Discussion
In this study, we found that food access insecurity was associated with a statistically significant shift in the distribution of children’s HAZ toward lower values, after adjusting for sociodemographic factors. Although prevalence of both food access insecurity and faltering in HAZ varied across countries, a likelihood ratio test for heterogeneity revealed that the relationship between these variables was consistent across countries. Our findings on the epidemiology of growth faltering are consistent with the literature. Previous studies have reported higher prevalence of stunting than wasting within populations [
23‐
25], and more variation in wasting than in stunting across populations [
1,
25]. Although our results indicate regional patterns in prevalence of wasting only, others have found clear regional patterns in both stunting and wasting [
1,
23,
25]. Variations between sites likely reflect the impact of numerous factors, including seasonal effects on the food supply, patterns of enteric infections, genetic predispositions, and access to prenatal and infant health services. Stunting and wasting are indicators of chronic and acute malnutrition, respectively [
11]. However, beyond reflecting differences in the length of exposure to deprivation, they are also differentially associated with other socio-demographic variables, such as maternal education and immunizations [
23,
25]. Given different risk factors for wasting and stunting, and the weak correlation between these measures in our data, it is not surprising that food access insecurity was associated with faltering in HAZ but not WHZ. In addition to different risk factors, growth faltering in WHZ tends to occur at younger ages and result in higher mortality than faltering in HAZ [
1]. Given the age of children enrolled in this study (older than 24 months), they were more likely to be stunted or healthy than to be wasted. Further research is warranted on approaches to expanding this household food access insecurity measure to more effectively capture factors associated with wasting. Patterns in SES, food access insecurity, and growth faltering were not clearly clustered by region, and no country ranked consistently highest or lowest in all factors. For example, Tanzanian households were among the poorest when measured by socioeconomic indicators, but were also among the most food access secure. We hypothesize that this difference in rankings by food access insecurity and household SES might be due to the predominantly agricultural setting, where reporting bias on food access insecurity might be more common, and where wealth may not be as closely tied to food access security as in urban settings. The opposite pattern was true of Brazilian households, which also had among the highest mean values of HAZ and WHZ scores. Our results indicate that food access insecurity was not simply an indicator of SES, but was also independently associated with growth faltering. The effect of a five-point decrease in food access insecurity was roughly comparable to the effect of a five-year increase in mother’s education on HAZ, and was approximately equal to one-third the effect of access to an improved water source. Although our analyses reveal that food access insecurity is independent of these socio-demographic indicators, these relationships warrant further exploration. The complexity of these relationships underlines the utility of a simple measure, such as the HFIAS, that could potentially predict growth faltering in children. The Food And Nutrition Technical Assistance (FANTA) project has worked since 2000 to validate and adapt the HFIAS [
18]. Recent validation work in multiple countries has produced mixed results, leading investigators to suggest a shortened version of the scale, called the Household Hunger Scale, comprising only the final three items related to hunger [
26]. The adapted version of the scale did not achieve statistical significance, suggesting that the full scale may be a better measure of chronic malnutrition, or that these two scales capture different information. However, in the context of the MAL-ED study, the full scale is more appropriate than the reduced scale for two reasons. First, more items generally result in higher scale reliability [
27]. Second, we seek to measure the full experience of food access insecurity to facilitate exploration of the relationships between food access, food utilization, enteric infections, and nutritional markers in the early years of life. These results also provide evidence of the acceptability and validity of the nine-item HFIAS in a multi-country research setting. We were able to use the questions in their original form (with translation) in diverse cultural settings with limited problems in administration and no missing data. Our results, demonstrating a statistically significant relationship between food access insecurity and HAZ – two variables that we would expect to be correlated – provide evidence of the construct validity of the HFIAS scale in a multi-country setting [
28]. Furthermore, although this measure only focuses on the access aspect of food insecurity, previous research has indicated that it correlates with dietary quality and the intake of a micronutrient rich diet, two aspects of food utilization [
20]. Finally, the lack of heterogeneity in this relationship across countries provides evidence of generalizability of its use in diverse low-income settings. The MAL-ED cohort study will allow us to look at food utilization and its relationship with food access more closely through inclusion of longitudinal measures of dietary intake and repeated measurement of food access insecurity. Our study has some potential limitations. The data are cross-sectional, preventing the collection of important longitudinal risk factors for malnutrition, such as intestinal infections. However, the statistically significant association between food access insecurity and HAZ indicates the utility of a short food security survey to screen for chronic malnutrition in settings where other data are not available. Our pilot study included children aged 24 to 60 months, although wasting effects are often greatest in the first two years of life [
1]. The MAL-ED cohort study will follow children from birth, collecting data on diarrheal incidence and infectious agents, seasonal changes in food access insecurity, and other important exposures, such as dietary intake. In addition, some MAL-ED study sites raised concerns that responses to certain food access insecurity items might be culturally dependent, as has been shown by Coates and colleagues [
14]. For example, although researchers in the Pakistan site felt that the HFIAS was robust to concerns, they noted the potential for bias given cultural stigma against reporting food insecurity. These differences are particularly relevant with regard to selecting universal cut points for food access insecurity, rather than associations between the continuous measure and outcomes. While further inquiry is warranted on cross-country variations in response thresholds, previous research indicates that the domains of food access insecurity that form the basis of the nine-item scale are similar across cultural settings (i.e. insufficient quantity, inadequate quality, and uncertainty or worry) [
14]. Also, our pilot study was not designed to assess the important role of seasonality in household food access insecurity (Additional file
1 and Additional file
2); however, we are assessing seasonality in the MAL-ED cohort study, in which we are measuring food access insecurity every six months based on child enrollment. Finally, factors affecting child growth are present not only at the individual and household levels but also at the community, national, and regional levels. Information provided through a household survey can only explain a limited amount of variation in child growth outcomes [
29]. In summary, a simple household food access insecurity score can help explain differences in HAZ distributions in a multi-country study, even after adjustment for demographic and SES indicators, and country-level differences. While we do not suggest that this tool should replace the collection of child anthropometry to assess nutritional status, it could be used as a rapid assessment tool to identify households at risk of child growth faltering. Given the simplicity of this measure, and its acceptability and validity in cross-country settings, we advocate its inclusion in research and programs seeking to understand and ameliorate the predictors of child malnutrition in developing countries.
Acknowledgements
MAL-ED Network Investigators by region: Africa: In South Africa: Pascal Bessong (University of Venda, Thohoyandou, South Africa), Angelina Mapula (University of Venda, Thohoyandou, South Africa), Emanuel Nyathi (University of Venda, Thohoyandou, South Africa), Cloupas Mahopo (University of Venda, Thohoyandou, South Africa), Amidou Samie (University of Venda, Thohoyandou, South Africa), Cebisa Nesamvuni (University of Venda, Thohoyandou, South Africa); In Tanzania: Erling Svensen (Haydom Lutheran Hospital, University of Bergen, Norway), Estomih R. Mduma (Haydom Lutheran Hospital, Haydom, Tanzania), Crystal L. Patil (University of Illinois, Urbana-Champaign, IL, USA), Caroline Amour (Haydom Lutheran Hospital, Haydom, Tanzania): South America: In Brazil: Aldo A. M. Lima (Universidade Federal do Ceara, Fortaleza, Brazil), Reinaldo B. Oriá (Universidade Federal do Ceara, Fortaleza, Brazil), Noélia L. Lima (Universidade Federal do Ceara, Fortaleza, Brazil), Alberto M. Soares, (Universidade Federal do Ceara, Fortaleza, Brazil), Alexandre H. Bindá (Universidade Federal do Ceara, Fortaleza, Brazil), Ila F. N. Lima (Universidade Federal do Ceara, Fortaleza, Brazil), Josiane S. Quetz (Universidade Federal do Ceara, Fortaleza, Brazil), Milena L. Moraes (Universidade Federal do Ceara, Fortaleza, Brazil). Bruna L. L. Maciel (Universidade Federal do Ceara, Fortaleza, Brazil), Hilda Costa (Universidade Federal do Ceara, Fortaleza, Brazil), Jose Quirino Filho (Universidade Federal do Ceara, Fortaleza, Brazil), Álvaro J. M. Leite (Universidade Federal do Ceara, Fortaleza, Brazil), Francisco B. Mota (Universidade Federal do Ceara, Fortaleza, Brazil), Alessandra F. Di Moura (Universidade Federal do Ceara, Fortaleza, Brazil); In Peru: Maribel Paredes Olortegui (A.B. PRISMA, Iquitos, Peru), Cesar Banda Chavez (A.B. PRISMA, Iquitos, Peru), Dixner Rengifo Trigoso (A.B. PRISMA, Iquitos, Peru), Julian Torres Flores (A.B. PRISMA, Iquitos, Peru), Angel Orbe Vasquez (A.B. PRISMA, Iquitos, Peru), Silvia Rengifo Pinedo (A.B. PRISMA, Iquitos, Peru), Angel Mendez Acosta (A.B. PRISMA, Iquitos, Peru); South Asia: In Bangladesh: Tahmeed Ahmed (ICDDR-B, Dhaka, Bangladesh), Rashidul Haque (ICDDR-B, Dhaka, Bangladesh), AM Shamsir Ahmed (ICDDR-B, Dhaka, Bangladesh), Munirul Islam, (ICDDR-B, Dhaka, Bangladesh), Iqbal Hossain (ICDDR-B, Dhaka, Bangladesh), Mustafa Mahfuz (ICDDR-B, Dhaka, Bangladesh), Dinesh Mondol (ICDDR-B, Dhaka, Bangladesh), Fahmida Tofail (ICDDR-B, Dhaka, Bangladesh); In India: Gagandeep Kang (Christian Medical College, Vellore, India), Sushil John (Christian Medical College, Vellore, India), Sudhir Babji (Christian Medical College, Vellore, India), Mohan Venkata Raghava (Christian Medical College, Vellore, India), Anuradha Rose (Christian Medical College, Vellore, India), Beena Kurien (Christian Medical College, Vellore, India), Anuradha Bose (Christian Medical College, Vellore, India), Jayaprakash Muliyil (Christian Medical College, Vellore, India), Anup Ramachandran (Christian Medical College, Vellore, India); In Nepal: Carl J Mason (Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand), Prakash Sunder Shrestha (Institute of Medicine, Tribuhvan University, Kathmandu, Nepal), Sanjaya Kumar Shrestha (Walter Reed/AFRIMS Research Unit, Kathmandu, Nepal), Ladaporn Bodhidatta, (Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand), Ram Krishna Chandyo (Institute of Medicine, Tribuhvan University, Kathmandu, Nepal), Rita Shrestha (Institute of Medicine, Tribuhvan University, Kathmandu, Nepal), Binob Shrestha (Walter Reed/AFRIMS Research Unit, Kathmandu), Tor Strand (University of Bergen, Bergen, Norway), Manjeswori Ulak (Institute of Medicine, Tribuhvan University, Kathmandu, Nepal); In Pakistan: Zulfiqar A Bhutta (Aga Khan University, Naushahro Feroze, Pakistan), Anita K M Zaidi (Aga Khan University, Naushahro Feroze, Pakistan), Sajid Soofi (Aga Khan University, Naushahro Feroze, Pakistan), Ali Turab (Aga Khan University, Naushahro Feroze, Pakistan), Didar Alam (Aga Khan University, Naushahro Feroze, Pakistan), Shahida Qureshi (Aga Khan University, Naushahro Feroze, Pakistan), Aisha K Yousafzai (Aga Khan University, Naushahro Feroze, Pakistan), Asad Ali (Aga Khan University, Naushahro Feroze, Pakistan), Imran Ahmed (Aga Khan University, Naushahro Feroze, Pakistan), Sajad Memon (Aga Khan University, Naushahro Feroze, Pakistan), Muneera Rasheed (Aga Khan University, Naushahro Feroze, Pakistan); North America: In the United States: Michael Gottlieb (Foundation for the NIH, Bethesda, MD, USA), Mark Miller (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Karen H. Tountas (Foundation for the NIH, Bethesda, MD, USA), Rebecca Blank (Foundation for the NIH, Bethesda, MD, USA), Dennis Lang, (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Stacey Knobler (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Monica McGrath (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Stephanie Richard (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Jessica Seidman (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Zeba Rasmussen (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Ramya Ambikapathi (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Benjamin McCormick (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Stephanie Psaki (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Vivek Charu (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Jhanelle Graham (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Gaurvika Nayyar (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Viyada Doan (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Leyfou Dabo (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Danny Carreon (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Archana Mohale (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Christel Host (Fogarty International Center/National Institutes of Health, Bethesda, MD, USA), Dick Guerrant (University of Virginia, Charlottesville, VA, USA), Bill Petri (University of Virginia, Charlottesville, VA, USA), Eric Houpt (University of Virginia, Charlottesville, VA, USA), Jean Gratz (University of Virginia, Charlottesville, VA, USA), Leah Barrett (University of Virginia, Charlottesville, VA, USA), Rebecca Scharf (University of Virginia, Charlottesville, VA, USA), Laura Caulfield (Johns Hopkins University, Baltimore, MD, USA), William Checkley (Johns Hopkins University, Baltimore, MD, USA), Margaret Kosek (Johns Hopkins University, Baltimore, MD, USA), Pablo Penataro Yori (Johns Hopkins University, Baltimore, MD, USA), Gwenyth Lee (Johns Hopkins University, Baltimore, MD, USA), Ping Chen (Johns Hopkins University, Baltimore, MD, USA), Robert Black (Johns Hopkins University, Baltimore, MD, USA), Laura Murray-Kolb (Pennsylvania State University, University Park, PA, USA), Barbara Schaefer (Pennsylvania State University, University Park, PA, USA), William Pan (Duke University, Durham, NC, USA).
Funding
The Etiology, Risk Factors and Interactions of Enteric Infections and Malnutrition and the Consequences for Child Health and Development Project (MAL-ED) is carried out as a collaborative project supported by the Bill & Melinda Gates Foundation. William Checkley was further supported by a Clinician Scientist Award from the Johns Hopkins University and a K99/R00 Pathway to Independence Award (K99HL096955) from the National Heart, Lung and Blood Institute, National Institutes of Health.