![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
|
|
|
|
|
||
3 Pan American Health Organization, Washington, DC 20037; 4 Institute of Science and Technology, Ministry of Public Health of Ecuador, Quito, Ecuador; 5 Faculty of Medicine, Central University of Ecuador, Quito, Ecuador; and 6 Ministry of Health, El Salvador, San Salvador, El Salvador
* To whom correspondence should be addressed. E-mail: lutterch{at}paho.org.
 |
ABSTRACT |
|---|
 TOP ABSTRACT IntroductionMethodsResultsDiscussionLITERATURE CITED |
|---|
|
Introduction |
|---|
|
TOPABSTRACTIntroductionMethodsResultsDiscussionLITERATURE CITED |
|---|
The relative effectiveness of interventions to change behaviors vs. provision of foods to improve young child nutrition is not known. Several studies show the efficacy of providing complementary foods to young children living in poverty on anemia and growth under research conditions (9,10). Others have shown an effect on linear growth of improved feeding behaviors (11,12). Less information is available on the effectiveness of such interventions when administered as individual interventions or together through public health services where delivery is embedded in routine care and compliance is not controlled (13).
The nutritional situation of infants and young children in Ecuador is characterized by linear growth retardation and a high prevalence of anemia consistent with global findings (2). The prevalence of anemia (hemoglobin < 110 g/L) of 72% in children <1 y of age (14) is higher than found in the only nationally representative nutrition survey 11 y earlier (15). A study in the 5 poorest provinces in Ecuador in children aged 12–59 mo showed serum retinol < 0.70 µmol/L (20 µg/dL) in 18% of rural children and 13% of urban children (16).
Ecuador launched its National Food Nutrition Program (PANN 2000)7 in 2000 during an acute economic crisis to prevent malnutrition in young children by improving feeding behaviors and dietary quality. It represents a substantial departure from the previous nutrition program. To reach the poorest children during their most vulnerable period of development, it targeted all children between birth and 24 mo living in conditions of extreme poverty rather than children < 5 y of age with low weight-for-age, many of whom were already likely to be permanently stunted, but with adequate weight-for-height. Rather than providing staple foods to the malnourished child's family, the program sought to improve the quality of the young child's diet by providing a specifically designed fortified complementary food (FCF) beginning at 6 mo. PANN 2000 is a national publicly financed program present throughout the country. Administered by the Ministry of Public Health (MSP), PANN 2000 reached 
125,000 infants and young children at the time of the evaluation in 1607 health centers in the poorest parishes.
The evaluation reported here was conducted in poor periurban and rural communities in Ecuador. The impact of 11 mo of participation in PANN 2000 was evaluated in the catchment populations of 10 participating government health clinics and 6 nearby control clinics. We evaluated both the process of the implementation of PANN 2000 and the impact with respect to maternal knowledge about child nutrition, maternal behavior and feeding practices, dietary intakes, micronutrient status, morbidity, and growth.
|
Methods |
|---|
|
TOPABSTRACTIntroductionMethodsResultsDiscussionLITERATURE CITED |
|---|
3 h by car from the capital of Ecuador in a low-lying malaria-endemic coastal area. Santo Domingo is a rapidly growing area because of its favorable location between the coast and the highlands. It comprises poor urban, periurban, and rural communities known to have a high level of both in- and out-migration and is characterized by low and insecure income, poor housing, and a general lack of 1 or more essential services (piped water, reliable electricity supply, sewage disposal). It has a prevalence of stunting (length-for-age Z-score < –2 SD) of 24.6, similar to the national median (17). The evaluation design took advantage of the planned rolling implementation of PANN 2000. Health centers in communities where the program began served as the program group and health centers in neighboring, apparently similar communities, where the program was to be implemented 1 y later, served as the control group. Design. This evaluation was quasi-experimental with nonrandomly chosen control subjects. Initially, the communities in the lowest (5th) poverty quintile were targeted for PANN 2000 with the incorporation of the 4th quintile at a later date. Thus, a priori the program group was expected to be poorer than the control group. Randomization was not possible as the government was committed to intervene in the poorest communities. No effort was made to affect program implementation so that its effectiveness would be evaluated under actual conditions.
To maximize the potential to measure program impacts, the age criterion for selection was 6–11 mo at baseline. A census was undertaken to identify households with eligible infants in the catchments of all 10 health clinics serving the health district of Los Rosales where PANN 2000 was to be implemented first and in the 6 health clinics in the neighboring health district of La Concordia where PANN 2000 was to be implemented 1 y later. Parents were informed of the evaluation protocol and asked to sign a consent form; there were few refusals. The evaluation was conducted by the research arm of MSP, which functioned autonomously from the PANN 2000 implementing team and was approved by the ethics committee of both MSP and the Pan American Health Organization. All control children were entered into PANN 2000 within 1 mo of the final survey.
The PANN 2000 program. PANN 2000 has 5 major components: 1) information, education, and communication; 2) training of health workers in infant and young child nutrition and counseling skills; 3) community participation; 4) provision of a FCF (Mi Papilla); and 5) monitoring and evaluation. The first component aimed to raise awareness of the importance of good nutrition during early childhood, inform families and communities about PANN 2000, and encourage families with young children to enroll. The training component aimed to provide health workers with information and skills needed to implement the program and to improve their knowledge and communication skills so that mothers were given appropriate age-specific child-feeding messages, including the use of Mi Papilla. The community participation component consisted of forming parent committees to select a distribution point for Mi Papilla and identify children in the targeted age range.
Mi Papilla consists of a daily ration of 65 g dry product that provides 275 kcal/d (1150.6 kJ/d) and has an energy density of 1.2 kcal/g (5.0 kJ/g) when mixed with the appropriate amount of water. It is designed to provide 10 g protein; 6 g lipid; 100% of the daily requirement of iron (as ferrous sulfate), folic acid, and zinc (as zinc sulfate); 60% of the daily requirement of vitamin C, the B vitamins, and magnesium; and 30% of the daily requirement of vitamin A, calcium, and phosphorus (Table 1). Macronutrients are provided by dry skim milk (minimum 15% of energy), sugar (maximum 10% of energy), cereal and legume flours (rice, corn, rye, soy), and vegetable oil (3% of total energy provided by the essential fatty acids linoleic and linolenic acid). The manufacturer can decide the exact proportions of cereal and legume flours, but they must provide the required nutrient profile. Mi Papilla is precooked and requires only a clean source of water for preparation and feeding. It complies with the Codex Alimentarius Standard for Processed Cereal-Based Foods for Infants and Children (Standard 74–1981) (20). Its quality is ensured through microbiological, bromatological, and micronutrient analyses.
|
At baseline, information was collected on family composition, socioeconomic conditions, maternal knowledge of and practices for breast-feeding and complementary feeding, and dietary intake. To assess micronutrient status, 5 mL venous blood was collected using sterile equipment and zinc-free tubes and immediately covered with aluminum foil to avoid contact with air and light. The serum was separated by centrifugation and placed in amber-colored vials. Samples were placed in dry ice, transported to the central laboratory, and stored at –80°C until analyzed. Collection and processing of blood samples were conducted according to the MSP procedures (21). Hemoglobin was measured in situ using 10 µL capillary blood and processed with a hemoglobinometer HemoCue B (HemoCue AN). The accepted variation coefficient was 1.5%. Serum retinol was determined using HPLC (21) and serum zinc was determined by flame atomic absorption spectrometry (22).
Community health workers associated with each health center conducted weekly in-home morbidity surveillance and were trained to recognize cases of diarrhea, cough, and difficulty breathing using standard protocols and to document intake of Mi Papilla the day before the visit (yes or no). Reported illness symptoms during the previous 24 h were used as an estimate of overall population morbidity incidence. At baseline and 13 mo later, children were weighed on a clock balance accurate to 100 g (ITAC) and calibrated weekly and recumbent length was measured using locally made, rigid stadiometers accurate to 0.1 cm. Field workers were trained and standardized using WHO guidelines (23). To estimate dietary intake, a 24-h recall at baseline and at the final survey were administered to the child's mother by trained nutritionists. Household utensils and locally made food models were used to estimate portion sizes and standard tables were used to calculate the weight of the food consumed using ProPAN (Process for the Promotion of Child Feeding) software (24). When a food consumed was not found in the standard tables, it was weighed using a digital balance (Soehnle DC 8115, maximum weight 2 kg, precision 1 g). Z scores were calculated using the new WHO Child Growth Standard (25).
Sample size.
Sample size calculations were based on the hypothesized differences PANN 2000 would make in growth, daily energy intake, serum retinol, and hemoglobin and based on a 2-tailed test, a significance level of 0.05%, and a statistical power of 0.8. The effects of the clusters (the unit of sampling was the health center) and different sizes of the clusters were presumed to be modest and not adjusted for in sample size calculations. Based on published studies, we expected a positive effect on linear growth of 0.65 ± 4.0 cm, energy intake of 195 ± 225 kcal/d (815.9 ± 941.1 kJ/d), hemoglobin of 20 ± 1.4 g/L, and serum retinol of 0.25 ± 0.24 µmol/L (7.3 ± 7.0 µg/dL). Because the necessary sample size depended on the outcome in question, we used a hierarchal nested design. The overall sample was selected to assess effect on growth (calculated at 250 per group), a subsample was selected to assess micronutrient status (calculated at 75 per group), and a subsample of the micronutrient sample was used to assess diet (calculated at 60 per group). To allow for attrition, these samples were increased by 25% and varied by group and subsample as all eligible children in the catchment area were invited to participate. Hemoglobin was assessed in most children in the overall sample as was morbidity.
Data analysis. Data were collected on forms that were previously pilot tested, checked by field supervisors, entered into EPI-Info 6.04, and converted to SPSS 12.0 for analysis. Distributions of all variables were checked for normality and transformed where necessary to achieve a normal distribution; when a normal distribution was not possible, nonparametric statistical tests were applied. Socioeconomic information was analyzed using principal component analysis and 3 clusters of associated variables were identified: housing, possessions, and parental education. Food intake was converted to nutrients using ProPAN, which includes food composition data from Latin American and United States food composition tables (24). We compared outcomes using Student's t test, chi-square, McNemar's test, ANOVA, multiple regression, and logistic regression. Variables controlled in the regression models were selected because of their relationship to child growth and included child age, child age squared, initial value (e.g. baseline weight-for-age Z score or hemoglobin), maternal education, maternal age, housing index, socioeconomic index, morbidity index, employment of household head, child sex, program, and the interaction of program with all other covariates. In the final model, only covariates that were significant at the 0.1 level (0.15 for interactions) were kept. To assess bias that may have resulted from loss to follow-up or loss to measurement, a dummy variable indicating loss-to-follow-up status was regressed on the same covariates in the final models (26). The Generalized least means procedure (SAS 8.02) was used to examine the models for the clustering effect of the health center (the unit of sampling) and adjust them, if necessary.
All analyses were conducted using an intention-to-treat analysis method in which all children in the program group, irrespective of intervention exposure and intake of Mi Papilla, were included in the analysis as the program group. Outcomes reported all pertain to the individual level. Definitions of outcomes were decided a priori: maternal knowledge about child nutrition and feeding, caregiver behavior and feeding practices, dietary intakes of energy, macro-, and micronutrients, and Mi Papilla; hemoglobin, transferring saturation, serum zinc, and serum retinol; final attained length, weight, and associated Z scores; and prevalence of underweight and stunting (<–2 SD) and overweight (>2 SD). For morbidity outcomes, diarrhea was defined as 3 or more liquid or semiliquid stools in 24 h and cough with difficulty breathing was defined as increased respiratory frequency (>40/min in children < 1 y of age and >50/min in older children) and thorax retraction (deepening of the abdomen toward the ribs during inhalation) according to parental reporting.
|
Results |
|---|
|
TOPABSTRACTIntroductionMethodsResultsDiscussionLITERATURE CITED |
|---|
|
10% of children in both groups had C-reactive protein levels > 952 nmol/L (10 mg/dL), indicating current infection. One-quarter of children had serum ferritin values below 12.0 µg/L, indicating deficient iron stores. Slightly >40% of the children had serum zinc < 10.7 µmol/L (65 µg/dL), indicating zinc deficiency.
|
70% of iron and zinc intake (Table 4; Fig. 1). On the day of the 24-h recall, Mi Papilla was consumed by 57.4% of the program children, who consumed a total of 56.6 ± 24.0 g. When all children with dietary recalls were included in the denominator (both those that consumed Mi Papilla and those that did not), consumption was 32.5 ± 33.5 g, or one-half the daily ration. Both total energy intake and energy intake per kilogram body weight were significantly higher in the program group as was the intake of fat. Intakes of iron, zinc, and calcium were also higher in program children. Consumption of Mi Papilla did not replace usual intake but increased net intake of energy and other nutrients; daily energy increased by 240 kcal and iron increased by nearly 9 mg.
|
|
Mothers in the program group were not more likely to report hearing messages or receiving counseling about breast-feeding and/or complementary feeding in health services compared with mothers in the program group (data not shown). In both groups, very few reported hearing messages on the radio or in health services. Breast-feeding and complementary feeding practices, apart from feeding Mi Papilla, did not improve in children in the program group. There were no differences in the proportion of mothers in either group that reported that "breastmilk is the best food for infants < 6 mo," "the ideal consistency of porridge for infants is thick," "the consistency of the main meal given to the infant yesterday was thick," or "breastmilk is the best food for infants < 6 mo" at the final compared with the baseline survey.
Nonadjusted program effects using the intention to treat method were positive and significant for length-for-age (P = 0.027) and weight-for-age (P = 0.021) Z scores and the prevalence of underweight (P = 0.006) (Table 4). The level of significance for the difference in stunting was 0.061, favoring the program group. There were no differences in the likelihood to be wasted or overweight.
Children in the program group had significantly higher hemoglobin values and were significantly less likely to be anemic than were children in the control group (Table 4). There were no between-group differences in levels of transferrin saturation or ferritin. Mean levels of serum zinc and the proportion of children considered zinc deficient did not differ between groups. The prevalence of vitamin A deficiency declined in both groups and no significant differences were found (P = 0.12). As in the baseline survey, no children had serum retinol values < 0.35 µmol/L (10 µg/dL). Mean hemoglobin in program children increased by 13.7 g/L, whereas in control children it only increased by 5.6 g/L (P < 0.0001) (data not shown).
Multiple regression and logistics regression analysis. The effect of PANN 2000 on linear growth was a function of child age when entered into the program. The overall effect was positive (0.37 cm) but not significant (P = 0.137) when we controlled for the covariates child age; child age squared; baseline length; the indices for socioeconomic level, housing, education, and employment of household head; and the interaction term for child age at baseline and program. When stratified by the age groups of 9–11 mo vs. 12–14 mo, a program effect of 0.66 cm was observed (P = 0.08) in the older children (Table 5). The coefficient for younger children was small and positive but not significant. A similar response for weight, significantly favoring only the children who were older at baseline, was also observed (Table 5). However, the interaction term of child age at baseline and program was significant (P = 0.029), indicating that the effect of the program on weight depended on the age of the child when the program began. At the final survey, an 8-kg child who was 12 mo old when the program began was 0.241 kg heavier than a control child of a similar initial weight and age, whereas an 8-kg child who was 13 mo old when the program began was 0.617 kg heavier than a control child of a similar initial weight and age.
|
The odds of being underweight were 75% lower for children in the program when we controlled for the covariates mentioned above (P = 0.007). The odds of being underweight were 7% lower for every year of maternal age and 81% lower for every 1 SD increase in weight-for-age at baseline with other variables being controlled for. The odds of being stunted were not significantly different.
The effect of the program on the risk of being anemic was significant (OR = 0.58; CI = 0.24, 0.75; P = 0.003). Baseline hemoglobin was negatively related to final hemoglobin and also significant (P < 0.002); children with higher baseline hemoglobin experienced less change in hemoglobin than those with lower hemoglobin. There was no interaction between baseline hemoglobin and program. Loss to follow-up does not appear to bias the results (data not shown). Neither program nor control children who were followed had baseline hemoglobin levels or maternal education different from those of children not followed. The effect of sampling at the unit of the health center was marginally significant (P = 0.06); however, the effects on the unstandardized coefficients was small and the final model was not adjusted for health center. When covariates were controlled for, the odds of being anemic were 58% lower for children in the program. Children of mothers with higher education and children with higher baseline hemoglobin scores were less likely to be anemic; the odds of being anemic were 8% lower for every year of maternal education and 34% lower for every 10 g/L additional hemoglobin at baseline when other covariates were controlled for. The results do not appear to be influenced by loss to measurement. There was no effect of health center clustering (P = 0.64).
|
Discussion |
|---|
|
TOPABSTRACTIntroductionMethodsResultsDiscussionLITERATURE CITED |
|---|
|
The significant difference in anemia occurred despite attempts to treat anemic children identified at baseline in both groups with ferrous sulfate. Data were not collected on the compliance; however, at baseline, only 11% of mothers in both groups reported giving an iron supplement in the 2 wk before the interview and we are not aware of any peer-reviewed studies showing that iron supplementation programs for infants and young children, although highly efficacious in clinical trials (30), are effective in a public health setting. The prevalence of anemia at baseline (76%) is higher than that reported in the only nationally representative nutrition survey (15) 11 y earlier, despite programs to improve micronutrient status, and illustrates the challenge of reducing iron deficiency anemia in infants and young children.
Iron status during the first 2 y of life is highly dynamic, which may explain why Mi Papilla did not affect serum ferritin despite having a significant positive effect on hemoglobin and anemia prevalence. In a study of well-nourished infants with a low prevalence of iron deficiency anemia, dietary iron predicted hemoglobin but not serum ferritin values during infancy (31). In this study, there was no correlation between dietary iron and serum ferritin before age 18 mo, a finding consistent with some (32,33) but not all studies (34) of iron metabolism during early childhood.
The fact that increased dietary zinc in program children did not lead to improved zinc status compared with control children suggests that the compound in Mi Papilla, zinc sulfate, was not effective. There are several possible reasons for this finding: it may not be bioavailable in a food matrix, zinc intake from traditional complementary foods provided the physiologic requirement, and/or plasma zinc may be an insensitive biomarker of zinc status. Previous studies showed zinc sulfate to be bioavailable in adults, although absorption was less from porridge than from bread, presumably because of the greater phytate content in porridge (35). Zinc sulfate provided as a supplement to young children is bioavailable and improves serum zinc status and linear growth (36). However, a recent study in Peru shows that zinc sulfate when given with food did not affect zinc plasma concentration in young children (37) and it is possible that high-phytate meals depress zinc absorption in zinc-FCF (38). The physiologic zinc requirement for children ages 1–3 y is 0.74 mg/d and the estimated average requirement is 2.5 mg/d (39). At the final survey, the daily zinc intake from traditional complementary foods, excluding that from Mi Papilla, was 2.9 for program children and 2.6 mg for control children. These intakes exceed the estimated average requirement; therefore, it is possible that physiologic requirements were met and the saturation point for absorption was approached (40).
Serum retinol concentration increased and the prevalence of subclinical vitamin A deficiency decreased in both groups and the program had no apparent effect on vitamin A status. The level of vitamin A is relatively low in Mi Papilla and provides only about one-third of the recommended daily intake. This amount of vitamin may have been dwarfed by high-dose supplements received by about one-half of the children in both groups in the 6 mo before the final survey.
The program had a far greater effect on the weight gain than on linear growth and only in children aged 12–14 mo when they began consuming Mi Papilla. This finding is counterintuitive to the perception that younger children in the most rapid phase of growth are more likely to respond to improved food intake. However, indicators of risk do not necessarily correspond to indicators of benefit (41). The gastric capacity of older children is greater, allowing them to eat more of the FCF with less displacement of usual intake. Also, older children are more likely to be weaned, which increases the proportion of total nutritional requirements provided by food intake. Greater improvements in linear growth may not have been observed because most of the stunting detected at the final survey had already occurred when baseline measures were taken. During the course of the evaluation, the relative increase in stunting in program and control children was only 24 and 38%, respectively. To ensure maximum impact of public health interventions that provide a FCF, greater efforts need to be made to extend the duration of exclusive breast-feeding to prevent growth faltering that occurs during the first 6 mo of life.
There have been few evaluations of the effect on growth of public health programs to improve diet and results are mixed (42). A recent evaluation in Mexico showed that the only subgroup to benefit from a FCF started supplementation before age 6 mo and was in the poorer half of the socioeconomic strata (43). After 2 y of follow-up, these children grew 1.1 cm more than children of the same age and socioeconomic strata who received the FCF for only 1 y. In India, children aged 4–12 mo who were randomly assigned to receive a milk-based cereal and nutrition counseling consumed more energy and gained 250 g more than children who only received counseling (44). Linear growth was not affected. In Peru, children who received a FCF did not improve in linear growth more than a similarly aged control group over 11 mo even in those who were youngest (aged 6–11 mo) at baseline (45).
The strength of our results is that they are from a public health program delivered through routine health services. The data showing improved dietary intake in the program group is congruent with the effects in this group on growth and micronutrient status. However, there were also some weaknesses in the design and implementation. The evaluation was not randomized nor could it be blinded except for the analysis of the blood samples, and the loss to final measurement was large for some evaluation components. Seemingly similar program and control communities were selected, and although the differences found between them were adjusted for in the analysis, this adjustment may have been incomplete. The lack of blinding could have led to bias; however, data collection was standardized, all interviews were structured, and different sets of interviewers collected data on diet and anthropometry. Although it is possible that knowledge of the group influenced data collectors' interpretation of responses or the recording of the dietary recall data, it is difficult to see how anthropometric measures could have been affected. Also, the determinations of serum retinol, iron indicators, and serum zinc were blinded and consistent with the dietary data.
We examined possible bias that may have been introduced by loss to final measurement by asking 2 questions: was the loss to measurement different for program vs. control children, and was the loss to measurement related to any of the variables in the regression model showing a positive effect of the program on weight or length? With respect to weight, both answers were negative. With respect to length, the probability of loss to measurement was associated with age and length at baseline but not program, showing that such loss is unlikely to have biased the results.
Linear growth retardation and anemia are the 2 most prevalent forms of malnutrition in Latin America and other regions of the world, affecting the health and development of millions of children. The FCF of the program described here was highly effective in reducing anemia; the effects on linear growth, while positive, failed to reach significance. Several countries in Latin America have implemented programs that include a FCF and others are contemplating such programs. Our evaluation provides further evidence they can be effective. However, it also points to the challenges and importance of simultaneously improving exclusive breast-feeding and complementary feeding behaviors so that the effect of improved dietary quality on growth can be maximized.
|
ACKNOWLEDGMENTS |
|---|
|
FOOTNOTES |
|---|
2 Author disclosures: C. K. Lutter, A. Rodríguez, G. Fuenmayor, L. Avila, F. Sempertegui, and J. Escobar, no conflicts of interest.
7 Abbreviations used: FCF, fortified complementary food; MSP, Ministry of Public Health; PANN 2000, National Food Nutrition Program of Ecuador.
Manuscript received 6 June 2007. Initial review completed 8 July 2007. Revision accepted 19 November 2007.
|
LITERATURE CITED |
|---|
|
TOPABSTRACTIntroductionMethodsResultsDiscussionLITERATURE CITED |
|---|
1. Shrimpton R, Victora CG, de Onis M, Lima RC, Blossner M, Glugston G. Worldwide timing of growth faltering: implications for nutrition interventions. Pediatr 2001;107:1–7. Available from: http://www.pediatrics.org/cgi/content/full/107/5/e75.
2. Lutter CK, Rivera JA. Nutrition of infants and young children and characteristics of their diets. J Nutr. 2003;133:S2941–9.
3. Martorell R. Results and implications of the INCAP follow-up study. J Nutr. 1995;125:S1127–38.
4. Scrimshaw NS. Community-based longitudinal nutrition and health studies: classical examples from Guatemala, Haiti and Mexico. Boston: International Foundation for Developing Countries; 1995.
5. Pelletier DL, Frongillo EA, Habicht J-P. Epidemiologic evidence for a potentiating effect of malnutrition on child mortality. Am J Public Health. 1993;83:1130–3.
6. Lozoff B, Georgieff MK. Iron deficiency and brain development. Semin Pediatr Neurol. 2006;13:158–65.[Medline]
7. Haas JD, Murdoch S, Rivera J, Martorell R. Early nutrition and later physical work capacity. Nutr Rev. 1996;54:S41–8.[Medline]
8. Bhargava SK, Sachdev HS, Fall CH, Osmond C, Lakshmy R, Barker DJ, Biswas SK, Ramji S, Prabhakaran D, et al. Relation to serial changes in childhood body mass index to impaired glucose tolerance in young adulthood. N Engl J Med. 2004;350:865–75.
9. Walter T, Dallman PR, Pizarro F, Velozo L, Pena G, Bartholmey SJ, Hertramph F, Olivares M, Letelier A, et al. Effectiveness of iron-fortified infant cereal in prevention of iron deficiency anemia. Pediatrics. 1993;91:976–82.
10. Lartey A, Manu A, Brown KH, Peerson JM, Dewey KG. A randomized, community-based trial of the effects of improved, centrally processed complementary foods on growth and micronutrient status of Ghanaian infants from 6 to 12 mo of age. Am J Clin Nutr. 1999;70:391–404.
11. Penny ME, Creed-Kanashiro HM, Robert RC, Narro MR, Caulfield LE, Black RE. Effectiveness of an educational intervention delivered through the health services to improve nutrition in young children: a cluster-randomized controlled trial. Lancet. 2005;365:1863–72.[Medline]
12. Guldan GS, Fan HC, Ma X, Ni ZZ, Xiang X, Tang MZ. Culturally appropriate nutrition education improves infant feeding and growth in rural Sichuan, China. J Nutr. 2000;130:1204–11.
13. Victora CG, Habicht J-P, Bryce J. Evidence-based public health: moving beyond randomized trials. Am J Public Health. 2004;94:400–5.
14. Rodríguez A, Acosta M, López-Jarmillo P, López R. Linea basal de anemias en el Ecuador. Quito (Ecuador): Ministerio de Salud Pública. Programa integrado de Micronutrientes. Sistema de Monitoreo y Evaluación; 1997.
15. Freire W, Dirren H, Mora JO, Arenales P, Granda E, Breih J, Campaña A, Páez R, Darquea L, et al. Diagnostico de la situación alimentaría, nutricional y de salud de la población Ecuatoriana menor de cinco años (DANS). Quito (Ecuador): CONADE, Ministerio de Salud Publica; 1988.
16. Rodríguez A, Guamán G, Nelson DP. Estado nutricional de los niños de cinco provincias del Ecuador con respecto a la vitamina A. Bol Oficina Sanit Panam. 1996;120:117–23.
17. Larrea C, Freire WB, Lutter C. Equidad desde el principio: situación nutricional de los niños ecuatorianos. Washington, DC: Pan American Health Organization; 2001.
18. WHO/UNICEF/Orstrom/University of California at Davis. Complementary feeding of young children in developing countries. WHO/NUT/98.1 WHO: Geneva; 1998.
19. Institute of Medicine. Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein, and amino acids. Washington, DC: National Academy Press; 2002.
20. WHO/FAO Codex alimentarius standard for processed cereal-based foods for infants and children (standard 74–1981) [cited 2006 Sept 28]. Available from: www.codexalimentarius.net/download/standards/290/CXS_074e.pdf.
21. Instituto de Ciencia y Tecnología. La Deficiencia de Vitamina A en los Niños Ecuatorianos, Bulletin No. 2. Quito (Ecuador): Ministerio de Salud Pública; 1999.
22. Iyengar GV. Reevaluation of the trace element content in reference man. Radiat Phys Chem. 1998;51:545–60.
23. WHO. Measuring change in nutritional status. Geneva: WHO; 1983.
24. Pan American Health Organization, Emory University, National Institute of Public Health of Mexico, Institute of Investigation in Nutrition (Peru). ProPAN process for the promotion of Chile feeding. Washington, DC: Pan American Health Organization; 2004. Available from: www.paho.org/English/AD/FCH/NU/ProPAN-index.htm
25. WHO. WHO child growth standards: methods and development. Geneva: WHO; 2006.
26. Hsiao C. Analysis of panel data. Cambridge: Cambridge University Press; 1986.
27. Lozoff B, De Andraca I, Castillo M, Smith JB, Walter T, Pino P. Behavioral and developmental effects of preventing iron deficiency anemia in healthy full-term infants. Pediatrics. 2003;112:846–54.
28. Lozoff B, Jimenez E, Smith JB. Double burden of iron deficiency in infancy and low socioeconomic status: a longitudinal analysis of cognitive test scores to age 19 years. Arch Pediatr Adolesc Med. 2006;160:1108–13.
29. Walter T. Impact of iron deficiency on cognition in infancy and childhood. Eur J Clin Nutr. 1993;47:307–16.[Medline]
30. Beaton GH, McCabe GP. Efficacy of intermittent iron supplementation in the control of iron deficiency anaemia in developing countries. An analysis of experience: final report to the Micronutrient Initiative. Ottawa: Micronutrient Initiative; 1999.
31. Lind T, Hernell O, Lonnerdal B, Stenlund H, Domellof M, Persson LA. Dietary iron intake is positively associated with hemoglobin concentration during infancy but not during the second year of life. J Nutr. 2004;134:1064–70.
32. Domellof M, Cohen RJ, Dewey KG, Hernell O, Rivera LL, Lonnerdal B. Iron supplementation of breastfed Honduran and Swedish infants from 4 to 9 months of age. J Pediatr. 2001;138:679–87.[Medline]
33. Fuchs GJ, Farris RP, DeWier M, Hutchinson SW, Warrier R, Doucet H, Suskind RM. Iron status and intake of older infants fed formula vs cow milk with cereal. Am J Clin Nutr. 1993;58:343–8.
34. Walter T, Pino P, Pizarro F, Lozoff B. Prevention of iron-deficiency anemia: comparison of high- and low-iron formulas in term healthy infants after six months of life. J Pediatr. 1998;132:635–40.[Medline]
35. Lopez de Romaña D, Lonnerdal B, Brown KH. Absorption of zinc from wheat products fortified with iron and either zinc sulfate or zinc oxide. Am J Clin Nutr. 2003;78:279–83.
36. Brown KH, Peerson JM, Allen LH, Rivera J. Effect of supplemental zinc on the growth and serum zinc concentrations of pre-pubertal children: a meta-analysis of randomized, controlled trials. Am J Clin Nutr. 2002;75:1062–71.
37. Brown KH, López de Romaña D, Arsenault JE, Peerson JM, Penny ME. Comparison of the effects of zinc delivered in a fortified food or a liquid supplement on the growth, morbidity, and plasma zinc concentrations of young Peruvian children. Am J Clin Nutr. 2007;85:538–47.
38. Brown KH, Wessells KR, Hess SY. Zinc bioavailability from zinc-fortified foods. Int J Vit Min Res. 2007;77:174–181.
39. Institute of Medicine. Reference intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. Washington, DC: National Academy Press; 2001.
40. Hambidge KM, Miller LV, Tran CD, Krebs NF. Measurements of zinc absorption: application and interpretation in studies designed to improve human zinc nutriture. Int J Vitam Nutr Res. 2005;75:385–93.[Medline]
41. Ruel MT, Habicht J-P, Rasmussen KM, Martorell R. Screening for nutrition interventions: the risk or the differential-benefit approach? Am J Clin Nutr. 1996;63:671–7.
42. Dewey KG. Success of intervention programs to promote complementary feeding. In: Black R, Michaelsen K, eds. Public health issues in infant and child nutrition. Nestlé Nutrition Series, Pediatric Program. 48th vol. Nestlé LTX. Philadelphia: Vevey/Lippincott Williams and Wilkins; 2002. p. 199–212.
43. Rivera JA, Sotres-Alvarez D, Habicht JP, Shamah T, Villalpando S. Impact of the Mexican program for education, health, and nutrition (Progresa) on rates of growth and anemia in infants and young children: a randomized effectiveness study. JAMA. 2004;291:2563–70.
44. Bhandari N, Bahl R, Nayyar B, Khokhar P, Rohde JE, Bhan MK. Food supplementation with encouragement to feet it to infants from 4 to 12 months of age has a small impact on weight gain. J Nutr. 2001;131:1946–51.
45. Lopez de Romaña G. Experiences with complementary feeding in the FONCODES Project. Food Nutr Bull. 2000;21:43–8.
This article has been cited by other articles:
|
|
 |
|
  C. K. Lutter Iron Deficiency in Young Children in Low-Income Countries and New Approaches for Its Prevention J. Nutr., December 1, 2008; 138(12): 2523 - 2528. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
