Published online August 28, 2006
PEDIATRICS Vol. 118 No. 4 October 2006, pp. e1055-e1060 (doi:10.1542/peds.2006-0024)
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ARTICLE

The Incidence of Anemia in an Israeli Population: A Population Analysis for Anemia in 34512 Israeli Infants Aged 9 to 18 Months

Joseph Meyerovitch, MDa,b, Michael Sherf, MD, MPHa,c, Felice Antebi, MBSa, Marie Barhoum-Noufi, MDd, Zeev Horev, MDe, Lutfi Jaber, MDf, Dorit Weiss, RN, PhDg and Ariel Koren, MDh

a Research and Health Planning Department, Health Planning and Policy Division
d Pediatric Health Center, Nazareth District
e Community Medical Division
g Community Nursing Division, Clalit Health Services, Tel Aviv, Israel
b Institute for Endocrinology and Diabetes, National Center for Childhood Diabetes, Schneider Children's Medical Center of Israel, Tel Aviv University, Sackler School of Medicine, Tel Aviv, Israel
c Department of Family Medicine, Ben-Gurion University, Beer-Sheva, Israel
f Neurology Clinic, Schneider Children's Medical Center of Israel, Tel Aviv University and Bridge to Peace Community, Tel Aviv, Israel
h Pediatric Hematology Unit and Pediatric Department B, Ha'Emek Medical Center, Afula and the Ruth and Baruch Rapapport School of Medicine, Technion, Haifa, Israel


    ABSTRACT
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
OBJECTIVES. The purpose of this work was to use the comprehensive computerized database of Clalit Health Services to analyze the prevalence and contributing factors of anemia among the population of Clalit Health Services-insured Israeli infants aged 9 to 18 months, characterized by ethnic sector.

METHODS. This was a cross-sectional retrospective study for the year 2003 using the computerized database of Clalit Health Services for 34512 infants aged 9 to 18 months insured by the Clalit Health Services sick fund. Children with abnormal white blood counts at the time of the hemoglobin test and with chronic diseases were excluded. The data were analyzed for age, infant hemoglobin level, ethnic origin, district distribution, type of clinic where the infant received treatment, the number of iron prescriptions dispensed to each child, and the mother's last hemoglobin level before giving birth. Anemia was defined as a hemoglobin level <105 g/L.

RESULTS. The prevalence of anemia among Israeli infants is 15.5%. The prevalence is significantly higher in the non-Jewish population (22.5%) as compared with the Jewish population (10.5%). The lowest prevalence of anemia was found in pediatric health centers (10.7%). A significant correlation was found between the presence of anemia in infants and the presence of anemia found in their mothers. Infants with anemia used significantly less iron preparations.

CONCLUSIONS. This study is one of the first studies to use a comprehensive computerized database to perform a population-based analysis of anemic infants. We found a considerable percentage of infants to be anemic and identified a specific population to be at high risk for anemia. We describe 2 factors that have the potential to be altered through intervention: improving compliance of iron intake and maternal anemia. Major national efforts should be made to minimize the prevalence of anemia, especially in the non-Jewish population, and to learn more about the causes of iron-deficiency anemia in this group. This study provides a base for an intervention study.


Key Words: iron deficiency • anemia • medical computerized database • infancy

Abbreviations: CHS—Clalit Health Services • IDA—iron-deficiency anemia

Clalit Health Services (CHS), the largest sick fund in Israel and one of the largest in the world, insuring >3.5 million people, has a computerized database that includes demographic data, a chronic disease registry, and all of the laboratory data, as well as data on health services used by its insured. The existence of such a database enabled us to perform one of the first population-based analyses using comprehensive and documented data.

Iron-deficiency anemia (IDA) in infants is a common problem worldwide and an enormous public health risk in developing countries. The prevalence of anemia in infants varies between <5% and 43% according to the population studied and the cutoff hemoglobin level used to define anemia in infancy.14 An even larger proportion of infants suffer from iron deficiency without anemia. The incidence is relatively low in developed countries, but even in these countries the incidence of IDA in low-income populations is significantly higher than in children belonging to high-income populations. In populations with a high frequency of anemia in infants we can assume that iron deficiency is the main cause of anemia.

Several studies have proven that iron deficiency in infants has a deleterious effect on growth and development, not only during infancy, but also in older children, causing significant irreversible alterations in behavior and learning capacity unless the iron deficiency is rapidly corrected or prevented.58

The Nutrition Committee of the American Academy of Pediatrics published specific recommendations for the prevention of IDA in infants.9 As of 1985, the Ministry of Health in Israel adopts similar recommendations. At or near the age of 12 months, a routine hemoglobin screening is also recommended.10 Iron-fortified cereal and meat intake should be encouraged during the second and even third year of life.

The purpose of this study was to use the comprehensive computerized database of CHS to analyze the prevalence and contributing factors of anemia among the population of CHS-insured Israeli infants aged 9 to 18 months, characterized by ethnic sector.


    METHODS
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
CHS has a state-of-the-art computerized data warehouse. Almost all of the data on medical service use by CHS members, as well as demographic data, are aggregated in this data warehouse and can be queried down to the level of an individual member. For the purpose of our study, we queried the demographic data, primary physician type, number of iron preparations purchased, the infant's hemoglobin and white blood count tests including results, mother's hemoglobin level, and the chronic illness registry.

The study was conducted using the data of 2003. The study population includes all of the infants aged 9 to 18 months insured by the CHS sick fund. Infants suffering from chronic diseases and infants with abnormal white blood counts at the time of the test were excluded. The data obtained included age, ethnic origin, infant's hemoglobin level, number of iron prescriptions dispensed to each child by CHS pharmacies, and the mother's last hemoglobin value before giving birth. The Rabin Medical Center ethics board approved the study protocol.

Anemia was defined as a hemoglobin level <105 g/L. In cases of infants with >1 hemoglobin analysis, only the first value was included.

Mothers were matched with their children using the database that includes family demographic data, and only the last blood count performed before birth was included in the study. Mothers were considered to be anemic if the hemoglobin values were <120 g/L. Data of iron preparations purchased at CHS pharmacies, and not in private pharmacies, enter the computerized database and were available to us.

Comparisons were made among the total population of anemic children, anemic children belonging to clinics of the Jewish sector, and anemic children belonging to clinics of the non-Jewish sector to examine any possible differences between the sectors. The categorical data analyzed included clinic type (proportions test), age (proportions test), iron supplementation ({chi}2), and mother's hemoglobin level before giving birth ({chi}2). For all the statistical analyses, the P values are provided. All of the testing was performed using the Excel Analysis Toolpak (Microsoft, Redmond, WA).


    RESULTS
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
A total of 34512 infants with hemoglobin determination were studied, and 19931 were of Jewish origin and 14581 of non-Jewish origin. The infants were born during the years 2002–2003 and aged 9 to 18 months when studied.

The present study includes 49.7% (66411) of the infants insured by CHS in this age group. Approximately 55% of the blood counts were performed on infants aged 11 to 13 months, in accordance with the recommendations of the Ministry of Health. We found that 15.5% of the infants had a hemoglobin concentration of <105 g/L. The highest prevalence of anemia was found at 10 months old, whereas at 11 to 13 months old, the prevalence was lowest (Fig 1A). The prevalence of anemia is significantly higher in the non-Jewish population, 22.5%, as compared with the Jewish population, at 10.5% (P < .001; Fig 1B). In a subgroup of the Jewish population, the extremely religious group, the frequency of anemia is closer to that of the non-Jewish population (18.9%).


Figure 1
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FIGURE 1 A, Percentage of anemic infants by age (total number of infants in parentheses). B, Percentage of anemic infants by age and sector (total number of infants in parentheses).

 
When comparing the prevalence of anemia by clinic characteristics, in both sectors the highest rate was found in rural clinics (19.1%; non-Jewish sector: 32.5%; Jewish sector: 13.6%), and the lowest prevalence was found in the pediatric health centers of the CHS sick fund (10.7%; non-Jewish sector: 21.0%; Jewish sector: 6.7%). Maternal predelivery hemoglobin records were obtained for 21047 infants, at 61%. A significant correlation was found between the presence of anemia in infants and anemia found in their mothers (P < .001). The percentage of anemic mothers with anemic infants was significantly higher among the non-Jewish population as compared with the Jewish population (23% vs 11%; P < .001; Fig 2). When comparing anemic and nonanemic infants receiving ≥2 preparations of iron with infants receiving <2 preparations of iron before their first blood test, a significant difference was found in the overall group, as well as in each sector (P < .02; Fig 3).


Figure 2
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FIGURE 2 Percentage of anemic infants by mother's anemia before giving birth and sector (total number of infants in parentheses).

 

Figure 3
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FIGURE 3 Percentage of anemic infants by number of iron supplements purchased before blood test and sector (total number of infants in parentheses).

 

    DISCUSSION
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In this study we used the computerized databases of the CHS sick fund to study the incidence of anemia in healthy Israeli infants aged 9 to 18 months and to look at demographic characteristics, use of iron preparations, and maternal anemia on incidence of anemia in this population. The World Health Organization recommends a hemoglobin level of 110 g/L as a cutoff point for the diagnosis of anemia in the pediatric population.11 The Nelson Textbook of Pediatrics recommends a level of 105 g/L as the cutoff point for the diagnosis of anemia in infants aged 9 to 18 months.12 A survey performed by Sheriff et al13 in the United Kingdom suggests that the cutoff point should be based on the fifth percentile of hemoglobin levels, which was found to be 100 g/L.

In this study, we found a prevalence of anemia of 15.5%. The prevalence was found to be higher at 9 to 10 months old and after the age of 13 months. This difference may be explained by the fact that blood counts are performed around the age of 12 months as a routine, whereas at an earlier age, blood counts are probably performed because of clinical suspicions of anemia. Beyond the age of 13 months, the frequency of anemic infants resurged, which may represent poor compliance both in the performance of routine blood analyses beyond the recommended age and in following the recommended iron prophylactic treatment.

This incidence was found to be in the same range as the frequency reported by other countries worldwide. The prevalence changed dramatically when we examined the different ethnic groups that comprise the Israeli population. In the non-Jewish population, the prevalence is higher than the mean as compared with the Jewish population, and in a subgroup of the Jewish population, the extremely religious group, the frequency of anemia is closer to that of the non-Jewish population. The demographic and socioeconomic status of this group is similar to the non-Jewish population, that is, commonly large and low-income families, as compared with the smaller and higher income families in the Jewish nonextremely religious population.

As we know from previous studies performed in Israel, the leading cause of anemia in Arab infants is iron deficiency (Shehab et al14 and A. K., verbal communication, 2005) . Other reasons for anemia in this population, such as thalassemia carriers, are responsible for <10% of anemia.15 Among the Jewish population, the carrier rate of thalassemia is significantly less frequent.

In the 1980s, several studies performed in Israel found a high frequency of anemia in infants, between 23% and 68%. The frequency of iron deficiency without anemia was found to be even higher (76%).1620 During the same period, similar frequencies of anemia in infants were found in several studies throughout the western world, which found significant differences between white and nonwhite children.21, 22 In developed countries, the incidence is even lower. In Norway, only 2% to 5% of infants were found to have IDA.23

Other recent reports studied the frequency of IDA in the Arab world: 7.5% of Iranian infants aged 6 to 23 months have IDA, and another 11.4% are iron deficient.24 Another study from Jordan reported a higher frequency of anemia, at 72%.25

One of the most common causes of anemia in infants is prematurity. The percentage of premature infants in the Israeli population is 8.4% of live births, 8.7% in the Jewish population, and 7.7% in the non-Jewish population. This percentage is too small to explain the percentage of IDA found in our study.

In this study, the higher incidence of IDA that was found in rural areas can be explained by the population that belongs to a lower socioeconomic status than other areas. The high incidence of IDA in infants that belong to low-income families is a well-known fact that is frequently described in the literature.13, 21, 22 The lower incidence found among infants treated in health centers attended by pediatricians can be related to the high awareness of the pediatricians as to the importance of preventing IDA in infants.

In mothers with severe iron deficiency, there is little immediate effect on the newborn, but infant iron storages may be depleted at a very early stage. In addition, the iron-deficient mother's breast milk lacks sufficient iron quantities. Thus, infants born to anemic mothers are more prone to develop IDA than infants born to mothers with a satisfactory iron balance. In our study, there is an evident correlation between the maternal hemoglobin level tested before delivery and the frequency of IDA in their offspring. The incidence of IDA in infants born to anemic mothers is significantly higher than in infants born to nonanemic mothers (16.1% and 11.0%, respectively; P < .001), and there is a significant difference between non-Jewish and Jewish anemic infants born to anemic mothers (23.2% and 11.0%, respectively; P < .001). Among the non-Jewish population in Israel, multiparity, frequent deliveries, and prolonged breastfeeding are more common than in the Jewish population. This may partially explain the differences between both populations studied. In a recently published study from Jordan, infants born to anemic mothers were found to be more anemic than infants born to nonanemic mothers.25 The improvement found in hematology parameters in breastfed infants who received iron supplementation from 1 to 6 months old as compared with breastfed infants not receiving supplements may provide indirect evidence that breastfeeding by itself does not provide enough iron for infant growth.26

Of course, lack of compliance with the recommendations to give iron supplementation may be the most significant cause of IDA. The number of iron bottles supplied to anemic infants was significantly lower than that of the nonanemic group. This difference was significant in both sectors. It should be noted that iron supplements may be bought without a doctor's prescription in private pharmacies. Data for these supplements are not available in our databases.

A previous study performed in Israel found that, among low-income families, the compliance for iron supplementation was significantly higher than among families belonging to the higher socioeconomic levels. This study, as ours, is most probably biased because of the fact that high-income families purchase iron supplements from private pharmacies.27

Prevention of IDA can improve performance in school, avoid behavioral alterations, and assure better growth, thus allowing children to grow into healthier adults. In addition, the burden on the country's economy may be reduced if we prevent IDA at an early age, thus reducing health expenditure in the future. Longitudinal studies consistently indicate that children who are anemic in infancy continue to have poorer cognition, long-lasting adverse effects on auditory and visual function, poor school achievement, and more behavioral problems into middle childhood. Short-term iron treatment failed to produce benefits in development, and even IDA correction is incapable of correcting these defects.5, 7, 2830

Because of the deleterious effects of iron deficiency in infancy, prevention is crucial. According to the recommendations of the American Academy of Pediatrics of 1999, infants who are not breastfed should receive iron-fortified formulas containing 4 to 12 mg/L of iron, from birth to 12 months of age. This committee also concluded that parents and health care clinicians should be educated as to the role of iron in infant growth and cognitive development.9

The Israeli Ministry of Health recommends that iron supplement preparations be given to all infants aged 4 to 12 months. Premature infants should start iron supplementation at 2 months old, and breastfed infants should start iron supplementation at 6 months old, provided that the lactating mother has adequate iron stores.10

In our study, which covered approximately one third of the infants born yearly in Israel, a significant percentage of infants was found to be anemic, and because IDA is the most common cause of anemia in this age group, we can conclude that IDA is still a major health problem in Israeli children. Using the comprehensive database available at CHS, we are able to analyze large populations and search for the causes of IDA in Israeli infants. In addition, we have developed several quality indicators for the assessment and treatment of anemia in infants.

Significant national efforts should be made to improve the iron condition of our children to assure that they will grow into healthy adults. More significant efforts should be made among the non-Jewish population to analyze the causes of IDA in this group, and then special efforts should be made to minimize the prevalence of anemia. Currently, such a program, based on our study, is being prepared in CHS.


    FOOTNOTES
 
Accepted Apr 24, 2006.

Address correspondence to Joseph Meyerovitch, MD, Research and Health Planning Department, Health Planning and Policy Division, Clalit Health Services, 101 Arlozorov St, PO Box 16250, Tel Aviv 62098, Israel. E-mail: josephm{at}clalit.org.il

The authors have indicated they have no financial relationships relevant to this article to disclose.


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PEDIATRICS (ISSN 1098-4275). ©2006 by the American Academy of Pediatrics



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