Consumption of micronutrient-fortified milk and noodles is associated with lower risk of stunting in preschool-aged children in Indonesia

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1 Consumption of micronutrient-fortified milk and noodles is associated with lower risk of stunting in preschool-aged children in Indonesia Richard D. Semba, Regina Moench-Pfanner, Kai Sun, Saskia de Pee, Nasima Akhter, Jee Hyun Rah, Ashley A. Campbell, Jane Badham, Martin W. Bloem, and Klaus Kraemer Abstract Background. Stunting is highly prevalent in developing countries and is associated with greater morbidity and mortality. Micronutrient deficiencies contribute to stunting, and micronutrient-fortified foods are a potential strategy to reduce child stunting. Objective. To examine the relationship between the use of fortified powdered milk and noodles and child stunting in a large, population-based sample of Indonesian children. Methods. Consumption of fortified milk and fortified noodles was assessed in children 6 to 59 months of age from 222,250 families living in rural areas and 79,940 families living in urban slum areas in Indonesia. Results. The proportions of children who consumed fortified milk and fortified noodles were 34.0% and 22.0%, respectively, in rural families, and 42.4% and 48.5%, respectively, in urban families. The prevalence of stunting among children from rural and urban families was 51.8% and 48.8%, respectively. Children from rural and urban families were less likely to be stunted if they consumed fortified milk (in rural areas, OR = 0.87; 95% CI, 0.85 to 0.90; p <.0001; in urban areas, OR = 0.80; 95% CI, 0.76 to 0.85; p <.0001) or fortified noodles (in rural areas, OR = 0.95; 95% CI, 0.91 to 0.99; p =.02; in urban areas, OR = 0.95; 95% CI, 0.91 to 1.01; p =.08) Richard D. Semba, Kai Sun, and Ashley A. Campbell are affiliated with the Department of Ophthalmology, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA; Regina Moench-Pfanner is affiliated with the Global Alliance for Improved Nutrition, Geneva; Saskia de Pee and Martin W. Bloem are affiliated with the Nutrition Service, Policy, Strategy and Programme Support Division, World Food Programme, Rome; Nasima Akhter is affiliated with Helen Keller International, New York; Jee Hyun Rah and Klaus Kraemer are affiliated with the DSM-WFP Partnership, Sight and Life, Kaiseraugst, Basel, Switzerland; Jane Badham is affiliated with JB Consultancy, Durban, South Africa. Please direct queries to the corresponding author: Richard D. Semba, Johns Hopkins University School of Medicine, Smith Building, M015, 400 N. Broadway, Baltimore, MD 21287, USA; rdsemba@jhmi.edu. in multiple logistic regression models adjusted for potential confounders. In both rural and urban families, the odds of stunting were lower when a child who consumed fortified milk also consumed fortified noodles, or when a child who consumed fortified noodles also consumed fortified milk. Conclusions. The consumption of fortified milk and noodles is associated with decreased odds of stunting among Indonesian children. These findings add to a growing body of evidence regarding the potential benefits of multiple micronutrient fortification on child growth. Key words: Fortification, micronutrients, milk, noodles, stunting Introduction Stunting is linear growth failure due to poor nutrition and infections in the pre- and postnatal periods [1] and affects nearly one-third of children under 5 years of age in developing countries [2]. Stunting is associated with poor child development and increased mortality [1, 3]. Stunted children do not reach their full growth potential and become stunted adolescents and adults [4] with reduced work capacity [5]. Women who were stunted have an increased risk of mortality during childbirth [6] and adverse birth outcomes [7, 8]. Multiple micronutrient deficiencies are common among poor families in South and Southeast Asia owing to low dietary diversity and limited access to animal-source foods. Micronutrients such as vitamin A, iron, and zinc are important for adequate growth of children [9]. Child stunting is a result of long-term consumption of a low-quality diet in combination with morbidity, infectious diseases, and environmental problems. Fortified foods may provide micronutrients that are crucial to infants as they make the transition from a diet of exclusively breastmilk to a mixed diet that includes breastmilk and other foods. Since the Food and Nutrition Bulletin, vol. 32, no , The United Nations University. 347

2 348 R. D. Semba mid-1990s, fortification of powdered milk with vitamins and minerals has been mandatory in Indonesia, and about one-half of instant noodles have been voluntarily fortified. The use of fortified powdered milk is fairly common in Indonesia, but the use of fortified instant noodles is less common, especially among households in remote rural areas [11]. The relationship between the consumption of fortified powdered milk and fortified noodles and health outcomes has not been well characterized. We hypothesized that young children aged 6 to 59 months who consumed micronutrient-fortified powdered milk and/or micronutrient-fortified noodles were at lower risk for stunting. To address this hypothesis, we examined the relationship between the use of fortified powdered milk and noodles and child stunting in a large, population-based sample of families from Indonesia. Subjects and methods The study subjects consisted of families from rural and urban areas that participated in the Nutritional Surveillance System (NSS) in Indonesia from January 1999 to September The NSS was established by the Ministry of Health, Government of Indonesia, and Helen Keller International in 1995 [11]. The NSS was based upon UNICEF s conceptual framework on the causes of malnutrition [12], with the underlying principle to monitor public health problems and guide policy decisions [13]. The NSS used stratified multistage cluster sampling of households in subdistricts of administrative divisions of the country in rural areas and slum areas of large cities. Data were collected from approximately 40,000 randomly selected households every quarter and involved five major urban poor populations from slum areas in the cities of Jakarta, Surabaya, Makassar, Semarang, and Padang and the rural population from the provinces of Lampung, Banten, West Java, Central Java, East Java, the island of Lombok (West Nusatenggara), and South Sulawesi. New households were selected every round. Data were collected by two-person field teams. A structured, coded questionnaire was used to record data on children aged 0 to 59 months, including anthropometric measurements, date of birth, and sex. The mother of the child or other adult member of the household was asked to provide information on the household s composition, parental education, and weekly household expenditures, along with other indicators of socioeconomic status, environmental sanitation, and health. Information was collected on the place where family members defecated, categorized as open defecation (river, pond, beach, bush, open space, garden), open unimproved pit latrine, and closed (improved) latrine (pit latrine with slab, ventilated pit latrine, flush/pour latrine). For each child in the family, data were collected on whether the child had received a vitamin A capsule and a deworming medication in the previous 6 months. The field teams also tested a sample of table salt from the household for the presence of iodine, as described in detail elsewhere [14]. For each child in the family, data were collected on whether the child had consumed industrially produced milk products in the previous week, the brand of the product, and how much money was spent on the milk product in the previous week. Similar data were collected on whether the child had consumed instant noodles in the previous week, the brand of the product (which allowed classification of noodles as fortified or not), and how much was spent on the noodles in the previous week. Milk products were fortified with vitamin A, vitamin C, vitamin D, vitamin E, vitamin K, vitamin B 12, thiamin, and riboflavin. Noodles were fortified with vitamin A, vitamin B 6, vitamin B 12, thiamin, niacin, folate, and iron. The field teams measured and recorded the weight of each child aged 0 to 59 months with a precision of 0.1 kg and the length/height with a precision of 0.1 cm. The birth dates of the children were estimated with the use of a calendar of local and national events and converted to the Gregorian calendar. Height-forage z-scores were calculated using the World Health Organization (WHO) Child Growth Standards as the reference growth curves [15]. Children with heightfor-age z-scores less than < 2 SD were considered stunted [15]. The participation rate of families in the surveillance system was greater than 97% in both the urban slum and the rural areas. The main reason for nonresponse was that the family had moved out of the area or was absent at the time the interviews were conducted. The rate of nonresponse because of refusal to participate in the surveillance system was very low (less than 1%). In each household, data were gathered regarding the expenditures in the previous week. Expenditure and price variables were collected in Indonesian rupiah. For this analysis, expenditures are presented in US dollars to control for the fluctuation of the Indonesian rupiah. In Indonesia, monthly exchange rates from 2000 to 2003 were established with the use of historic data publicly available through the Bank of Canada [16]. Mean exchange rates by data collection round were calculated based upon the months in which data were collected for each round. Expenditure and price variables in US dollars per round were created and calculated with the use of the exchange rates by round. The study protocol complied with the principles enunciated in the Helsinki Declaration [17]. The field teams were instructed to explain the purpose of the nutrition surveillance system and data collection to each child s mother or caretaker and, if he was present, the father and/or household head; data collection

3 Fortified foods and child stunting proceeded only after written informed consent had been obtained. Participation was voluntary, no remuneration was provided to subjects, and all subjects were free to withdraw at any stage of the interview. The NSS in Indonesia was approved by the Ministry of Health, Government of Indonesia. The plan for secondary data analysis was approved by the Institutional Review Board of the Johns Hopkins University School of Medicine. The study was limited to children aged 6 to 59 months because the use of fortified milk and noodles in children under 6 months was uncommon and exclusive breastfeeding is recommended during this period. For families with more than one child aged 6 to 59 months, the analysis was limited to the youngest child only (i.e., families were not counted more than once, because stunting tends to cluster within families). Maternal age was divided into quartiles. Maternal and paternal education was categorized as 0, 1 to 6 (primary school), 7 to 9 (junior high school), or 10 or more (high school or greater) years. The proportion of mothers and fathers with more than 12 years of education (i.e., high school graduates) was small (2.3% and 3.8%, respectively), and these parents were therefore included in the category of those with 10 or more years of education. Weighting was used to adjust for urban and rural population size, by city and province, respectively, and all results are weighted. Weekly per capita household expenditure was used as the main indicator of socioeconomic status. A crowded household was defined one in which more than four individuals were eating meals from the same kitchen. Chi-square tests were used to compare categorical variables between groups. Analysis of variance (ANOVA) was used to compare the adjusted prevalence of stunting across groups by expenditure. Multivariate logistic regression models were used to examine the relationship between child stunting and the use of fortified milk versus no fortified milk, the use of fortified noodles versus no fortified noodles, and the use of both fortified milk and noodles versus no fortified milk or noodles. Models were tested for interactions between fortified milk and fortified noodles. Variables were included in the multivariate models if they were significant in univariate analyses. A relationship with p <.05 was considered significant. Covariance matrices were used to examine for multicollinearity among independent variables in the models. Data analyses were conducted with the use of SAS Survey. Results In 222,250 families from rural areas and 79,940 families from urban slum areas, the proportion of children aged 6 to 59 months who consumed fortified milk was 34.0% and 42.4%, respectively, and the proportion of 349 children who consumed fortified noodles was 22.0% and 48.5%, respectively. The prevalence of stunting among children from rural and urban slum families was 51.8% and 48.8%, respectively. The relationship of demographic and other characteristics of families from rural areas and urban slum areas with child stunting is shown in table 1. Factors associated with a greater proportion of child stunting were younger child age, male sex, lower maternal age, lower maternal education, lower paternal education, current breastfeeding, deworming, history of diarrhea, paternal smoking, more than four household members eating from the same kitchen, and lower weekly per capita household expenditure. Factors associated with a lower proportion of child stunting were consumption of fortified milk, consumption of fortified noodles, consumption of both fortified milk and fortified noodles, vitamin A supplementation, presence of an improved latrine in the household, and the use of adequately iodized salt. These findings were consistent for families from both rural areas and urban slum areas, except for child s sex, which was not significant for families from urban slum areas. Continuous variables, such as maternal height, weekly per capita expenditure for animal-source food, and weekly per capita expenditure for plant food, are compared between families with and without a stunted child in table 2. In both rural and urban families, maternal height and per capita expenditure on animalsource and plant foods was significantly lower for families with stunted children. The relationship between consumption of fortified milk and noodles and child stunting was examined in separate multiple logistic regression models for families from rural areas and urban slum areas (table 3). In rural and urban families, consumption of fortified milk was significantly associated with lower odds of child stunting in separate multiple logistic regression models after adjustment for child s age, child s sex, maternal age, maternal education, maternal height, current breastfeeding, vitamin A supplementation, deworming, history of diarrhea, household with an improved latrine, adequately iodized salt, paternal smoking, expenditure for animal-source food, expenditure for plant food, household size, weekly per capita household expenditure, and location. In rural families, consumption of fortified noodles was significantly associated with lower odds of child stunting, but the association only reached marginal significance (p =.08) in the multivariate models. An interaction was found between the consumption of fortified milk and fortified noodles in both rural families (p <.0001) and urban families (p <.0001). In rural families, the consumption of fortified milk was associated with lower odds of child stunting when the child who consumed fortified milk also consumed fortified noodles (OR = 0.74; 95% CI, 0.70

4 350 R. D. Semba TABLE 1. Demographic and other factors in relation to stunting in children aged 6 to 59 months from families in rural areas and urban slum areas of Indonesia Characteristic a Rural Urban n Stunting (%) p b n Stunting (%) p b Child consumes fortified milk Yes 75, < , <.0001 No 145, , Child consumes fortified noodles Yes 48, < , <.0001 No 173, , Child consumes both fortified milk and fortified noodles Yes 23, < , <.0001 No 199, , Child s age (mo) , < , < , , , , Child s sex Male 112, < , Female 109, , Maternal age (yr) 24 50, < , < , , , , , , Maternal education (yr) 0 13, < , < , , , , , , Paternal education (yr) 0 9, < , < , , , , , , Child currently breastfeeding Yes 37, < , <.0001 No 184, , Child received vitamin A in past 6 mo Child received deworming medication in past 6 mo Yes 146, < , <.0001 No 69, , Yes 50, , <.0001 No 169, , Child had diarrhea in past 7 days Yes 12, < , <.0001 No 208, , Household has improved latrine Yes 99, < , <.0001 No 122, , Household uses adequately iodized salt Yes 148, < , <.0001 No 72, , Father is a smoker Yes 161, < , <.0001 No 55, , No. of household members eating meals from same kitchen Weekly per capita household expenditure, quintile , < , <.0001 > 4 114, , , < , < , , , , , , , , a. Missing data for variables were as follows (rural, urban): fortified milk (975, 5,374), fortified noodles (26, 4), child s age (5, 0), child s sex (0, 0), maternal age (293, 0), maternal education (1,232, 225), paternal education (10,918, 2,096), breastfeeding (220, 95), vitamin A (6,341, 3,133), deworming (2,184, 141), diarrhea (1,206, 306), improved latrine (127, 93), adequately iodized salt (1,202, 872), paternal smoking (5,158, 1,578), number of household members (21,743, 583), weekly per capita household expenditure (21,724, 238). b. Chi-square tests are used to compare categorical variables.

5 Fortified foods and child stunting 351 TABLE 2. Comparison of maternal height and animal and plant food expenditures between families with and without a stunted child mean (SD) Location Variable Stunted Not stunted p Rural Maternal height (cm) (4.9) (4.9) <.0001 Animal food expenditures, per capita per week (US$) 0.22 (0.26) 0.27 (0.38) <.0001 Plant food expenditures, per capita per week (US$) 0.26 (0.22) 0.31 (0.26) <.0001 Urban Maternal height (cm) (4.9) (4.9) <.0001 Animal food expenditures, per capita per week (US$) 0.29 (0.27) 0.32 (0.29) <.0001 Plant food expenditures, per capita per week (US$) 0.32 (0.28) 0.39 (0.28) <.0001 TABLE 3. Multiple logistic regression models for consumption of both fortified milk and fortified noodles and child stunting in families from rural and urban areas of Indonesia a Characteristic Rural Urban OR 95% CI p OR 95% CI p Child consumes fortified milk , 0.90 < , 0.85 <.0001 Child consumes fortified noodles , , Child s age (mo) , , , , 0.88 <.0001 Male child , , Maternal age, (yr) , 0.91 < , 0.88 < , 0.89 < , 0.88 < , 0.83 < , 0.81 <.0001 Maternal education (yr) , 1.68 < , 1.78 < , 1.49 < , 1.48 < , 1.27 < , 1.31 < Maternal height (cm) , < , <.0001 Child currently breastfeeding , 1.21 < , 1.39 <.0001 Child received vitamin A in past 6 mo , , Child received deworming medication in past 6 mo , 1.12 < , 1.17 <.0001 Diarrhea in past 7 days , 1.37 < , Household has an improved latrine , 0.84 < , 0.89 <.0001 Household uses adequately iodized salt , 0.92 < , Father is a smoker , 1.11 < , Plant food expenditure , 0.84 < , Animal food expenditure , 0.92 < , 0.85 <.0001 > 4 individuals eating meals from same kitchen , 1.12 < , 1.19 <.0001 Weekly per capita household expenditure, quintile , , , , , 0.93 < , , 0.89 < , Separate multiple logistic regression models were analyzed for rural and urban participants. All models were adjusted for location (province for rural model, city for urban model).

6 352 R. D. Semba to 0.79; p <.0001). The consumption of fortified noodles was associated with lower odds of child stunting when the child who consumed fortified noodles also consumed fortified milk (OR = 0.81; 95% CI, 0.77 to 0.85; p <.0001). In families from urban slum areas, the consumption of fortified milk was associated with lower odds of child stunting when the child who consumed fortified milk also consumed fortified noodles (OR = 0.72; 95% CI, 0.68 to 0.76; p <.0001). The consumption of fortified noodles was associated with lower odds of child stunting when the child who consumed fortified noodles also consumed fortified milk (OR = 0.86; 95% CI, 0.81 to 0.91; p <.0001). Families were divided into four categories based upon weekly expenditure per child on fortified milk (fig. 1) and fortified noodles (fig. 2). The prevalence of child stunting decreased across the four categories of expenditure on fortified milk in both rural and urban families after adjustment for the same covariates as in table 3 (p <.0001). The prevalence of child stunting decreased across the four categories of expenditure on fortified noodles in rural (p =.02) but not urban (p =.83) families. Discussion The present study shows that children aged 6 to 59 months who consumed either micronutrient-fortified milk or micronutrient-fortified noodles were less likely to be stunted than children who did not consume micronutrient-fortified milk. Children who consumed both micronutrient-fortified milk and micronutrientfortified noodles had the lowest risk of stunting. To our knowledge, this is the first population-based study to show an association between consumption of fortified milk and/or fortified noodles and reduced risk of stunting in children aged 6 to 59 months. The findings of the study were consistent both for children from families from rural areas and for children from families from urban slums. Whether the consumption of fortified milk and/or noodles is causally related to a lower risk of stunting cannot be definitively concluded from these results, since the observations are based upon cross-sectional associations from a nutritional surveillance program. However, such a conclusion seems reasonable. There was a graded relationship between per capita expenditure on fortified milk and the prevalence of stunting. In addition, the odds of stunting were lowest among children who consumed both fortified milk and fortified noodles. The strengths of this study are the large population-based sample size, the consistency of the results between rural and urban slum areas, and data that allowed analyses to be controlled for potential confounding factors. In epidemiologic studies, it is not possible to control for all factors, and unmeasured factors may have influenced the relationship between the use of fortified milk or fortified noodles and child stunting. In the present study, children 6 to 59 months of age who were still breastfeeding were at higher risk for stunting. These findings are consistent with those of previous studies in Uganda [18] and Nepal [19] that Stunting (%) Stunting (%) Expenditure category Expenditure category FIG. 1. Prevalence of stunting in children aged 6 to 59 months from families in rural areas (black bars) and urban slum areas (gray bars) by per capita expenditure on fortified milk. Category 0 represents zero expenditure, while categories 1, 2, and 3 represent the three tertiles of expenditure for families who used fortified milk. For rural families (0, n = 158,202; 1, n = 20,432; 2, n = 20,789; 3, n = 20,599). For urban families (0, n = 47,042; 1, n = 10,609; 2, n = 10542; 3, n = 10,578). Prevalence is adjusted for all covariates as in table 3. P <.0001 by ANOVA across the four categories for both rural and urban families FIG. 2. Prevalence of stunting in children aged 6 to 59 months from families in rural areas (black bars) and urban slum areas (gray bars) by per capita expenditure on fortified noodles. Category 0 represents zero expenditure, while categories 1, 2, and 3 represent the three tertiles of expenditure for families who used fortified noodles. For rural families (0, n = 72,922; 1, n = 49,587; 2, n = 49,399; 3, n = 49,353). For urban families (0, n = 18,749; 1, n = 20,197; 2, n = 20,171; 3, n = 20,225). Prevalence is adjusted for all covariates as in table 3. P =.02 by ANOVA across the four categories for rural families and p = 0.83 for urban families.

7 Fortified foods and child stunting have shown an association between prolonged breastfeeding and stunting. By the age of 6 months, exclusive breastfeeding is not sufficient to meet the requirements for many micronutrients. Complementary foods containing vitamin A, iron, zinc, and other micronutrients are needed in order to meet the needs of growing infants. The results of the present study do not apply to children under 6 months of age who are breastfeeding. Factors that were protective against stunting in the present study included vitamin A supplementation within the previous 6 months, presence of an improved latrine, and use of adequately iodized salt. Poor sanitation increases the risk of diarrheal disease and poor growth associated with diarrhea. These findings are consistent with those of a study in Uganda that linked lack of a latrine in the household with child stunting [20]. Correction of iodine deficiency has been shown 353 to improve linear growth [21]. Maternal education was strongly associated with a reduced risk of stunting, as was previously shown in Indonesia and Bangladesh [22]. Higher maternal education is associated with adherence to a greater number of activities that promote child health, such as complete childhood immunizations, receipt of vitamin A capsules, and use of iodized salt [22]. The results of the present study suggest that compulsory fortification of milk with micronutrients in Indonesia reduces child stunting and that the voluntary fortification of some noodles has an additional positive impact. These findings support initiatives to address stunting among preschool-aged children through the fortification of commonly eaten foods together with other public health interventions and improved education for women. References 1. Grantham-McGregor S, Cheung YB, Cueto S, Glewwe P, Richter L, Strupp B, International Child Development Steering Group. 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