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    Food and Nutrition Bulletin,vol. 32, no. 4 2011, The United Nations University. 347

    Consumption of micronutrient-fortified milk andnoodles is associated with lower risk of stunting inpreschool-aged children in Indonesia

    Abstract

    Background.Stunting is highly prevalent in developingcountries and is associated with greater morbidity andmortality. Micronutrient deficiencies contribute to stunt-ing, and micronutrient-fortified foods are a potentialstrategy to reduce child stunting.Objective.To examine the relationship between the

    use of fortified powdered milk and noodles and childstunting in a large, population-based sample of Indone-sian children.Methods.Consumption of fortified milk and fortified

    noodles was assessed in children 6 to 59 months of agefrom 222,250 families living in rural areas and 79,940families living in urban slum areas in Indonesia.

    Results.The proportions of children who consumedfortified milk and fortified noodles were 34.0% and

    22.0%, respectively, in rural families, and 42.4% and48.5%, respectively, in urban families. The prevalence ofstunting among children from rural and urban familieswas 51.8% and 48.8%, respectively. Children from ruraland urban families were less likely to be stunted if theyconsumed 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 (inrural areas, OR = 0.95; 95% CI, 0.91 to 0.99; p = .02; inurban areas, OR = 0.95; 95% CI, 0.91 to 1.01; p = .08)

    in multiple logistic regression models adjusted for poten-tial confounders. In both rural and urban families, theodds of stunting were lower when a child who consumed

    fortified milk also consumed fortified noodles, or whena child who consumed fortified noodles also consumed

    fortified milk.Conclusions.The consumption of fortified milk and

    noodles is associated with decreased odds of stuntingamong Indonesian children. These findings add to a

    growing body of evidence regarding the potential benefitsof multiple micronutrient fortification on child growth.

    Key words:Fortification, micronutrients, milk,noodles, stunting

    IntroductionStunting is linear growth failure due to poor nutritionand infections in the pre- and postnatal periods [1] andaffects nearly one-third of children under 5 years of agein developing countries [2]. Stunting is associated withpoor child development and increased mortality [1, 3].Stunted children do not reach their full growth poten-tial and become stunted adolescents and adults [4] withreduced work capacity [5]. Women who were stuntedhave an increased risk of mortality during childbirth[6] and adverse birth outcomes [7, 8].

    Multiple micronutrient deficiencies are commonamong poor families in South and Southeast Asiaowing to low dietary diversity and limited access toanimal-source foods. Micronutrients such as vitaminA, iron, and zinc are important for adequate growthof children [9]. Child stunting is a result of long-termconsumption of a low-quality diet in combinationwith morbidity, infectious diseases, and environmentalproblems.

    Fortified foods may provide micronutrients thatare crucial to infants as they make the transitionfrom a diet of exclusively breastmilk to a mixed diet

    that includes breastmilk and other foods. Since the

    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

    Richard D. Semba, Kai Sun, and Ashley A. Campbell areaffiliated with the Department of Ophthalmology, JohnsHopkins University School of Medicine, Baltimore, Maryland,USA; ReginaMoench-Pfanner is affiliated with the GlobalAlliance for Improved Nutrition, Geneva; Saskiade Pee andMartin W. Bloem are affiliated with the Nutrition Service,Policy, Strategy and Programme Support Division, WorldFood Programme, Rome; NasimaAkhter is affiliated withHelen Keller International, New York; JeeHyun Rah andKlaus Kraemer are affiliated with the DSM-WFP Partnership,Sight and Life, Kaiseraugst, Basel, Switzerland; Jane Badhamis affiliated with JB Consultancy, Durban, South Africa.

    Please direct queries to the corresponding author: RichardD. Semba, Johns Hopkins University School of Medicine,Smith Building, M015, 400 N. Broadway, Baltimore, MD21287, USA; e-mail: [email protected].

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    348 R. D. Semba

    mid-1990s, fortification of powdered milk with vita-mins and minerals has been mandatory in Indonesia,and about one-half of instant noodles have been vol-untarily fortified. The use of fortified powdered milkis fairly common in Indonesia, but the use of fortifiedinstant noodles is less common, especially among

    households in remote rural areas [11]. The relationshipbetween the consumption of fortified powdered milkand fortified noodles and health outcomes has not beenwell characterized.

    We hypothesized that young children aged 6 to59 months who consumed micronutrient-fortifiedpowdered milk and/or micronutrient-fortified noo-dles were at lower risk for stunting. To address thishypothesis, we examined the relationship between theuse of fortified powdered milk and noodles and childstunting in a large, population-based sample of familiesfrom Indonesia.

    Subjects and methods

    The study subjects consisted of families from ruraland urban areas that participated in the NutritionalSurveillance System (NSS) in Indonesia from January1999 to September 2003. The NSS was established bythe Ministry of Health, Government of Indonesia,and Helen Keller International in 1995 [11]. The NSSwas based upon UNICEFs conceptual framework on

    the causes of malnutrition [12], with the underlyingprinciple to monitor public health problems and guidepolicy decisions [13]. The NSS used stratified multi-stage cluster sampling of households in subdistricts ofadministrative divisions of the country in rural areasand slum areas of large cities. Data were collected fromapproximately 40,000 randomly selected householdsevery quarter and involved five major urban poorpopulations from slum areas in the cities of Jakarta,Surabaya, Makassar, Semarang, and Padang and therural 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 chil-dren aged 0 to 59 months, including anthropometricmeasurements, date of birth, and sex. The mother ofthe child or other adult member of the household wasasked to provide information on the households com-position, parental education, and weekly householdexpenditures, along with other indicators of socio-economic 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), openunimproved pit latrine, and closed (improved) latrine(pit latrine with slab, ventilated pit latrine, flush/pour

    latrine). For each child in the family, data were col-lected on whether the child had received a vitamin Acapsule and a deworming medication in the previous6 months. The field teams also tested a sample of tablesalt from the household for the presence of iodine, asdescribed in detail elsewhere [14].

    For each child in the family, data were collected onwhether the child had consumed industrially producedmilk products in the previous week, the brand of theproduct, and how much money was spent on the milkproduct in the previous week. Similar data were col-lected on whether the child had consumed instantnoodles in the previous week, the brand of the product(which allowed classification of noodles as fortifiedor not), and how much was spent on the noodles inthe previous week. Milk products were fortified withvitamin A, vitamin C, vitamin D, vitamin E, vitaminK, vitamin B

    12

    , thiamin, and riboflavin. Noodles werefortified with vitamin A, vitamin B6, vitamin B12, thia-min, niacin, folate, and iron.

    The field teams measured and recorded the weightof each child aged 0 to 59 months with a precisionof 0.1 kg and the length/height with a precision of0.1 cm. The birth dates of the children were estimatedwith the use of a calendar of local and national eventsand converted to the Gregorian calendar. Height-for-age z-scores were calculated using the World HealthOrganization (WHO) Child Growth Standards as thereference growth curves [15]. Children with height-

    for-age z-scores less than < 2 SD were consideredstunted [15].The participation rate of families in the surveillance

    system was greater than 97% in both the urban slumand the rural areas. The main reason for nonresponsewas that the family had moved out of the area or wasabsent at the time the interviews were conducted. Therate of nonresponse because of refusal to participatein the surveillance system was very low (less than 1%).

    In each household, data were gathered regarding theexpenditures in the previous week. Expenditure andprice variables were collected in Indonesian rupiah. For

    this analysis, expenditures are presented in US dollarsto control for the fluctuation of the Indonesian rupiah.In Indonesia, monthly exchange rates from 2000 to2003 were established with the use of historic data pub-licly available through the Bank of Canada [16]. Meanexchange rates by data collection round were calculatedbased upon the months in which data were collectedfor each round. Expenditure and price variables in USdollars per round were created and calculated with theuse of the exchange rates by round.

    The study protocol complied with the principlesenunciated in the Helsinki Declaration [17]. The field

    teams were instructed to explain the purpose of thenutrition surveillance system and data collection toeach childs mother or caretaker and, if he was present,the father and/or household head; data collection

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    349Fortified foods and child stunting

    proceeded only after written informed consent hadbeen obtained. Participation was voluntary, no remu-neration was provided to subjects, and all subjectswere free to withdraw at any stage of the interview.The NSS in Indonesia was approved by the Ministryof Health, Government of Indonesia. The plan for sec-

    ondary data analysis was approved by the InstitutionalReview Board of the Johns Hopkins University Schoolof Medicine.

    The study was limited to children aged 6 to 59months because the use of fortified milk and noodlesin children under 6 months was uncommon andexclusive breastfeeding is recommended during thisperiod. For families with more than one child aged 6to 59 months, the analysis was limited to the youngestchild only (i.e., families were not counted more thanonce, because stunting tends to cluster within families).Maternal age was divided into quartiles. Maternal andpaternal education was categorized as 0, 1 to 6 (primaryschool), 7 to 9 (junior high school), or 10 or more (highschool or greater) years. The proportion of mothers andfathers with more than 12 years of education (i.e., highschool graduates) was small (2.3% and 3.8%, respec-tively), and these parents were therefore included inthe category of those with 10 or more years of educa-tion. Weighting was used to adjust for urban and ruralpopulation size, by city and province, respectively, andall results are weighted.

    Weekly per capita household expenditure was used

    as the main indicator of socioeconomic status. Acrowded household was defined one in which morethan four individuals were eating meals from the samekitchen. Chi-square tests were used to compare cat-egorical variables between groups. Analysis of variance(ANOVA) was used to compare the adjusted prevalenceof stunting across groups by expenditure. Multivariatelogistic regression models were used to examine therelationship between child stunting and the use offortified milk versus no fortified milk, the use of forti-fied noodles versus no fortified noodles, and the useof both fortified milk and noodles versus no fortified

    milk or noodles. Models were tested for interactionsbetween fortified milk and fortified noodles. Variableswere included in the multivariate models if they weresignificant in univariate analyses. A relationship with

    p< .05 was considered significant. Covariance matri-ces were used to examine for multicollinearity amongindependent variables in the models. Data analyseswere conducted with the use of SAS Survey.

    Results

    In 222,250 families from rural areas and 79,940 fami-lies from urban slum areas, the proportion of childrenaged 6 to 59 months who consumed fortified milk was34.0% and 42.4%, respectively, and the proportion of

    children who consumed fortified noodles was 22.0%and 48.5%, respectively. The prevalence of stuntingamong children from rural and urban slum familieswas 51.8% and 48.8%, respectively.

    The relationship of demographic and other charac-teristics of families from rural areas and urban slum

    areas with child stunting is shown in table 1. Factorsassociated with a greater proportion of child stuntingwere 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 mem-bers eating from the same kitchen, and lower weeklyper capita household expenditure. Factors associatedwith a lower proportion of child stunting were con-sumption of fortified milk, consumption of fortifiednoodles, consumption of both fortified milk and forti-fied noodles, vitamin A supplementation, presence ofan improved latrine in the household, and the use ofadequately iodized salt. These findings were consist-ent for families from both rural areas and urban slumareas, except for childs sex, which was not significantfor 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, arecompared between families with and without a stuntedchild in table 2. In both rural and urban families,maternal height and per capita expenditure on animal-

    source and plant foods was significantly lower forfamilies with stunted children.The relationship between consumption of fortified

    milk and noodles and child stunting was examined inseparate multiple logistic regression models for familiesfrom rural areas and urban slum areas (table 3). Inrural and urban families, consumption of fortified milkwas significantly associated with lower odds of childstunting in separate multiple logistic regression modelsafter adjustment for childs age, childs sex, maternalage, maternal education, maternal height, currentbreastfeeding, vitamin A supplementation, deworm-

    ing, history of diarrhea, household with an improvedlatrine, adequately iodized salt, paternal smoking,expenditure for animal-source food, expenditure forplant food, household size, weekly per capita householdexpenditure, and location. In rural families, consump-tion of fortified noodles was significantly associatedwith lower odds of child stunting, but the associationonly reached marginal significance (p= .08) in themultivariate models.

    An interaction was found between the consump-tion of fortified milk and fortified noodles in bothrural families (p< .0001) and urban families (p 4 114,233 56.9 40,542 52.1

    Weekly per capita householdexpenditure, quintile

    1 40,106 60.6 < .0001 15,942 56.2 < .0001

    2 40,103 55.5 15,937 51.2

    3 40,107 51.6 15,947 48.5

    4 40,105 47.7 15,934 46.4

    5 40,105 42.3 15,942 41.7

    a. Missing data for variables were as follows (rural, urban): fortif ied milk (975, 5,374), fortified noodles (26, 4), childs age (5, 0), childs 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.

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    351Fortified foods and child stunting

    TABLE 2. Comparison of maternal height and animal and plant food expenditures between families with and without astunted child mean (SD)

    Location Variable Stunted Not stunted p

    Rural Maternal height (cm) 148.8 (4.9) 141.2 (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) 148.8 (4.9) 151.3 (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 stuntingin families from rural and urban areas of Indonesiaa

    Characteristic

    Rural Urban

    OR 95% CI p OR 95% CI p

    Child consumes fortified milk 0.87 0.85, 0.90 < .0001 0.80 0.76, 0.85 < .0001

    Child consumes fortified noodles 0.95 0.91, 0.99 .02 0.95 0.91, 1.01 .08Childs age (mo) 611 1.00 1.00

    1223 1.03 0.99, 1.06 .09 0.94 0.90, 0.98 .003

    2459 0.94 0.91, 0.97 .0001 0.83 0.79, 0.88 < .0001

    pfor trend < .0001 pfor trend < .0001

    Male child 1.03 1.01, 1.05 .03 1.03 0.99, 1.07 .13

    Maternal age, (yr) 24 1.00 1.00

    2528 0.88 0.85, 0.91 < .0001 0.84 0.79, 0.88 < .0001

    2932 0.86 0.83, 0.89 < .0001 0.83 0.78, 0.88 < .0001

    33 0.80 0.77, 0.83 < .0001 0.77 0.72, 0.81 < .0001

    pfor trend < .0001 pfor trend < .0001Maternal education (yr) 0 1.57 1.46, 1.68 < .0001 1.62 1.47, 1.78 < .0001

    16 1.44 1.38, 1.49 < .0001 1.41 1.34, 1.48 < .0001

    79 1.22 1.17, 1.27 < .0001 1.24 1.17, 1.31 < .0001

    10 1.00 1.00

    pfor trend < .0001 pfor trend < .0001

    Maternal height (cm) 0.902 0.900, 0.904 < .0001 0.898 0.894, 0.901 < .0001

    Child currently breastfeeding 1.17 1.13, 1.21 < .0001 1.32 1.25, 1.39 < .0001

    Child received vitamin A in past 6 mo 0.96 0.93, 0.99 .005 0.97 0.93, 1.01 .17

    Child received deworming medication in past 6 mo 1.09 1.06, 1.12 < .0001 1.12 1.07, 1.17 < .0001

    Diarrhea in past 7 days 1.30 1.22, 1.37 < .0001 1.09 1.01, 1.18 .02

    Household has an improved latrine 0.81 0.79, 0.84 < .0001 0.85 0.81, 0.89 < .0001

    Household uses adequately iodized salt 0.89 0.87, 0.92 < .0001 0.94 0.90, 0.98 .005

    Father is a smoker 1.08 1.05, 1.11 < .0001 1.03 0.98, 1.07 .22

    Plant food expenditure 0.79 0.74, 0.84 < .0001 0.86 0.79, 0.94 .0006

    Animal food expenditure 0.87 0.82, 0.92 < .0001 0.78 0.72, 0.85 < .0001

    > 4 individuals eating meals from same kitchen 1.09 1.06, 1.12 < .0001 1.14 1.09, 1.19 < .0001

    Weekly per capita householdexpenditure, quintile

    1 1.00 1.00

    2 0.97 0.93, 1.01 .14 0.95 0.89, 1.01 .09

    3 0.92 0.88, 0.96 .0001 0.93 0.87, 0.99 .034 0.89 0.85, 0.93 < .0001 0.97 0.90, 1.04 .37

    5 0.84 0.80, 0.89 < .0001 0.87 0.80, 0.94 .0005

    pfor trend < .0001 pfor trend < .0001

    Separate multiple logistic regression models were analyzed for rural and urban participants. All models were adjusted for location (provincefor rural model, city for urban model).

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    352 R. D. Semba

    to 0.79;p< .0001). The consumption of fortified noo-dles was associated with lower odds of child stuntingwhen the child who consumed fortified noodles alsoconsumed fortified milk (OR = 0.81; 95% CI, 0.77 to0.85; p< .0001). In families from urban slum areas,the consumption of fortified milk was associated

    with lower odds of child stunting when the child whoconsumed fortified milk also consumed fortified noo-dles (OR = 0.72; 95% CI, 0.68 to 0.76;p< .0001). Theconsumption of fortified noodles was associated withlower odds of child stunting when the child who con-sumed fortified noodles also consumed fortified milk(OR = 0.86; 95% CI, 0.81 to 0.91;p< .0001).

    Families were divided into four categories basedupon weekly expenditure per child on fortified milk(fig. 1) and fortified noodles (fig. 2). The prevalenceof child stunting decreased across the four categories ofexpenditure on fortified milk in both rural and urbanfamilies after adjustment for the same covariates as intable 3 (p< .0001). The prevalence of child stuntingdecreased across the four categories of expenditureon fortified noodles in rural (p= .02) but not urban(p= .83) families.

    Discussion

    The present study shows that children aged 6 to 59months who consumed either micronutrient-fortified

    milk or micronutrient-fortified noodles were less likelyto be stunted than children who did not consumemicronutrient-fortified milk. Children who consumed

    both micronutrient-fortified milk and micronutrient-fortified noodles had the lowest risk of stunting. To ourknowledge, this is the first population-based study toshow an association between consumption of fortifiedmilk and/or fortified noodles and reduced risk of stunt-ing in children aged 6 to 59 months. The findings of the

    study were consistent both for children from familiesfrom rural areas and for children from families fromurban slums.

    Whether the consumption of fortified milk and/ornoodles is causally related to a lower risk of stuntingcannot be definitively concluded from these results,since the observations are based upon cross-sectionalassociations from a nutritional surveillance program.However, such a conclusion seems reasonable. Therewas a graded relationship between per capita expendi-ture on fortified milk and the prevalence of stunting.In addition, the odds of stunting were lowest amongchildren who consumed both fortified milk and forti-fied noodles.

    The strengths of this study are the large popula-tion-based sample size, the consistency of the resultsbetween rural and urban slum areas, and data thatallowed analyses to be controlled for potential con-founding factors. In epidemiologic studies, it is not pos-sible to control for all factors, and unmeasured factorsmay have influenced the relationship between the useof 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 forstunting. These findings are consistent with those ofprevious studies in Uganda [18] and Nepal [19] that

    FIG. 1. Prevalence of stunting in children aged 6 to 59 monthsfrom families in rural areas (black bars) and urban slumareas (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 familieswho 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 < .0001by ANOVA across the four categories for both rural andurban families

    0

    10

    20

    30

    40

    50

    60

    Stunting(%)

    Expenditure category0 1 2 3

    FIG. 2. Prevalence of stunting in children aged 6 to 59 monthsfrom 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 familieswho 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 = .02by ANOVA across the four categories for rural families and

    p= 0.83 for urban families.

    0

    10

    20

    30

    40

    50

    60

    Stunting(%)

    Expenditure category0 1 2 3

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    353Fortified foods and child stunting

    have shown an association between prolonged breast-feeding and stunting. By the age of 6 months, exclusivebreastfeeding is not sufficient to meet the requirementsfor many micronutrients. Complementary foods con-taining vitamin A, iron, zinc, and other micronutrientsare needed in order to meet the needs of growing

    infants. The results of the present study do not apply tochildren under 6 months of age who are breastfeeding.

    Factors that were protective against stunting in thepresent study included vitamin A supplementationwithin the previous 6 months, presence of an improvedlatrine, and use of adequately iodized salt. Poor sanita-tion increases the risk of diarrheal disease and poorgrowth associated with diarrhea. These findings areconsistent with those of a study in Uganda that linkedlack of a latrine in the household with child stunting[20]. Correction of iodine deficiency has been shown

    to improve linear growth [21].Maternal education was strongly associated with

    a reduced risk of stunting, as was previously shownin Indonesia and Bangladesh [22]. Higher maternaleducation is associated with adherence to a greaternumber of activities that promote child health, such as

    complete childhood immunizations, receipt of vitaminA capsules, and use of iodized salt [22].

    The results of the present study suggest that com-pulsory fortification of milk with micronutrients inIndonesia reduces child stunting and that the voluntaryfortification of some noodles has an additional positiveimpact. These findings support initiatives to addressstunting among preschool-aged children through thefortification of commonly eaten foods together withother public health interventions and improved educa-tion for women.

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