Original Article
Long-Term Developmental Outcome of Infants with Iron Deficiency
N Engl J Med 1991; 325:687-694September 5, 1991
- Abstract
- Abstract
Background.
Iron-deficiency anemia has been associated with lowered scores on tests of mental and motor development in infancy. However, the long-term developmental outcome of infants with iron deficiency is unknown, because developmental tests in infancy do not predict later intellectual functioning.
Methods.
This study is a follow-up evaluation of a group of Costa Rican children whose iron status and treatment were documented in infancy. Eighty-five percent (163) of the 191 children in the original group underwent comprehensive clinical, nutritional, and psychoeducational assessments at five years of age. The developmental test battery consisted of the Wechsler Preschool and Primary Scale of Intelligence, the Spanish version of the Woodcock—Johnson Psycho-Educational Battery, the Beery Developmental Test of Visual—Motor Integration, the Goodenough—Harris Draw-a-Man Test, and the Bruininks—Oseretsky Test of Motor Proficiency.
Results.
All the children had excellent hematologic Status and growth at five years of age. However, children who had moderately severe iron-deficiency anemia as infants, with hemoglobin levels ≤100 g per liter, had lower scores on tests of mental and motor functioning at school entry than the rest of the children. Although these children also came from less socioeconomically advantaged homes, their test scores remained significantly lower than those of the other children after we controlled for a comprehensive set of background factors. For example, the mean (—SD) adjusted Woodcock—Johnson preschool cluster score for the children who had moderate anemia in infancy (n = 30) was 448.6±9.7, as compared with 452.9±9.2 for the rest of the children (n = 133) (P<0.01); the adjusted visual—motor integration score was 5.9±2.1, as compared with 6.7±2.3 (P<0.05).
Conclusions.
Children who have iron-deficiency anemia in infancy are at risk for long-lasting developmental disadvantage as compared with their peers with better iron status. (N Engl J Med 1991; 325:687–94.)
Article Activity
- Article
SEVERAL consistent results have emerged from five recent studies of the behavior and development of infants with iron-deficiency anemia, a condition that affects at least 20 to 25 percent of the world's babies.1 , 2 All five studies3 4 5 6 7 used careful definitions of iron status and included comparison groups without anemia, and all showed that infants with anemia scored lower on tests of mental development administered before treatment than infants without anemia (an average of 6 to 14 points lower on the Bayley Scales of Infant Development). Four of the studies found that the anemic infants' scores on tests of motor development were lower as well (by an average of 9 to 11 points).3 , 5 6 7 With respect to the effects of iron therapy on the infants' behavior, one to two weeks of treatment did not produce significantly greater increases in scores on developmental tests for infants with anemia who were treated with iron in any study that included a placebo group3 , 6 7 8 (and Moffatt MEK: personal communication). In the three studies that examined infants' performance on developmental tests and their behavior after a two-to-three-month course of iron therapy similar to that used in pediatric practice, most infants with iron-deficiency anemia did not have improvement in test scores, even though they had a good hematologic response to iron therapy.6 , 7 , 9
Because developmental tests in infancy do not prediet later intellectual functioning,10 it has been unclear whether the lower test scores of infants with iron-deficiency anemia indicated a condition that would resolve spontaneously or one that would persist into the school years. Concern about this question motivated our reevaluation of a group of five-year-old Costa Rican children whose iron status and iron treatment had been carefully documented in infancy.
Methods
Population
The original study of 191 infants was conducted in the urban community of Hatillo, located at an elevation of 1100 m near San José, the capital of Costa Rica. The population of the community was predominantly lower-middle-class, and the infants' parents had an average of 8 to 10 years of education. The study consisted of door-to-door screening of the entire community and included singleton infants 12 to 23 months old with birth weights ≥2.5 kg who had had uncomplicated births, who had no acute or chronic medical problems, and who had normal physical examinations. These healthy infants had low blood lead levels (mean, 0.52 μmol per liter of whole blood [10.8 μg per deciliter]; range, 0.26 to 1.04 μmol per liter [5.4 to 21.5 μg per deciliter]) and normal hemoglobin electrophoreses and hemoglobin A2 levels; had no evidence of growth failure or deficiencies of vitamin B12, folic acid, or protein; and were free of parasites, except ascaris in 2 percent and Giardia lamblia in 5 percent. Their iron status in infancy, determined by measurement of venous levels of hemoglobin, transferrin saturation, erythrocyte protoporphyrin, and serum ferritin, varied from iron sufficiency to moderate iron-deficiency anemia (defined as a hemoglobin level ≤100 g per liter, a serum ferritin level ≤12 μg per liter, and either an erythrocyte protoporphyrin level >1.77 μmol per liter [100 μg per deciliter] of packed red cells or transferrin saturation ≤10 percent). (Hemoglobin values at this altitude are approximately 4 g per liter higher than the corresponding values at sea level.) Comprehensive information was collected about each child and his or her family, including demographic characteristics, birth history, nutritional status, socioeconomic status, level of stimulation in the home, and parental IQ. The Bayley Scales of Infant Development11 were administered before the intramuscular or closely supervised oral administration of iron, with appropriate placebo controls, and one week and three months thereafter. Details of the original study have been published previously.6
The infants with moderate iron-deficiency anemia had lower scores than the rest of the sample on tests of mental and motor functioning both before and after treatment, even though their hematologic response to iron therapy was excellent, with an average increase of 37 g per liter in the hemoglobin level. In all the infants with iron-deficiency anemia, the anemia was corrected with three months of iron therapy, but many infants (64 percent) still had biochemical abnormalities, such as elevated erythrocyte protoporphyrin values. When data analysis made it clear that these infants still had lower scores on developmental tests, the children enrolled in the early part of the study were already two to three years old. Since iron status often improves in the preschool years as the growth rate slows and dietary iron intake increases, it was not clear whether additional iron therapy would be of benefit or not. Nonetheless, each previously anemic child who became iron sufficient in infancy was matched on the basis of age and sex with two previously anemic children who continued to have evidence of iron deficiency; after random assignment, one of the two received an additional three months of iron therapy between three and four years of age. All others had comparable contact with study personnel, who were not aware of the children's iron status. This additional treatment, though clearly limited as an experimental intervention, seemed to be a reasonable approach to the unexpected findings that lower scores on developmental tests persisted after the initial iron treatment.
For the present follow-up study, project psychologists contacted each family in the original study one to two months before the child's fifth birthday. Eighty-five percent of the families in the original cohort (163 of 191) were located and agreed to participate in the follow-up assessments. Written informed consent for the follow-up evaluation was obtained by the pediatrician. The follow-up protocol, like the initial study design, was approved by the institutional review boards of University Hospitals, Case Western Reserve University School of Medicine, Cleveland, and of the Hospital Nacional de Niños, the Social Security Administration, and the National Ministry of Health, San José, Costa Rica. All but 15 children were tested within two weeks of their fifth birthdays (age range, 59 to 63 months).
The relatively low attrition rate (15 percent) was noteworthy, given the long-term follow-up involved. There was no difference in attrition according to background characteristics, iron status in infancy, or initial scores on mental-development tests. Those who were lost to follow-up had slightly higher mean (±SD) initial scores on tests of motor development than those who were reexamined (115.4±16.7 vs. 109.3±16.1,P = 0.07). The effect of this difference on the results at five years would probably be to decrease slightly the motor scores of the entire sample, since attrition did not vary as a function of iron status.
Procedure
The five-year follow-up assessments were conducted in two sessions of 1 1/2 to 2 hours each. They included a complete physical examination and detailed neurologic evaluation, venipuncture for collection of a blood specimen to determine current iron status (indicated by hemoglobin level, transferrin saturation, erythrocyte protoporphyrin level, and serum ferritin level), and a psychoeducational test battery consisting of the Wechsler Preschool and Primary Scale of Intelligence,12 the Goodenough—Harris Draw-a-Man Test,13 the Beery Developmental Test of Visual—Motor Integration,14 the Spanish version of the Woodcock—Johnson Psycho-Educational Battery,15 and the Bruininks—Oseretsky Test of Motor Proficiency.16 In addition, a home visit was made by study psychologists to administer the preschool version of the HOME (Home Observation for Measurement of the Environment scale,17 a well-validated measure of the degree of stimulation in the home), and to gather further information on the family's current circumstances. The study personnel were unaware of the children's hematologic status and treatment in infancy, but the families had been given this information at the conclusion of the initial infant study.
In this follow-up assessment we used several measures that were developed and standardized in the United States. Although applying such tests in another culture is always a matter of concern, this group of Costa Rican children did not have lower scores than those considered normal in the United States. During infancy, the mean (±SD) score of the entire sample on the Bayley Mental Development Index was 103.1±15.1, as compared with the U.S. norm of 100±16, and the score on the Psychomotor Development Index averaged 110.2±16.3, as compared with the U.S. norm of 100±16. At five years of age, the children's full-scale IQ scores averaged 103.8±11.8, as compared with the U.S. norm of 100±15, and their motor scores were similar to U.S. norms on the Bruininks—Oseretsky Test of Motor Proficiency. The average total HOME score of 29.8 in infancy was similar to the average of 31.2 in the U.S. standardization sample.17 These observations suggest that the measures were appropriate for use in Costa Rica. Furthermore, the stringent entrance criteria used in this study were effective in identifying a group of normal children, who continue to test in the normal range by U.S. standards.
Statistical Analysis
Analysis of variance was the primary statistical technique used to determine whether iron-deficiency anemia in infancy was associated with lower scores on developmental tests at five years of age. Analysis of variance was also used to detect differences in background variables and nutritional status at five years. Categorical variables were analyzed by the chi-square test. The effects of potentially confounding variables were controlled in multiple regression analyses, and analysis of covariance was used to generate adjusted means.
Results
nutritional Outcome
The first step in assessing outcome at five years of age was to evaluate the effect of receiving additional iron in the preschool period. The children who had anemia in infancy were found to be comparable on measures of iron status and development at five years of age, regardless of whether they had become iron sufficient in infancy and whether or not they received additional iron therapy in the preschool years (data are available elsewhere*). The additional treatment was therefore not a factor in our further analysis.
Children who had had moderate anemia (hemoglobin level ≤100 g per liter) were found to be comparable to those who had had better iron status in infancy on all nutritional measures at five years of age (Table 1Table 1
nutritional Status at Five Years of Age.*). In general, the children's iron status was excellent, comparable to that in the reference sample of 5-to-10-year-old U.S. children who were free of iron deficiency in the Second National Health and Nutrition Examination Survey (NHANES II).18 The children's general nutritional status, as reflected in their growth, was also excellent. These Costa Rican five-year-olds, on average, had heights and weights at the 50th percentile for U.S. reference populations.19 , 20 Developmental Testing
The children who had moderate iron-deficiency anemia in infancy still scored lower than the rest of the children on tests of mental and motor functioning at
*See NAPS document no. 04889 for 15 pages of supplementary material. Order from NAPS c/o Microfiche Publications, P.O. Box 3513, Grand Central Station, New York, NY 10163–3513. Remit in advance (in U.S. funds only) $7.75 for photocopies or $5 for microfiche. Outside the U.S. and Canada add postage of $4.50 ($1.50 for microfiche postage). There is a $15 invoicing charge on all orders filled before payment. five years of age (Table 2Table 2
Scores on Developmental Tests at Five Years of Age.*). Statistically significant differences in test scores were found on all tests except the verbal IQ, the spatial-relations and visual—auditory-learning subtests of the Woodcock—Johnson battery, and the Goodenough—Harris Draw-a-Man Test. In general, the magnitude of the differences in test scores was greater for tasks requiring nonverbal skills, visual—motor integration, and motor coordination than for purely verbal tasks (Fig. 1Figure 1
Differences in Results of Developmental Tests at Five Years of Age between Children Who Had Moderate Iron-Deficiency Anemia in Infancy and the Comparison Group.).Potentially Confounding Variables
In the original study the lower mental and motor test scores of the infants with iron-deficiency anemia remained statistically significant even after we controlled for background factors.6 Nonetheless, children who had moderate anemia as infants differed in a variety of ways from the rest of the children. More of them were male (74 vs. 52 percent, P = 0.02); they weighed slightly less at birth (mean [±SD] weight, 3.12±0.44 vs. 3.33±0.43 kg; P = 0.01); and they were weaned from breast-feeding earlier (at 16.7±17.2 vs. 33.3± 25.3 weeks, P<0.001). Their home environments were less stimulating in infancy (total HOME score, 25.6± 6.3 vs. 30.7±6.5; P<0.001), but no differences on the HOME scale were found at five years. More of the children with anemia had grown up in households in which the father was absent (41 vs. 20 percent, P = 0.01), had lived with their grandparents (62 vs. 36 percent, P = 0.005), or both. Their mothers were somewhat shorter (height, 153.0±5.6 vs. 155.8±5.3 cm; P = 0.01) and had lower IQ scores on a Spanish version of the Wechsler Adult Intelligence Scale (WAIS)21 (74.6±10.6 vs. 84.1±13.2, P<0.001). These IQ scores are probably comparable to those of women of lower socioeconomic status who have young children in the United States. Although we were unable to find data on WAIS scores for such a group, information was available for the Peabody Picture Vocabulary Test,22 a brief test that is often used in place of full-scale IQ testing. In the United States, white mothers with 12 years of education averaged 87 on the Peabody test,23 and black mothers with 11 years of schooling averaged in the mid-70s.24
In the current study, as in the earlier study, multiple regression analyses were used to control for differences in background characteristics before we considered the effects of moderate iron-deficiency anemia in infancy on the developmental outcome at five years of age. The relations between moderate iron-deficiency anemia and both the full-scale IQ and the Woodcock—Johnson picture-vocabulary subtest were the only ones that were no longer statistically significant (P = 0.13 for both comparisons). Differences in test scores with and without adjustment for confounding factors are shown in Table 2.
Exploratory Analyses
Our results suggested that scores on developmental tests did not drop in this population unless iron deficiency in infancy was chronic and severe enough to cause anemia with hemoglobin levels ≤100 g per liter. To determine whether this conclusion was warranted, we conducted further analyses of children who had had iron deficiency with hemoglobin levels above 100 g per liter. Test scores at five years of age were examined in relation to pretreatment iron status in infancy, with use of the iron-status categories from the original study,6 individual iron values treated as continuous variables, and intervals of hemoglobin levels (≤100 g per liter, 101 to 110 g per liter, 111 to 119 g per liter, and ≥120 g per liter). No significant correlations with test scores were found, and the distribution of the values did not indicate any other threshold level (data on these analyses are available elsewhere*). However, iron status after treatment in infancy did identify another group with lower scores at five years of age. Among children with initial hemoglobin levels above 100 g per liter, those in whom three months of iron therapy had not fully corrected the iron deficiency had lower scores on developmental tests at five years. There were no statistically significant differences on any test of mental or motor development between these children and those who had moderate anemia, and both groups had lower test scores than the other children in a variety of areas (Table 3Table 3
Adjusted Test Scores at Five Years of Age and Response to Iron Therapy in Infancy.*). In contrast, children with hemoglobin levels above 100 g per liter whose iron deficiency had been fully corrected in infancy did at least as well as those who had maintained good iron status throughout the infant study (defined as those with normal hemoglobin levels and either all three measures of iron status in the normal range or a low ferritin level as the sole abnormality). Figure 2Figure 2
Differences in Results of Developmental Tests at Five Years of Age According to Iron Status before and after Treatment in Infancy. illustrates these findings, with children with good iron status before and after treatment used as the reference group.Like the group with moderate anemia, the children who were still iron deficient after treatment had evidence of more severe and chronic iron deficiency. They had lower initial hemoglobin levels and higher initial erythrocyte protoporphyrin values than the children whose iron deficiency had been corrected (mean hemoglobin level, 109 vs. 114 g per liter; mean erythrocyte protoporphyrin level, 3.41 vs. 2.55 μmol per liter [192.6 vs. 143.9 μg per deciliter] of packed red cells; P<0.05 for both comparisons). The children who remained iron deficient also came from less socioeconomically advantaged families. Like the group with moderate anemia, they had mothers with less education and lower IQ scores, and their homes were less stimulating. A greater proportion of the group was male than of the sample as a whole. Most differences in test scores remained statistically significant after we controlled for such background variables (Table 3). However, the outcome for the children who did not respond fully to treatment may have been influenced by factors other than those affecting the group with moderate anemia. Their hematologic response to iron therapy in infancy was less dramatic, with an average increase in the hemoglobin level of only 11 g per liter (as compared with 37 g per liter for the group with moderate anemia) and an average final erythrocyte protoporphyrin value of 204 μmol per liter (115 μg per deciliter) of packed red cells.
Discussion
In this study we reevaluated a group of five-year-old Costa Rican children whose iron status had been documented in infancy and in whom anemia had been corrected by carefully supervised iron therapy. The children who had moderate iron-deficiency anemia as infants still had lower scores on tests of mental and motor functioning at five years of age. These differences remained statistically significant after we controlled for a comprehensive set of background factors.
An unexpected finding was that children who had hemoglobin levels above 100 g per liter before treatment and iron deficiency both before and after treatment also had poorer outcomes at five years of age. The duration and severity of iron deficiency may be important factors in understanding these observations. Both the children with moderate anemia and those with iron deficiency after three months of treatment probably had more severe iron deficiency, as evidenced by lower initial hemoglobin levels and higher initial erythrocyte protoporphyrin values. However, differences in the response to iron therapy suggest that conditions such as undetected giardiasis25 or vitamin A deficiency26 may have affected children with initial hemoglobin levels above 100 g per liter in whom iron deficiency was not completely corrected by three months of carefully supervised treatment.
Some of the results of this study are similar to those of two other follow-up studies of children who had anemia as infants. A study by Palti et al.,27 based on data from a comprehensive health-surveillance program in Israel, found that lower hemoglobin levels at nine months of age were associated with lower developmental and IQ scores and less desirable behavior in the preschool years27 and at school age,28 even after other important factors, such as maternal education, social class, and birth weight, were considered. The second study, by Dommergues et al.29 in France, found that children who had anemia as two-year-olds continued to have lower test scores at four years of age. Although the results are congruent with ours, these studies used more limited measures of iron status, response to iron therapy, or development. However, preliminary results from another follow-up study using a comprehensive set of measures, conducted by Walter and associates in Chile, indicate that formerly anemic children still have lower test scores than other children at 5 1/2 years of age.30
The consistency in the findings of the available long-term studies indicates that the lower scores on developmental tests of children with iron-deficiency anemia in infancy persist years after the period of deficiency. However, the threshold for the hemoglobin level at which iron-deficiency anemia was associated with lower scores varied from study to study. It would therefore be premature to generalize cut-off points from any study to populations in which different conditions, such as altitude, infectious diseases, and diet, affect iron status.
None of the studies available to date prove that iron deficiency caused the children's lower test scores in infancy and at five years of age.31 Establishing a cause- and-effect relation between two factors on the basis of correlational data depends on documenting a reliable association between them, confirming that the supposed cause precedes the supposed effect in time, and proving that the relation is neither spurious nor fortuitous — that is, that the association cannot be explained by some other factor or by chance alone.32 Recent research on the relation between iron-deficiency anemia in infancy and children's behavior meets the first criterion of reliable association, but not the others. A prospective study would be needed to demonstrate that the behavior of infants with iron deficiency was not different from that of nondeficient infants before the onset of the deficiency. Even if preexisting behavioral differences were absent, other conditions closely associated with iron deficiency could account for the observed alterations in behavior. A deficiency of one nutrient suggests that the intake of calories or other nutrients might also be inadequate. This possibility must be kept in mind, even though no evidence for other deficiencies was found in the recent studies in Costa Rica and Chile6 , 7 and even though the children's hematologic response to iron confirms that they had iron deficiency. It is also difficult to be sure that the children never had a recurrence of iron deficiency after the initial study. Iron deficiency is less common in the preschool years, however, and the children's iron status was normal at five years of age.
In contrast, differences in the home environment are likely.18 , 33 34 35 In this study, statistical control for differences in background variables did not eliminate the significant effect of chronic and severe iron deficiency on developmental-test scores. However, the available measures of the home environment are too crude to dismiss the possibility that differences among families accounted for the difference in scores. In fact, it seems probable that there were other important differences in the degree of stimulation and type of care the children received. Thus, as with several other risk factors,36 37 38 39 40 41 such as low birth weight, elevated blood lead levels, and generalized undernutrition, a worse developmental outcome in infants with iron deficiency may be inextricably linked to perinatal and environmental factors.31 , 42
Despite such unresolved issues, the results of this study indicate that relatively severe and chronic iron deficiency in infancy may serve as a convenient marker for any associated factors that contribute to poor developmental outcome but are harder to identify during routine pediatric care. Our findings also call into question the adequacy of current therapeutic approaches. The possibility that earlier detection of iron deficiency or longer treatment in infancy might be effective in preventing developmental disadvantage needs to be assessed. Infants with severe and chronic iron deficiency may also require special intervention in addition to iron therapy. Such intervention — for example, enrichment programs — would ideally be targeted to the specific alterations in behavior observed in infants with iron deficiency and tailored to the special needs of their families. However, given the findings to date that lower test scores persist, a vigorous effort to prevent iron deficiency is the safest approach.
Supported by a grant (R22 HD14122–10) from the National Institutes of Health.
Preliminary results were presented at the meetings of the New York Academy of Medicine, New York, March 9, 1989, and the Society for Pediatric Research, Washington, D.C., May 4, 1989.
We are indebted to the families in the study for their continued dedication to this project; to the research team in Costa Rica, especially Angela Radan, Maria Elena Chacon, and Patricia Alvarado for assessments of the children and their families, Rafael Jimenez, M.Q.C., M.Sc., and Luis A. Mora, M.Q.C., for laboratory evaluations, Yvonne Gomez, M.D., Ada Oveido, M.D., and Zulma Campos, M.D., for providing pediatric care, and Denney Artavia for data entry; to Edward C. Nelson, Ph.D., for extensive discussions that led us to broaden the context in which we considered the effects of early iron deficiency and for designing the figures; to Donna K. McClish, Ph.D., for consultation on statistical analysis and Nancy K. Klein, Ph.D., for consultation on the psychoeducational test battery; to Barbara T. Felt, M.D., and Peter R. Dallman, M.D., for their critical comments; to Information Systems of MetroHealth Medical Center for the use of their computer facilities; to Lois Klaus for data processing; to Dorise Hunter for assistance in the preparation of the manuscript; and to Claudia Brittenham for scoring the children's drawings.
Source Information
From the Departments of Pediatrics (B.L.) and Psychiatry (A.W.W.), Rainbow Babies and Childrens Hospital, MetroHealth Medical Center, Case Western Reserve University School of Medicine, Cleveland, and Hospital Nacional de Niños, University of Costa Rica, San José, Costa Rica (E.J.). Address reprint requests to Dr. Lozoff at the Rainbow Babies and Childrens Hospital, 2074 Abington Rd., Cleveland, OH 44106.
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