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* Center for Epidemiology and Biostatistics and Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio; and Departamento de Infectologia, Instituto Nacional de Ciencias Medicas y Nutricion, Mexico, DF
3 To whom correspondence should be addressed. E-mail: Ardythe.Morrow{at}cchmc.org.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2.2 kg. All mothers received home-based peer counseling to promote EBF. Infant feeding data were collected weekly. Nurses measured hemoglobin (Hb) values every 3 mo. Hb was measured in 183 infants at 9 mo of age. Anemia at 9 mo was defined as a Hb value <100 g/L. EBF was defined by WHO criteria and ranged in duration from 0 to 31 wk. At 9 mo, Hb (mean ± SEM) was 114 ± 0.9 g/L; 23 children (12.5%) had Hb levels <100 g/L. EBF >6 mo, but not EBF 4–6 mo, was associated with increased risk of infant anemia compared with EBF <4 mo (odds ratio = 18.4, 95% CI = 1.9, 174.0). Maternal anemia was independently (P = 0.03) associated with a 3-fold increased risk of infant anemia. These associations were not explained by confounding with other maternal or infant factors. By linear regression, a lower infant Hb at 9 mo was associated with increased EBF duration among mothers who had a history of anemia (ß = –0.07, P = 0.003), but not among mothers with no history of anemia. Infants who are exclusively breast-fed for >6 mo in developing countries may be at increased risk of anemia, especially among mothers with a poor iron status; greater attention to this issue is warranted.
KEY WORDS: • infant anemia • maternal anemia • exclusive breast-feeding
Iron deficiency is the most common nutrient deficiency and cause of anemia in childhood (1). Although prevalence rates of anemia among healthy term infants 6–18 mo of age are reported to be as low as 2–6% in Western Europe and the United States (2–4), iron deficiency anemia was shown to affect more than half of the children in some developing countries (5). In Mexico, 27% of children <5 y old are anemic (6,7). A national probabilistic survey of Mexican children reported the prevalence of anemia to be 13% at 6–11 mo of age, but as high as 49% among children 12–24 mo old (8). Varying degrees of anemia in young children are associated with poor cognitive outcomes (9–13). Anemia diagnosed at 8 or 9 mo of age has been associated with significantly lower achievement scores in 2nd grade children (14) and impaired motor development at 18 mo (15). Iron deficiency anemia was also shown to be significantly associated with mental retardation (16), decreased activity, increased wariness or hesitance, and remaining in close proximity with caregivers (17).
Although the iron in human milk is highly bioavailable (
50% absorption) (18–21), the iron content is at its highest in early transitional milk and decreases steadily over the course of lactation (22). In general, infants born at term and with an adequate birth weight have sufficient iron stores for the first 4–6 mo of life. However, evidence suggests that infants with adequate birth weight born to anemic mothers have low iron stores and are more likely to develop anemia (23–26). By 6 mo, complementary foods are required to provide the iron and other nutrients necessary for infant development (27,28). A randomized trial conducted in Honduras concluded that at 6 mo, the risk of iron deficiency is low among exclusively breast-fed (EBF)4 infants with birth weights >3000 g (29), although infants who were exclusively breast-fed to 6 mo had significantly lower hemoglobin (Hb) levels (104 g/L) than infants who had received iron-fortified complementary foods (109 g/L). Simple iron-fortified complementary feedings before age 6 mo, however, were not sufficient to prevent anemia among the study infants. A second trial, conducted on micronutrient deficiencies during the period of EBF among term, low-birth-weight infants (1500–2500 g) in Honduras, found that infants who received iron supplements did not benefit from complementary foods at 4–6 mo. Dewey et al. (30) thus recommended that term, low-birth-weight infants be exclusively breast-fed for 6 mo with iron supplementation.
In 2001, the WHO issued the recommendation for EBF for the 1st 6 mo of life (31). EBF reduces infant mortality due to common childhood illnesses such as diarrhea or pneumonia, and is associated with shorter recovery time during illness (32). There is some concern, however, about the potential for increased risk of anemia associated with longer duration of EBF in populations with a high prevalence of maternal and infant anemia. Between 1998 and 2003, we conducted a cohort study of breast-feeding mother-infant pairs in Mexico City. Following the protocol of our previous community-based efficacy trial of breast-feeding support (33), we provided peer breast-feeding counseling to all study mothers in this cohort with the goal of achieving the WHO recommendations for EBF for 6 mo. This counseling was associated with a median duration of 3–4 mo exclusive breast-feeding, much longer than previously seen in this population. To determine the effect of this new pattern, we examined the association between EBF, maternal anemia, and other factors in relation to the prevalence of anemia among infants in our cohort.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Blood sampling. Nurses collected a venous blood sample from study infants every 3 mo, and Hb values were determined at each occasion. Capillary blood, collected by heel or finger stick, was used when venous blood was unattainable. Hb concentration was measured using the HemoCue® hemoglobin photometer. All infants and mothers identified with low Hb concentrations (<100 g/L for infants and <125 g/L for mothers) were referred for treatment at the San Pedro Martir community health center. Treatment of study mothers and children with iron was not part of the study protocol per se and was at the discretion of an individual physician. Serum transferrin receptor (TfR) concentration was determined from the blood samples of the infants diagnosed with anemia to verify that the observed anemia was caused by iron deficiency (36,37). Serum TfR concentrations are increased in iron deficiency anemia and can help to differentiate this disorder from other causes of anemia, such as anemia associated with chronic infection or inflammation (38,39). The Ramco TfR test kit and enzyme immunoassay were used for the quantitative determination of TfR concentration in our serum samples.
Definitions.
Anemia was defined as a Hb concentration <100 g/L at 9 mo (40). The duration of EBF was defined as the number of days an infant was exclusively breast-fed, i.e., received only human milk without ever receiving any other fluid or food. EBF was categorized as 0–3.9 mo (
122 d), 4–6 mo (123–182 d), and >6 mo (183 d). The percentage of human milk, solid foods, liquids (water, juice, tea), and cow's milk feedings was calculated as the number of these feedings divided by the total number of feedings. Predominant breast-feeding was defined as receiving human milk but also receiving water, water-based drinks (sweetened or flavored water, teas), fruit or vegetable juice, or oral rehydration salts solution; no other liquids or solids were included.
Statistical analysis.
All statistical analyses were carried out using SAS® for Windows (version 8.2). Means ± SEM and medians with ranges were reported for continuous variables (i.e., Hb levels and duration of EBF). Crude associations between anemia status, EBF and confounding variables were tested using the two-sample t test, Wilcoxon sum-rank test, and the Pearson's 
2 test. The primary analysis investigated the relation between infant anemia at 9 mo and EBF history, accounting for the effects of maternal anemia and other maternal and infant factors; logistic regression was used to model this relation. A secondary analysis was conducted using linear regression to determine the relation between infant hemoglobin concentration at 9 mo (a continuous variable) and EBF history in days accounting for maternal anemia and other factors. Maternal anemia was investigated as a potential independent risk factor, confounder, and/or effect modifier in relation to EBF duration and infant anemia at 9 mo. Confounding and effect modification of the relation between EBF duration and risk of infant anemia was investigated for all variables that were statistically significant in the regression models. Statistical significance was considered at the 
= 0.05 level. The potential effects of outliers were evaluated in all analyses. The logistic regression model was tested for goodness of fit using the Hosmer and Lemeshow test.
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2.2 kg at birth (median birth weight 3.12 kg; only 5 infants weighed 2.2–2.5 kg at birth); the median weight at 9 mo of age was 8.15 kg (6.0–10.4 kg). Among the 183 study infants at 9 mo, the Hb was 114 g/L; 23 (12.5%) infants were defined as anemic (Hb concentration <100 g/L). Anemic and nonanemic infants did not differ with respect to median birth weight, maternal age, or maternal education (Table 1). There was a marginally significant difference with respect to infant gender and anemia; 65% of children who were anemic were boys compared with 45% of the nonanemic group (P = 0.07). Infants who were anemic had a significantly (P = 0.04) longer median duration of EBF (18 wk for anemic infants conmpared with 11 wk for nonanemic infants), although the median duration of any breast-feeding did not differ between anemic and nonanemic infants. Infants who were anemic also had a significantly (P = 0.02) larger weight gain between birth and 9 mo (5.32 kg for anemic infants compared with 4.88 kg for nonanemic infants). Hb data for 3 and/or 6 mo were available for 168 (92%) of the 183 infants. The rate of anemia at 9 mo was higher among infants who were previously anemic at 3 and/or 6 mo of age (37%) compared with those who were never previously anemic (9%; P = 0.003).
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EBF duration. The duration of EBF in the 183 study children ranged from 0 to 31 wk (218 d) with a median of 12 wk. EBF was not initiated by 19 mother-infant pairs, but all 19 of these mothers reported predominant breast-feeding for a brief time (range 8–16 d). The duration of any breast-feeding in the 183 study children ranged from 19–732 d; 119 (65%) infants were exclusively breast-fed for <4 mo, 59 (32%) for 4–6 mo, and 5 (3%) for >6 mo. Of the 5 infants who were exclusively breast-fed for >6 mo, 2 were exclusively breast-fed for 185 d, and the remaining three were exclusively breast-fed for 194, 197, and 218 d. These EBF duration groups did not differ with respect to maternal age, infant sex, previous anemic status of infant, maternal anemia, or median birth-to-9-mo weight gain. The median birth weight differed significantly among EBF groups but the differences do not appear meaningful (Table 1).
There was a significant (P = 0.001, Cochrane-Armitage test for trend) trend toward increasing proportion of infants with anemia at 9 mo in relation to duration of EBF: of the 119 infants who were exclusively breast-fed for <4 mo, 11 (9%) were anemic; of 59 infants exclusively breast-fed for 4–6 mo (123–182 d), 9 (15%) were anemic; and of 5 infants who were exclusively breast-fed for >6 mo (183–218 d), 3 (60%) were anemic.
We also evaluated the duration of predominant breast-feeding in relation to risk of anemia. The trend of increasing likelihood of anemia at 9 mo with increasing duration of predominant breast-feeding was significant (P = 0.005), similar to the trend with duration of EBF. Of the 100 infants predominantly breast-fed < 4 mo, 7 (7%) were anemic at 9 mo of age; of the 74 infants predominantly breast-fed 4–6 mo, 13 (18%) were anemic, and of the 9 infants who were predominantly breast-fed for >6 mo, 3 (33%) were anemic at 9 mo of age. Figure 2 shows the prevalence of anemia at 9 mo by both duration of EBF and predominant breast-feeding.
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Maternal iron status. The relation between maternal iron status in the first 6 mo postpartum and infant iron status at 9 mo of age was evaluated. Maternal Hb data are available at 0, 3 and/or 6 mo for 171 (93%) of the 183 mother-infant pairs (Table 1). Anemia at 0, 3, and/or 6 mo postpartum occurred in 71% of mothers whose infants were anemic at 9 mo of age compared with 45% of the mothers whose infants were not anemic at 9 mo (P = 0.025). Maternal Hb level at the first Hb measurement was positively, but modestly correlated with infant Hb at 9 mo of age (Pearson's correlation r = 0.18; P = 0.02). However, maternal Hb was not significantly correlated with the duration of EBF (r = 0.09; P = 0.26).
Other feeding practices. During the first 6 mo of life, the percentage of total feedings that were human milk was high in both the anemic (98%) and nonanemic groups (91%; P < 0.0001). Between 6 and 9 mo of age, anemic infants had a significantly higher percentage of human milk feedings (69%) than nonanemic infants (58%; P = 0.03). There was no significant association with the percentage of solid feedings and anemia between 0 and 6 mo of age or 0 and 9 mo of age. The percentage of cow's milk feedings between 0 and 6 mo was very low, but was unexpectedly lower (0.07%) among infants with anemia compared with infants without anemia (0.4%) at 9 mo of age (P = 0.014). There was no association with the age of introduction of solid foods, juice, tea, or cow's milk and risk of anemia. There also was no association between types of complementary solid foods introduced and risk of anemia. The percentage of total feedings that were formula between birth and 9 mo of age was lower among infants with anemia (0.2%) compared with infants without anemia (5%) at 9 mo of age (P < 0.0001).
Twenty (11%) of the 183 study infants received supplemental iron before 9 mo of age. There was no association between previous iron supplementation and anemia at 9 mo (P = 0.23).
Multivariable regression analysis of infant anemia. The objective of the primary analysis was to investigate the association between infant anemia at 9 mo (as a dichotomous variable) and EBF status (as a categorical variable) accounting for maternal anemia and other risk factors through logistic regression analyses (Table 2). Infants who were exclusively breast-fed for >6 mo (183–218 d) were more likely to be anemic than infants who were exclusively breast-fed for <4 mo [odds ratio (OR) = 18.4, 95% CI = 1.9, 174; P = 0.011], but not infants who were exclusively breast-fed 4–6 mo (123–182 d; OR = 2.0, 95% CI = 0.71, 5.6; P = 0.19). Other risk factors associated with anemia were whether the infant was previously anemic at either 3 or 6 mo of age (OR = 3.9, 95% CI = 1.2, 13.0; P = 0.03) and maternal anemia at 0, 3, and/or 6 mo (OR = 3.3, 95% CI = 1.1, 9.9; P = 0.03). Birth weight, infant gender, maternal education, and weight gain since birth were not significant in the model. Potential effect modification by maternal anemia on the relation between EBF duration and infant anemia at 9 mo was tested in the logistic regression model but was not significant (P = 0.84). When we excluded the 5 infants whose birth weight was <2.5 kg, our results remained consistent.
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Multivariable regression analysis of infant hemoglobin.
The objective of the secondary analysis was to understand infant Hb at 9 mo of age (as a continuous variable) in relation to duration of EBF (as a continuous variable), accounting for maternal anemia and other factors. In a linear regression analysis, Hb values at 9 mo of age had a modest inverse relation with the duration of EBF (Fig. 3). Duration of EBF remained significant after controlling for gender, maternal anemia, and whether the infant was previously anemic at either 3 or 6 mo (ß = –0.05; P = 0.002, Table 3). After excluding the 5 infants who were exclusively breast-fed for 183 d, the effect remained significant (ß = –0.04; P = 0.02), even after accounting for maternal education, infant birth weight, and infant weight gain, which were not significant in the multivariate regression model. There was no interaction or effect modification for the relation between EBF duration and gender. Effect modification by maternal anemia on the relation between EBF duration and infant anemia was tested in a linear regression model, which indicated a marginally significant interaction (P = 0.08). After stratifying the linear regression on the basis of the maternal anemia status, the relation between duration of EBF and infant Hb values at 9 mo of age continued to have a significant inverse relation among mothers with a history of anemia (Table 3). Although the trend toward an association between EBF duration and infant anemia persisted among mothers who were not previously anemic, it was not as strong and was no longer significant.
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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183 d). EBF beyond 6 mo was significantly associated with an increased risk of infant anemia at 9 mo. Although a history of maternal anemia was independently associated as a risk factor for infant anemia at 9 mo, maternal anemia did not appear to confound or modify the effect of the duration of EBF on the risk of infant anemia. Consistent with the increased risk of anemia, lower infant Hb at 9 mo of age was associated with a history of maternal anemia and with increased duration of EBF, although the effect was modest when EBF did not exceed 6 mo. Our data further suggested that maternal anemia may modify the effect of the duration of EBF on infant Hb status at 9 mo. Calculations based on our linear regression suggested that EBF for 185 d was associated with an infant Hb at 9 mo of 109 g/L if the mother was anemic or an Hb of 118 g/L if the mother was not anemic. Thus, our data suggest the possibility that maternal anemia may not only be an independent risk factor for infant anemia but may also modify the effect of EBF duration beyond 6 mo such that the effects of prolonged EBF may be most problematic in anemic mothers.
The risk of anemia (Hb <100 g/L) at 9 mo of age was low (12%) in this population of full-term breast-fed infants, including those who were exclusively breast-fed for longer durations. This prevalence is similar to that previously reported from a national probability survey of Mexican children 6–11 mo old (8). EBF within the recommended duration (up to 6 mo) was not associated with increased risk of infant anemia in our study population, although increasing duration of EBF was modestly associated with decreasing Hb concentrations at 9 mo of age. The relation between EBF duration and decreasing hemoglobin levels remained significant after removing the data from the 5 infants with the longest (183 d) EBF duration. Thus, it is not likely that the modest association observed can be explained by a few influential data points or prolonged EBF only. In our study cohort, there was a small subset of infants (3%) who were exclusively breast-fed beyond 6 mo (183–219 d); there was a sharp increase in anemia in these infants. This small high-risk subgroup defined by EBF >6 mo may also have had social and biological differences that we were unable to control; these differences may have predisposed the infants to become anemic.
Our data on maternal nutritional status were limited to Hb concentrations measured when requested by the mothers. Hb values for the first 6 mo postpartum were not available for 12 (7%) of the mothers nor were we able to collect information on maternal iron supplementation. Although some studies reported no correlation with maternal iron stores and iron concentration in human milk (42–44), a recent study reported an association between the occurrences of maternal and infant iron deficiency anemia (45).
We chose Hb <100 g/L to classify infants as anemic because it is the standard medical practice in Mexico. This cut-off value is consistent with findings reported by Domellöf et al. (40), who defined anemia as a Hb of <100 g/L, which is 2 SD below the cut-off values of iron-replete infants in a population of healthy breast-fed Honduran infants. Our methods of anemia detection were consistent with other studies on anemia and screening situations (15,46). The HemoCue was shown to have excellent precision and validity (47–49). It has a higher sensitivity and specificity than cyanmethemoglobin measurements when venous blood is used (26,50), as was the case in our study. Hb is sensitive to anemia; however, it is not sensitive to mild iron deficiency that may not affect Hb concentrations (51). We verified that the anemia in our population was truly iron deficiency anemia using measurements of serum TfR levels in the blood samples of children who were anemic at 9 mo of age.
Findings in other studies on the duration of EBF and the risk of anemia or iron deficiency are inconsistent. Some studies suggested that most EBF infants are able to maintain adequate iron stores for y 1 of life (52–54). Siimes et al. (42) followed a cohort of Finnish mothers who practiced EBF for varying durations, and compared iron status in 36 infants with 9 mo of EBF to 32 infants who were completely weaned before 3.5 mo. Results of this study showed a sharp decline in infant Hb after 6 mo of age with prolonged EBF, although none of the exclusively breast-fed infants in their study developed anemia at 9 mo. The concentration of Hb remained higher among the breast-fed infants compared with the controls in this study at 4 and 6 mo.
Corn and beans are important staple foods in Mexico; they contain high quantities of phytic acid and other inhibitors of iron absorption. In our study, information on food intake was based on the number of feedings in the past 24 h. Because this does not quantify nutritional intake, we could not determine whether infants were receiving the physiologic requirement of bioavailable iron. However, in our population, infants who were anemic had a smaller proportion of feeds that were cow's milk (0.07%) compared with infants who were not anemic (0.4%). According to the Mexican National Nutrition Survey 1999, the dietary intake of iron among Mexican children <5 y old was relatively high, but due to the small amount of heme iron and the high intake of phytic acid, the resulting bioavailable iron did not satisfy the mean physiologic requirement for this age group (6).
Breast-feeding is the ideal feeding practice for many well-documented reasons. When EBF is continued beyond 6 mo, however, even when the duration of EBF exceeds recommendations only slightly, the bioavailability of iron in human milk may not be sufficient to maintain optimal infant iron status. Previous studies demonstrated that term normal-birth-weight infants who are exclusively breast-fed beyond 6 mo of age have a higher rate of iron deficiency anemia than infants fed iron-fortified formula or iron-fortified complementary foods (55–57).
The findings of this study are consistent with current global breast-feeding recommendations that encourage EBF for 6 mo. Because EBF of infants is continuing for longer durations, the burden of infectious disease morbidity and mortality is significantly decreased (32,58,59). However, this report should serve as an alert. Our data are not definitive but suggest the possibility that the promotion of EBF to 6 mo may modestly increase the number of infants exclusively breast-fed past 6 mo and that these infants may be at increased risk for anemia later in infancy, particularly if their mothers are anemic. As we continue to encourage EBF, we should also be vigilant regarding maternal and infant anemia and the timely introduction of appropriate complementary foods to infants by 6 mo. Potential additional intervention strategies include improved maternal diet, maternal supplementation, provision of low doses of iron to all infants in developing countries regardless of breast-feeding status, and/or targeted screening and treatment of infants exclusively breast-fed for 6 mo as a group that may be at especially high risk for anemia. In areas in which progress has been made in promoting EBF, we encourage follow-up studies to determine the proportion of infants who are exclusively breast-fed beyond 6 mo, and further investigate the occurrence of iron deficiency anemia in this important group.
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FOOTNOTES |
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2 Supported by The National Institute of Child Health and Human Development HD13021.
4 Abbreviations used: EBF, exclusive breast-feeding; Hb, hemoglobin; OR, odds ratio; TfR, transferrin receptor.
Manuscript received 1 July 2005. Initial review completed 6 September 2005. Revision accepted 1 December 2005.
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LITERATURE CITED |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1. Centers for Disease Control and Prevention. Recommendations to prevent and control iron deficiency in the United States. MMWR Recomm Rep. 1998;47:1–29.[Medline]
2. Lind T, Hernell O, Lönnerdal 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.
3. Thorsdottir I, Gunnarsson BS, Atladottir H, Michaelsen KF, Palsson G. Iron status at 12 months of age—effects of body size, growth and diet in a population with high birth weight. Eur J Clin Nutr. 2003;57:505–13.[Medline]
4. Soh P, Ferguson EL, McKenzie JE, Homs MY, Gibson RS. Iron deficiency and risk factors for lower iron stores in 6-24-month-old New Zealanders. Eur J Clin Nutr. 2004;58:71–9.[Medline]
5. Food and Agriculture Organization/World Health Organization. International Conference on Nutrition: World Declaration and Plan of Action. FAO of the United Nations, Rome, Italy. WHO, Geneva, Switzerland; 1992.
6. Rivera JA, Monterrubio EA, Gonzalez-Cossio T, Garcia-Feregrino R, Garcia-Guerra A, Sepulveda-Amor J. Nutritional status of indigenous children younger than five years of age in Mexico: results of a national probabilistic survey. Salud Publica Mex. 2003;45 Suppl 4:S466–76.[Medline]
7. Rivera JA, Sepulveda Amor J. Conclusions from the Mexican National Nutrition Survey 1999: translating results into nutrition policy. Salud Publica Mex. 2003;45 Suppl 4:S565–75.[Medline]
8. Villalpando S, Shamah-Levy T, Ramirez-Silva CI, Mejia-Rodriguez F, Rivera JA. Prevalence of anemia in children 1 to 12 years of age. Results from a nationwide probabilistic survey in Mexico. Salud Publica Mex. 2003;45 Suppl 4:S490–8.[Medline]
9. Lozoff B, Jimenez E, Wolf AW. Long-term developmental outcome of infants with iron deficiency. N Engl J Med. 1991;325:687–94.[Abstract]
10. Lozoff B, Wolf AW, Jimenez E. Iron-deficiency anemia and infant development: effects of extended oral iron therapy. J Pediatr. 1996;129:382–9.[Medline]
11. Walter T. Infancy: mental and motor development. Am J Clin Nutr. 1989;50:655–61.
12. Walter T, De Andraca I, Chadud P, Perales CG. Iron deficiency anemia: adverse effects on infant psychomotor development. Pediatrics. 1989;84:7–17.
13. de Andraca I, Castillo M, Walter T. Psychomotor development and behavior in iron-deficient anemic infants. Nutr Rev. 1997;55:125–32.[Medline]
14. Palti H, Meijer A, Adler B. Learning achievement and behavior at school of anemic and non-anemic infants. Early Hum Dev. 1985;10:217–23.[Medline]
15. Sherriff A, Emond A, Bell JC, Golding J. Should infants be screened for anaemia? A prospective study investigating the relation between haemoglobin at 8, 12, and 18 months and development at 18 months. Arch Dis Child. 2001;84:480–5.
16. Hurtado EK, Claussen AH, Scott KG. Early childhood anemia and mild or moderate mental retardation. Am J Clin Nutr. 1999;69:115–9.
17. Lozoff B, Klein NK, Nelson EC, McClish DK, Manuel M, Chacon ME. Behavior of infants with iron-deficiency anemia. Child Dev. 1998;69:24–36.[Medline]
18. Dallman PR. Nutritional anemia of infancy: iron, folic acid, and vitamin B12. In: Tsang RC, Nichols BL, editors. Nutrition during infancy. Philadelphia, PA: Henley and Belfus; 1988. p. 216–35.
19. Oski FA. Iron deficiency in infancy and childhood. N Engl J Med. 1993;329:190–3.
20. Saarinen UM, Siimes MA, Dallman PR. Iron absorption in infants: high bioavailability of breast milk iron as indicated by the extrinsic tag method of iron absorption and by the concentration of serum ferritin. J Pediatr. 1977;91:36–9.[Medline]
21. Krebs NF. Bioavailability of dietary supplements and impact of physiologic state: infants, children and adolescents. J Nutr. 2001;131:1351S–4.
22. Siimes MA, Vuori E, Kuitunen P. Breast milk iron—a declining concentration during the course of lactation. Acta Paediatr Scand. 1979;68:29–31.[Medline]
23. Colomer J, Colomer C, Gutierrez D, Jubert A, Nolasco A, Donat J, Fernandez-Delgado R, Donat F, Alvarez-Dardet C. Anaemia during pregnancy as a risk factor for infant iron deficiency: report from the Valencia Infant Anaemia Cohort (VIAC) study. Paediatr Perinat Epidemiol. 1990;4:196–204.[Medline]
24. Kilbride J, Baker TG, Parapia LA, Khoury SA, Shuqaidef SW, Jerwood D. Anaemia during pregnancy as a risk factor for iron-deficiency anaemia in infancy: a case-control study in Jordan. Int J Epidemiol. 1999;28:461–8.
25. Morton RE, Nysenbaum A, Price K. Iron status in the first year of life. J Pediatr Gastroenterol Nutr. 1988;7:707–12.[Medline]
26. De Pee S, Bloem MW, Sari M, Kiess L, Yip R, Kosen S. The high prevalence of low hemoglobin concentration among Indonesian infants aged 3–5 months is related to maternal anemia. J Nutr. 2002;132:2215–21.
27. Picciano MF. Nutrient composition of human milk. Pediatr Clin North Am. 2001;48:53–67.[Medline]
28. Dewey KG. Nutrition, growth, and complementary feeding of the breastfed infant. Pediatr Clin North Am. 2001;48:87–104.[Medline]
29. Dewey KG, Cohen RJ, Rivera LL, Brown KH. Effects of age of introduction of complementary foods on iron status of breast-fed infants in Honduras. Am J Clin Nutr. 1998;67:878–84.[Abstract]
30. Dewey KG, Cohen RJ, Brown KH. Exclusive breast-feeding for 6 months, with iron supplementation, maintains adequate micronutrient status among term, low-birthweight, breast-fed infants in Honduras. J Nutr. 2004;134:1091–8.
31. World Health Organization. Global strategy for infant and young child feeding: the optimal duration of exclusive breastfeeding. 2001; Geneva, Switzerland.
32. Kramer MS, Chalmers B, Hodnett ED, Sevkovskaya Z, Dzikovich I, Shapiro S, Collet JP, Vanilovich I, Mezen I, et al. Promotion of Breastfeeding Intervention Trial (PROBIT): a randomized trial in the Republic of Belarus. JAMA. 2001;285:413–20.
33. Morrow AL, Guerrero ML, Shults J, Calva JJ, Lutter C, Bravo J, Ruiz-Palacios G, Morrow RC, Butterfoss FD. Efficacy of home-based peer counselling to promote exclusive breastfeeding: a randomised controlled trial. Lancet. 1999;353:1226–31.[Medline]
34. Velazquez FR, Matson DO, Calva JJ, Guerrero L, Morrow AL, Carter-Campbell S, Glass RI, Estes MK, Pickering LK, Ruiz-Palacios GM. Rotavirus infections in infants as protection against subsequent infections. N Engl J Med. 1996;335:1022–8.
35. Guerrero ML, Morrow RC, Calva JJ, Ortega-Gallegos H, Weller SC, Ruiz-Palacios GM, Morrow AL. Rapid ethnographic assessment of breastfeeding practices in periurban Mexico City. Bull World Health Organ. 1999;77:323–30.[Medline]
36. Akesson A, Bjellerup P, Berglund M, Bremme K, Vahter M. Serum transferrin receptor: a specific marker of iron deficiency in pregnancy. Am J Clin Nutr. 1998;68:1241–6.[Abstract]
37. Akesson A, Bjellerup P, Vahter M. Evaluation of kits for measurement of the soluble transferrin receptor. Scand J Clin Lab Invest. 1999;59:77–81.[Medline]
38. Ferguson BJ, Skikne BS, Simpson KM, Baynes RD, Cook JD. Serum transferrin receptor distinguishes the anemia of chronic disease from iron deficiency anemia. J Lab Clin Med. 1992;119:385–90.[Medline]
39. Pettersson T, Kivivuori SM, Siimes MA. Is serum transferrin receptor useful for detecting iron-deficiency in anaemic patients with chronic inflammatory diseases? Br J Rheumatol. 1994;33:740–4.
40. Domellof M, Dewey KG, Lönnerdal B, Cohen RJ, Hernell O. The diagnostic criteria for iron deficiency in infants should be reevaluated. J Nutr. 2002;132:3680–6.
41. Ramco Laboratories. An in vitro enzyme immunoassay for quantifying human transferrin receptor in serum or plasma as an aid in the diagnosis of iron deficiency anemia, particularly in the presence of other disease status. 1998; Houston, TX.
42. Siimes MA, Salmenpera L, Perheentupa J. Exclusive breast-feeding for 9 months: risk of iron deficiency. J Pediatr. 1984;104:196–9.[Medline]
43. Muslimatun S, Schmidt MK, West CE, Schultink W, Hautvast JG, Karyadi D. Weekly vitamin A and iron supplementation during pregnancy increases vitamin A concentration of breast milk but not iron status in Indonesian lactating women. J Nutr. 2001;131:2664–9.
44. Celada A, Busset R, Gutierrez J, Herreros V. No correlation between iron concentration in breast milk and maternal iron stores. Helv Paediatr Acta. 1982;37:11–6.[Medline]
45. Yurdakok K, Temiz F, Yalcin SS, Gumruk F. Efficacy of daily and weekly iron supplementation on iron status in exclusively breast-fed infants. J Pediatr Hematol Oncol. 2004;26:284–8.[Medline]
46. Irwin JJ, Kirchner JT. Anemia in children. Am Fam Physician. 2001;64:1379–86.[Medline]
47. Bridges N, Parvin RM, van Assendelft OW. Evaluation of a new system for hemoglobin measurement. Am Clin Prod Rev. 1987;22:2–5.
48. Carlson DA, Daigneault RW, Statland BE. Evaluation of the hemocue photometer for measurement of blood donor hemoglobin. 40th Anniversary Meeting of the American Association of Blood Banks, November, 1987; Orlando, FL.
49. von Schenck H, Falkensson M, Lundberg B. Evaluation of "HemoCue," a new device for determining hemoglobin. Clin Chem. 1986;32:526–9.
50. Sari, M., de Pee, S., Martini, E., Herman, S., Sugiatmi, Bloem, M. W. & Yip, R. (2001) Estimating the prevalence of anaemia: a comparison of three methods. Bull World Health Organ 79: 506–511.[Medline]
51. Binkin NJ, Yip R. When is anemia screening of value in detecting iron deficiency? In: Hercberg S, Galan P. Dupin H, editors. Recent knowledge on iron and folate deficiencies in the world. Colloq INSERM. 1990;197:137–46.
52. McMillan JA, Landaw SA, Oski FA. Iron sufficiency in breast-fed infants and the availability of iron from human milk. Pediatrics. 1976;58:686–91.
53. Pastel RA, Howanitz PJ, Oski FA. Iron sufficiency with prolonged exclusive breast-feeding in Peruvian infants. Clin Pediatr (Phila). 1981;20:625–6.
54. Pisacane A, De Vizia B, Valiante A, Vaccaro F, Russo M, Grillo G, Giustardi A. Iron status in breast-fed infants. J Pediatr. 1995;127:429–31.[Medline]
55. Saarinen UM. Need for iron supplementation in infants on prolonged breast feeding. J Pediatr. 1978;93:177–80.[Medline]
56. Pizarro F, Yip R, Dallman PR, Olivares M, Hertrampf E, Walter T. Iron status with different infant feeding regimens: relevance to screening and prevention of iron deficiency. J Pediatr. 1991;118:687–92.[Medline]
57. Calvo EB, Galindo AC, Aspres NB. Iron status in exclusively breast-fed infants. Pediatrics. 1992;90:375–9.
58. Morrow AL, Reves RR, West MS, Guerrero ML, Ruiz-Palacios GM, Pickering LK. Protection against infection with Giardia lamblia by breast-feeding in a cohort of Mexican infants. J Pediatr. 1992;121:363–70.[Medline]
59. Kramer MS, Kakuma R. Optimal duration of exclusive breastfeeding. The Cochrane Library, Issue 2, Chichester, UK: John Wiley & Sons; 2005.
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