Anemia in infancy: etiology and prevalence

Jornal de Pediatria - Vol. 78, Nº4, 2002 321
0021-7557/02/78-04/321
Jornal de Pediatria
Copyright © 2002 by Sociedade Brasileira de Pediatria
ORIGINAL ARTICLE
Anemia in infancy: etiology and prevalence
Maria Claret C.M. Hadler1, Yara Juliano2, Dirce M. Sigulem3
Abstract
Objective: to verify the prevalence of anemia, iron deficiency anemia and iron deficiency in infants,
at a Public Health Unit in the city of Goiânia - Brazil; to analyze and to correlate the hematologic and
biochemical variables.
Methods: a cross-sectional study was carried out. One hundred and ten full-term infants of the 120
mothers interviewed were included. The infants aged between six and twelve months and there were not
twins. Socioeconomic and hematologic data was obtained. Venous blood was taken from fasting infants
in order to carry out a complete hemogram through electronic cell counting, serum iron, serum ferritin and
C-reactive protein, which were used in the evaluation of the etiology of iron deficiency in the anemic
infants. Children with hemoglobin < 11g/dL were considered anemic.
Results: the prevalence of anemia was 60.9%. In the diagnosis of the iron deficiency etiology in infants
without an inflammation process, when considering the alteration of hemoglobin plus two more indices
among mean corpuscular volume (MCV) or mean corpuscular hemoglobin (MCH) or serum ferritin or
serum iron, the prevalence of the iron deficiency was 87%. Nevertheless, when red cell distribution width
(RDW) was included in the indices, the prevalence was 97.8%. In the non-anemic infants, considering
ferritin and RDW, the prevalence of iron deficiency observed was 28%. The best correlation among
hematologic and biochemical variables were between hemoglobin and hematocrit (r = 0.946), and MCH
with MCV (r = 0.950).
Conclusions: the main etiology in infants was iron deficiency anemia and its prevalence varied
according to different parameters and criteria.
J Pediatr (Rio J) 2002; 78 (4): 321-6: iron deficiency anemia, nutritional status, iron, epidemiologic
factors, infant, acute-phase proteins.
Introduction
Children between the ages of six and 24 months are
Iron deficiency may cause skin, mucosal and
among the most vulnerable to iron deficiency anemia, with
gastrointestinal abnormalities, low weight for age, reduced
the greatest risk being between six and twelve months, when
capacity for work and reduced immune response.1,2 Anemia
complementary feeding has begun.
also compromises physical, motor, psychological,
behavioral, cognitive and language development.3,4
Iron deficiency develops in three stages. Firstly, there is
1. Master’s Degree in Nutrition, Universidade Federal de São Paulo/Escola
a reduction in serum ferritin, which is directly related to iron
Paulista de Medicina (UNIFESP/EPM). PhD student in Nutrition, UNIFESP/
EPM and Assistant Professor, College of Nutrition - Universidade Federal
reserves.5 Secondly, a reduction in serum iron concentration
de Goiás.
and an increase in iron binding capacity. The third stage
2. Professor of Collective Medicine, Universidade de Santo Amaro.
occurs with restriction in the synthesis of hemoglobin,
3. Associate Professor, Department of Pediatrics, UNIFESP/EPM.
Coordinator of the Graduation Course in Nutrition, UNIFESP/EPM.
which may lead to anemia.1,5 In iron deficiency anemia, red
Financially supported by: Convênio PICDT 00046/00-0 CAPES.
cells undergo morphological change from normocytic and
Manuscript received Nov 19 2001. Accepted for publication Oct 04 2002.
normochromic to microcytic and hypochromic.1
321

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322 Jornal de Pediatria - Vol. 78, Nº4, 2002
Anemia in infancy: etiology and prevalence - Hadler MCCM et alii
Electronic cell counting allows analysis of hematimetric
by the Ethics and Research Committees of the Hospital das
indices, which are important in the differential diagnosis of
Clínicas of the Federal University of Goiás and the Hospital
anemia. Low mean corpuscular volume (MCV) together
São Paulo, Federal University of São Paulo.
with anemia favors diagnosis of iron deficiency anemia, as
One hundred and twenty mothers were interviewed, and
MCV obtained electronically is accurate and highly
110 infants included in the study. These infants were non-
reproducible. Mean corpuscular hemoglobin (MCH) is also
twins born at term, between six and twelve months of age
abnormal in iron deficiencies.5
(69 between six and nine months and 41 between nine and
In infants, low hemoglobin together with MCV below
twelve months), not using iron sulfate and attending the
72 fl and/or MCH below 24 pg suggests iron deficiency.6,7
pediatric outpatients ward. Infants with diarrhea were
Inadequate iron intake results in anisocytosis, where the
excluded as reduced plasmatic volume leads to a false
erythrocytes produced are of small average size and large
erythropoiesis, obscuring early signs of anemia.8
size variation. Anisocytosis is measured by red cell
A pilot study was carried out, with socioeconomic and
distribution width (RDW). Iron deficiency anemia thus
hematological data collected between November 1997 and
leads to precocious increase in RDW, allowing early
May 1998, after parents’ informed consent was obtained.
detection of iron deficiency before a large reduction in
Per capita income expressed in US dollars was calculated
MCV occurs.8,9 Ferritin allows a quantitative analysis of
on the basis of the minimum wage (R$120.00 per month)
the body’s iron stores. Ferritin concentration below 10 or 12
and the average month-end exchange rate (US$ 1.0 =
ng/mL is considered indicative of iron depletion at all
R$1.1304) during the collection period.
ages.5,7,10,11
Eight mL of venous blood was collected after fasting to
A number of tests can be used to evaluate iron deficiency:
perform full hemogram, serum iron, ferritin and CRP tests
hemoglobin, hematocrit, ferritin, transferrin saturation,
at the clinical laboratory of the Hospital das Clínicas of the
erythrocyte protoporphyrin, serum iron,11-14 iron binding
Federal University of Goiás.
capacity, MCV, MCH, mean corpuscular hemoglobin
Hemoglobin concentration was determined by electronic
concentration (MCHC), RDW,14 circulating serum
count, using Abbott Cell-Dyn 3000 equipment. MCV,
transferrin receptor and reticulocyte hemoglobin content.15
MCH and RDW were also evaluated. Serum iron was
As many of these tests lack specificity, a number of them are
evaluated using the enzymatic-colorimetric test on Merck
used together in the evaluation of types of anemia and the
Mega equipment. Ferritin was evaluated using the automated
differential diagnosis of microcytosis.14
chemiluminescence assay on Immulite equipment. Serum
Infections and inflammations increase serum ferritin by
CRP was evaluated using the latex agglutination test. CRP
two to four times, reducing its diagnostic value,10 as ferritin
> 6 mg/l indicates infection or inflammation. Anemic infants
is a positive reactant in the acute phase.16,17 It is therefore
with temperature > 37.5º C and CRP > 6 mg/l were excluded
important to exclude infants with these conditions by means
from analysis of iron deficiency etiology, as were those for
of C-reactive protein (CRP), which is one of the acute phase
whom results were not obtained for all parameters.
proteins whose concentration also increases rapidly in case
Children with hemoglobin less than 11 g/dL were
of infections and inflammations, allowing them to be detected
considered anemic, following WHO guidelines (1968).22
before clinical diagnosis.16,18
Besides hemoglobin, iron deficiency etiology in anemic
Venous blood gives greater reproducibility of results
infants was evaluated using the lower normal limits for
and diagnostic security for anemia than does capillary
hematocrit (32%), MCV (72 fl), MCH (24 pg), serum iron
blood.5,7,19,20 Nonetheless, there is little research in Brazil
(50 mg/dL)23 and ferritin (10 ng/mL).7 RDW greater than
using venous blood from term infants to evaluate the etiology
14.5% was taken to indicate iron deficiency, as recommended
of anemia and analyze biochemical and hematological
for children from one to five years.14,24
variables. Sigulem et al. make reference to venipuncture.21
Data were analyzed on Epi-Info 6.0225 and Sigma Stat
This study was carried out in the pediatric outpatients
for Windows 2.0 software, using the following statistical
ward of a public health unit in the city of Goiânia, central
methods: chi-square test, Student’s t test, Mann-Whitney
Brazil, with the aim of establishing the prevalence of
test, Spearman correlation coefficient and analysis of
anemia, iron deficiency anemia and iron deficiency in
sensitivity and specificity. Significance was established at
infants between six and twelve months of age, comparing
5%.
the use of two or more parameters in the diagnosis of iron
deficiency anemia and analyzing and correlating the
biochemical and hematological variables.
Results
Study group characteristics and socioeconomic
conditions
Methods
Among the 110 infants studied, 54 were male, and 56
The study was observational and historical in nature,
female. There was no significant difference in distribution
with cross-sectional epidemiological design. It was approved
by sex in the age groups six to nine months (n = 69) and nine

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Anemia in infancy: etiology and prevalence - Hadler MCCM et alii
Jornal de Pediatria - Vol. 78, Nº4, 2002 323
to twelve months(n = 41) (P = 0.657). There was also no
Table 3 shows significant differences between anemic
significant difference between anemic and non-anemic
and non-anemic groups in terms of hematocrit (P < 0.001),
infants in relation to age group (P = 0.413) or sex (P =
RDW (P = 0.012), serum iron (P < 0.001) and ferritin (P
0.128).
<0.001). Hemoglobin < 11 g/dL is therefore an adequate
Among the anemic infants, 62.7% were from families
cutoff point for diagnosis of anemia.
with per capita income below one minimum wage, that is,
US$ 106.16 per month. There was no significant relationship
Prevalence of iron deficiency anemia and iron
between anemia and per capita family income among infants
deficiency
from six to twelve months (P =0.770). There was also no
Table 4 shows the variations in prevalence of iron
significant difference in proportion of anemic infants among
deficiency anemia according to the criteria adopted. It was
children of mothers above and below median level of
found that when a second parameter was used (MCV, MCH,
schooling (sixth grade) (P =0.926).
ferritin or serum iron) including RDW or not, iron deficiency
prevalence reached 97.8%.
Prevalence of anemia
Using hemoglobin and RDW, anemia prevalence was
Observed prevalence of anemia was 60.9% (Table 1),
89.1%. When hemoglobin and two other parameters were
with 95% confidence of error within 9% absolute. Median,
used (not including RDW), prevalence was 87.0%. When
standard deviation and 95% confidence interval of
RDW was included, prevalence was 97.8%. RDW increased
hematological test results are presented in Table 2.
the sensitivity of iron deficiency detection, as well as
Significant differences were found between anemic and
allowing the differential diagnosis of iron deficiency anemia
non-anemic groups in terms of erythrocytes (P < 0.001),
and thalassemia.
MCV (P < 0.001), MCH (P < 0.001) and MCHC (P
Iron reserve depletion was 20% in 35 infants defined as
<0.001).
non-anemic by ferritin level, and 28% in 32 infants defined
as non-anemic by ferritin level and RDW. Abnormal CRP
was found in 23% and 10% of anemic and non-anemic
infants with normal temperature, respectively.
Table 1 -
Infants of the anemic and non-anemic groups, both
male and female, according to age group, Goiânia,
Correlation between biochemical and hematological
1998
variables
Age group
Anemia
Proportion of
As shown in Table 5, there was no correlation between
Yes
No
Total
anemic infants (%)
erythrocyte numbers and RDW (r = 0.134) or serum iron (r=
0.044). Correlation was found with the other biochemical
6 | 9
40
29
69
58.0
and hematological variables. Hemoglobin showed the best
9 | 12
27
14
41
65.9
correlation with hematocrit (r = 0.946), and MCH showed
Total
67
43
110
60.9
the best correlation with MCV (r = 0.950) and ferritin (r =
χ2
= 0.67 not significant.
0.634).
calc
Table 2 -
Mean (M), standard deviation (SD) and confidence interval (CI) of 95% of the parameters:
hemoglobin (Hb), n. of erythrocytes (n. erythr.), mean corpuscular volume (MCV) and mean
corpuscular hemoglobin (MCH), of the anemic and non-anemic groups
Anemia
Student t
Parameters*
Yes
No
test
M±SD
CI 95%
M±SD
CI 95%
tcalc
P
Hb (g/dL)
10.1±0.59
9.96 || 10.24
11.8±0.69
11.59 || 12.01
13.72*
< 0.001
n. erythr. (M/µl)
4.7±0.38
4.61 || 4.79
5.0±0.38
4.89 || 5.11
3.86*
< 0.001
MCV (fl)
68.9±5.22
67.65 || 70.15
73.7±4.14
72.46 || 74.94
5.11*
< 0.001
MCH (pg)
21.7±2.08
21.21 || 22.19
23.7±1.51
23.25 || 24.15
5.68*
< 0.001
MCHC (g/dL)
31.4±1.15
31.12 || 31.68
32.2±0.86
31.94 || 32.46
4.03*
< 0.001
* These parameters were analyzed in 67 anemic children and 43 non-anemic children.

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324 Jornal de Pediatria - Vol. 78, Nº4, 2002
Anemia in infancy: etiology and prevalence - Hadler MCCM et alii
Table 3 -
The 25th percentile (25thP), median (Mi) and the 75th percentile (75thP) of the parameters:
hematocrit (Hto), Red cell Distribution Width (RDW), serum iron and rods of anemic or non-
anemic infants
Parameters
Anemia*
Mann-Whitney
Yes
No
test
25thP
Mi
75thP
25thP
Mi
75thP
Z
P
calc
Hto (%)
31.1
32.4
33.4
35.0
36.3
38.0
8.50*
< 0.001
RDW (%)
15.3
16.4
17.5
14.4
15.6
16.8
2.52*
0.012
Serum iron (ng/dL)
28.0
35.0
45.0
34.0
53.0
72.0
4.05*
< 0.001
Ferritin† (ng/mL)
3.9
8.2
17.5
11.6
20.0
37.4
3.58*
< 0.001
Rods (%)
1.0
2.0
3.0
1.0
2.0
3.0
0.45
0.652
* These parameters were analyzed in 67 anemic children, and in 43 non-anemic children.
† Excluded the infants with temperature > 37.5°C, and those with CRP > 6 mg/L.
The highest negative correlations with RDW were with
No association was observed in the present study between
ferritin in infants without infection or inflammation, (r =
anemia in infants and per capita family income. In the city
-0.506), ferritin in the group as a whole (r = -0.443), and
of São Paulo, no significant difference was observed between
MCH (r = -0.438). These correlations are, nonetheless,
families with per capita income above and below one
weak.
minimum wage in terms of anemia levels among infants
under 24 months. Among those over 24 months, however,
Discussion
an association between income and anemia was found.21
In infants aged six to twelve months in the city of São
Monteiro et al analyzed the prevalence of anemia in
Paulo, the prevalence of anemia increased from 41.3% in
children between zero and 59 months in the city of São
1973/74 to 53.7% in 1984/85 and 71.8% in 1995/96.21,26,27
Paulo in 1995/96, finding that increased per capita income
In the state of São Paulo, the prevalence of anemia was
and maternal schooling are associated with reduced anemia
55.5% in infants from six to eight months and 62.8% in
and increased MCHC.27 This analysis was not carried out
infants from nine to eleven months. These values are similar
separately for infants under 24 months. Nonetheless, an
to the 60.9% obtained in the present study.28
evaluation of the research carried out in 1984/85 and
No association was observed between anemia and
1995/96 shows an improvement in the socioeconomic
maternal schooling in the present study, confirming the
variables (per capita income and maternal schooling) and a
findings of Sigulem et al.21
concurrent 25% increase in anemia at all economic levels.
Table 4 -
Prevalence of iron deficiency etiology in anemic infants according to the association of
different criteria
Criteria
n†
%
Alteration of Hb + one index between MCV,
or MCH,or ferritin, or serum iron
45
97.8
Alteration of Hb + one index between MCV,
or MCH, or ferritin, or serum iron, or RDW
45
97.8
Alteration of Hb + RDW
41
89.1
Alteration of Hb + two indexes between MCV,
or MCH or ferritin, or serum iron
40
87.0
Alteration of Hb + two indexes between MCV, or MCH,
or ferritin, or serum iron, or RDW
45
97.8
* Infants with temperature <37.5, CRP < 6 mg/L, and presenting results for all parameters (Hb, MCV, MCH, ferritin, serum
iron and RDW) were assessed.
† Number of infants that met the criteria.

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Anemia in infancy: etiology and prevalence - Hadler MCCM et alii
Jornal de Pediatria - Vol. 78, Nº4, 2002 325
Table 5 -
Spearman correlation coefficient (values of r) between hematologic and biochemical variables of infants
Parameters
Hematocrit
n. of
MCH
MCV
Serum
Ferritin
Ferritin¶
RDW
erythrocytes
iron
Hemoglobin
0.946*
0.382*
0.556*
0.512*
0.467*
0.416*
0.474*
-0.313†
Hematocrit
0.519*
0.401*
0.428*
0.405*
0.355*
0.388*
-0.270†
n. of erythrocytes
-0.442*
-0.450*
0.044§
-0.241‡
- 0.154§
0.134§
MCH
0.950*
0.424*
0.634*
0.655*
-0.438*
MCV
0.415*
0.622*
0.612*
-0.415*
Serum iron
0.292†
0.350†
-0.211‡
Ferritin
-0.443*
Ferritin¶
-0.506*
* P < 0.001
† P < 0.01
‡ P < 0.05
§ P > 0.05
¶ Excluded CRP > 6 mg/L and temperature > 37.5°C.
The erythrocyte count normally shows an inverse
Compared to Allen’s study of the 18 to 36 month age
correlation with MCV, which can be confirmed in Table 5
range, the present study found greater correlation between
(r = -0.450).8 This relationship was also found with MCH
hemoglobin and hematocrit (r = 0.946 compared to r =
(r = -0.442) and ferritin (r = -0.241).
0.76), hemoglobin and MCH (r = 0.556 compared to r =
0.42) and MCV and MCH (r = 0.950 compared to r =
Taking hemoglobin less than 11 g/dL as the standard for
0.82).30 While Allen found no correlation in infants of six
diagnosis of anemia in infants, the cutoff point of MCH = 24
to twelve months between MCH and hematocrit (r = 0.05),
pg showed sensitivity of 91%, specificity of 42%, positive
hemoglobin and MCV (r = 0.04) and MCV and hematocrit
predictive value of 71%, negative predictive value of 75%,
(r = 0.05),30 the present study found such correlations
and accuracy of 72%.6 The use of the cutoff point of MCH
(Table 5). However, in infants from 18 to 36 months, there
= 22.2 pg gave greater specificity (84%) and positive
was greater correlation of erythrocyte numbers with
predictive value (83%), but lower sensitivity (52%), negative
hematocrit (r = 0.57), MCH (r = -0.63) and MCV (r = -0.77)
predictive value (53%) and accuracy (64%).
than was found in infants. Of the variables analyzed in this
The data of the present study are confirmed by Oski,14
study, those showing strong correlation were hemoglobin
who stated that RDW seems to be the first hematological
and hematocrit (r = 0.946) and MCV and MCH (r = 0.950).
manifestation of iron, and is more sensitive to screening for
It was also confirmed that iron deficiency is the most
iron deficiency anemia than serum iron or serum ferritin,
common etiology for anemia in infants between six and
while also allowing the differential diagnosis of iron
twelve months, although prevalence levels depend on the
deficiency anemia and thalassemia. Choi and Reid state that
parameters used and thus on the criteria adopted.
normal RDW (RDW < 14.0) indicates normal state in
healthy children.29 However, only 6.0% of healthy infants
researched presented with normal RDW.
Acknowledgements
Considering that the present study found only 52.2% of
We would like to thank Fátima M. Machado Barbosa
infants with reduced hemoglobin, MCV and ferritin, it was
and Euselina M.Q. Pereira for the collection of blood, and
found that ferritin, despite being highly specific for iron
Márcia Maranhão De Conti for the nutritional follow up of
deficiency, is less sensitive in infants. This confirms the
anemic subjects.
affirmation of Wilson et al.,17 and contradicts the hypothesis
that ferritin would be the most sensitive index of iron
deficiency.5,10
Among the infants with anemia and iron deficiency
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E-mail: clarethadler@uol.com.br
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