monitor egg intakes (for egg group only). Baseline and end-point outcome measures included anthropometry, dietary intake frequencies, and morbidity symptoms.
No allergic reactions to the eggs were reported. Generalized linear regression modeling revealed that the egg supplementation increased length-for-age z score by 0.63 (95% CI 0.38–0.88) and weight-for-age z score by 0.61 (95% CI 0.45–0.77). Log-binomial models with robust Poisson demonstrated a 47% reduction in the rate of stunting (prevalence ratio [PR] 0.53; 95% CI 0.37–0.77) and a 74% reduction in the prevalence of underweight (PR 0.26; 95% CI 0.10–0.70). Compared with controls, children in the intervention group had higher dietary intakes of eggs (PR 1.57; 95% CI 1.28–1.92) and a reduced intake of sugar-sweetened foods (PR 0.71; 95% CI 0.51–0.97).
This study suggests that the early introduction of eggs significantly improves growth in young children. Given the relative accessibility of eggs, this intervention may help to meet the global target set by the WHO to reduce stunting by 40% by 2025.
The egg intervention increased length-for-age z-score by 0.63 and reduced the prevalence of stunting by 47%. These are impressive results in comparison even against all of the LNS studies that have used a product specifically designed to enhance child growth (see last year’s Year Book). The authors note that “Eggs are a complete food, safely packaged and arguably more accessible in resource-poor populations than other complementary foods, specifically fortified foods” and “Moving forward, there is a need for effectiveness studies to identify scalable strategies to increase egg availability and access to vulnerable households and promote eggs early in the complementary feeding period in different cultural contexts.”
In next year’s Year Book, I look forward to being able to summarize the long-awaited results from the Wash Benefits Trials (in Kenya and Bangladesh) and the SHINE Trial in Zimbabwe. Initial results have been presented at conferences but not yet as full papers.
- 1 Nabwera HM, Fulford AJ, Moore SE, Prentice AM: Growth faltering in rural Gambian children after four decades of interventions: a retrospective cohort study. Lancet Glob Health 2017;5:e208–e216.
- 2 Saxton J, Rath S, Nair N, Gope R, Mahapatra R, Tripathy P, Prost A: Handwashing, sanitation and family planning practices are the strongest underlying determinants of child stunting in rural indigenous communities of Jharkhand and Odisha, Eastern India: a cross-sectional study. Matern Child Nutr 2016; 12:869–884.
- 3 Danaei G, Andrews KG, Sudfeld CR, Fink G, McCoy DC, Peet E, Sania A, Smith Fawzi MC, Ezzati M, Fawzi WW: Comparative Risk Assessment Analysis at Global, Regional, and Country Levels. PLoS Med 2016;13:e1002164.
- 4 Owino V, Ahmed T, Freemark M, Kelly P, Loy A, Manary M, Loechl C: Environmental Enteric Dysfunction and Growth Failure/Stunting in Global Child Health. Pediatrics 2016;138:e20160641.
- 5 DeBoer MD, Scharf RJ, Leite AM, Férrer A, Havt A, Pinkerton R, Lima AA, Guerrant RL: Systemic inflammation, growth factors, and linear growth in the setting of infection and malnutrition. Nutrition 2017;33:248–253.
- 6 Kosek MN, MAL-ED Network Investigators: Causal pathways from enteropathogens to environmental enteropathy: findings from the MAL-ED birth cohort study. EBioMedicine 2017;18:109–117.