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3
SEAMEO-TROPMED Regional Center for Community Nutrition, University of Indonesia, Salemba, Jakarta 10430, Indonesia;
*
UNICEF Indonesia, Jakarta 12920, Indonesia; and
Deutsche Gesellschaft fur Technische Zusammenarbeit, Eschborn, Germany
3To whom correspondence should be addressed at UNICEF Headquarters, New York, NY.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • hemoglobin • anemia • iron deficiency • humans • screening
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Most affected are children
and women in the developing world. Considering the magnitude of the
problem and the multitude effects of iron deficiency, assessment of the
iron status of the population is important for every country.
The most commonly used screening methods for the presence of iron
deficiency in a population are the measurements of hemoglobin or
hematocrit concentration for the presence of anemia (WHO
1994
). These measurements are relatively simple and cheap, can
be carried out under field conditions, and values below a certain
cut-off point indicate or define that anemia is likely to exist.
The cut-off value defining anemia has been determined by convention
as the value at -2 SD from the mean or the 2.5th
percentile of the normal distribution of a healthy iron-replete
population. Because iron deficiency is often the most common cause of
anemia, the presence of anemia is also used as a screening tool for
iron deficiency. Although other iron-related tests are required for
the confirmation of iron deficiency, it is reasonable to assume that a
population with a high anemia prevalence is likely to also have a high
prevalence of iron deficiency (Freire 1989
, Yip 1994
).
In view of the close relationship between anemia and iron deficiency
for either individual-based screening or for defining the burden of
iron deficiency on a population basis, it is very important to ensure
the validity of the hemoglobin cut-off point for the detection of
iron deficiency. It is well known that there are a number of
physiologic characteristics such as age (Garn et al.
1981a
, Yip et al. 1984
), sex
(Garn et al. 1981a
) and stage of pregnancy (WHO
1994
) influence hemoglobin concentration; thus, an appropriate
anemia cut-offthat takes into account the normal variations is
indicated. There are some environmental factors that also influence
hemoglobin distribution such as changes in altitude (Miale 1982
) and smoking habits (Nordenberg et al. 1990
, Stonesifer 1978
). Vitamin A deficiency
(Bloem 1995
) and inflammation (Farid et al. 1969
) also influence the hemoglobin concentration. In addition,
several investigators (Garn et al. 1981b
, Jackson et al. 1983
, Johnson-Spear and Yip 1994
,
Perry et al. 1993
, Williams 1981
and
Yip 1996
) found that hemoglobin distribution varies
among races or ethnic backgrounds. The general world-wide
application of the common cut-off for anemia may be questioned. An
analysis of data from the National Health and Nutrition Survey
(NHANES)4
II by Johnson-Spear and Yip (1994)
showed that
individuals of African extraction in the U.S. have hemoglobin
concentrations that are on average 8 g/L lower than those of European
extraction, with the difference not due to iron nutriture. To have a
similar screening performance for iron deficiency in terms of
sensitivity and specificity, the hemoglobin cut-off point for those
of predominantly African extraction is 10 g/L lower than for those of
European extraction. A survey report in Vietnam showed that the healthy
Vietnamese population had mean hemoglobin values 10 g/L lower than the
mean Hb of the Caucasian population, which resulted in a 10 g/L
reduction of cut-off values (Yip 1996
).
The correct interpretation of hemoglobin values requires the application of appropriate cut-offs and knowledge of the influencing factors. Application of a single inappropriate cut-off will result in misclassification and exaggeration or underestimation of the iron-deficiency problem in a community. More information is therefore required on the validity of the use of hemoglobin cut-off values as a screening for iron deficiency because the frequently used WHO cut-off may not be universal.
Iron deficiency is common in Indonesia, and it is important to estimate the problem adequately. It was the aim of the study to examine whether hemoglobin distribution of healthy young Indonesians was similar to that of an American population and whether population-specific hemoglobin cut-off values for detection of iron deficiency were required. This study might serve as model or basis for further studies of this issue.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The ethical committee of the Faculty of Medicine, University of Indonesia approved the conduct of this study.
Blood samples were drawn by venipuncture into two different vacutainers between 0800 and 1300 h. Blood (~10 mL) was drawn into a vacutainer tube with EDTA for determination of hemoglobin (Hb), hematocrit (Ht), mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), mean corpuscular hemoglobin concentration (MCHC), red blood cell count (RBC), white blood cell count (WBC), erythrocyte sedimentation rate (ESR) and zinc protoporphyrin (ZP). The tubes with EDTA-treated blood were stored in a cool box and analyzed within 4 h of collection. Blood (~4 mL) was drawn into a plain vacutainer tube for determination of serum iron (SI), total iron-binding capacity (TIBC) and serum ferritin (SF). Blood was allowed to clot at room temperature (25°C) and was centrifuged at 3000 x g for 15 min. Each serum sample was divided into two tubes and stored at -20°C for mo 1 and then at -80°C for mo 2. Serum ferritin determination was done within 1 mo of blood collection, and SI and TIBC were measured within 1–2 mo.
Hb, Ht, WBC, RBC, MCV, MCH and MCHC were determined using a Coulter
counter (Coulter® AC-T10 Hematology Analyzer; Coulter Electronic,
Miami, FL). ESR was analyzed by the Westergreen method
(Widmann 1983
). Serum ferritin was determined with the
use of a microparticle enzyme immunoassay procedure with a commercial
kit (IMX Ferritin Assay, Abbott, Abbott Park, IL). Serum iron and TIBC
were determined by a colorimetric procedure (Gibson 1990
) using a commercial kit (Hoffman-la Roche, Basel,
Switzerland). All of the above assays were done once. Zinc
protoporphyrin was measured fluorometrically in duplicate in red blood
cells (Hematofluorometer model 206D, AVIV Biomedical, Lakewood, NJ),
which were obtained by centrifuging the EDTA-treated blood samples
(Hastka et al. 1992
). The Coulter counter and SI/TIBC
results were analyzed at the Clinical Pathology Department, Cipto
Mangunkusumo Hospital, Faculty of Medicine, University of Indonesia;
the other measurements were done at the SEAMEO-TROPMED Center.
Choice of cutoff points for abnormal values of iron status indicators and ESR.
Three tests were used to assess the iron status of the subjects. The
respective criteria for each test,indicating low iron status, were as
follows: serum ferritin < 12 µg/L
(Dallman et al. 1996
), transferrin saturation < 16% (Dallman et al. 1996
) and zinc protoporphyrin
> 40 µmol/mol heme (Hastka et al. 1992
). A subject was considered to be iron deficient when at
least two of the three test values were beyond the cut-off value,
indicating deficiency (Dallman et al. 1996
). For
hemoglobin, the cut-off criterion indicating anemia was the WHO
cut-off of 120 g/L for females and 130 g/L for males (WHO
1994
). Hematocrit was considered to be abnormal at values
< 0.36 for females and < 0.41 for males (Gibson 1993
). RBC for females was considered normal in the range of
4200–5800/mm3 and for males, 3600–5600/mm3
(Gibson 1993
). The cut-off values for the red blood
cell indices were as follows: MCV < 80 fL, MCH < 27 pg and
MCHC < 320 g/L (Gibson 1993
). For serum iron (SI)
and total iron-binding capacity (TIBC) the cut-off points were
60 µg/dL (10.74 µmol/L) and 410
µg/dL (73.39 µmol/L), respectively
(Cook and Finch 1979
).
ESR and WBC were used as indicators of the presence of a possible
infection because the NHANES II survey, in which percentile values were
used for comparison, also used ESR and WBC as indicators of
inflammation (Expert Scientific Working Group 1985
). ESR was considered
to be abnormal at >15 mm/h for males and >20 mm/h for females
(Widmann 1983
), whereas WBC values
<3400/mm3 or >11500/mm3 were judged to be
abnormal (Expert Scientific Working Group 1985
). To conserve sample
size, the hemoglobin concentration of smokers was adjusted downward
according to the number of cigarettes smoked per day (Centers for Disease Control 1989
).
Statistical analysis.
ANOVA and the Kruskall-Wallis test were used to detect differences
in the characteristics of men and women (Snedecor and Cochran 1980
). Comparison of percentiles values and analysis of means
and confidence intervals were used to compare the distribution of the
present data set with that from the NHANES II and III surveys
(Dallman et al. 1996
, Gibson 1993
). For
the hematological and biochemical indices, normality was tested by the
one-sample Kolmogorov Smirnov test. WBC, ESR, RBC, MCV, MCH, MCHC,
serum ferritin and zinc protoporphyrin were not normally distributed;
thus medians were used as the measure of central tendency. Because Hb,
Ht, SI, TIBC and transferrin saturation were normally distributed,
means were used as the measure of central tendency.
The performance (sensitivity and specificity) of different cut-off criteria for anemia as a screening tool for iron deficiency was estimated in female subjects. Sensitivity was defined as the proportion of cases of iron deficiency correctly identified by Hb as anemic and specificity as the proportion of cases of iron adequacy correctly identified by Hb as nonanemic.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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. The subjects ranged in age from 18 to 27 y with a mean age of
21.6 y for men and 22.0 y for women (Table 1)
. Fifteen
percent of the men and 18.6% of the women had a body mass index
< 18.5 kg/m2. Ethnicity of the subjects was
defined by the origin of their parents, the majority of whom came from
the island of Java. A small percentage of the sample (7.9% males and
12.7% females) had parents originating from parts of Indonesia other
than Java and Sumatra. This study therefore refers mainly to the
western part of Indonesia. There was no significant difference in mean
Hb concentration among the different ethnic groups. Considering the
educational level of the father and household possession of selected
commodities, all subjects belonged to the middle or high socioeconomic
class (Table 1)
.
|
). The prevalence of high zinc protoporphyrin values (>40
µmol/mol heme) was higher than the prevalence of low seum
ferritin or low transferrin saturation. When 50 µmol/mol
heme was used as a cut-off point, the prevalence of high values
among women became 28.8% in stead of 51.8%. Hemoglobin concentrations
and values of iron status indicators did not always correlate
(Table 3
). Among anemic women, 40% were iron deficient, whereas 16.7%
of the nonanemic women were iron deficient (using 40
µmol/mol heme zinc protoporphyrin as a cut-off point).
|
|
). Of the noniron-deficient subjects, 3.1% of men and 9.9%
of women had a hemoglobin concentration <130 and 120 g/L,
respectively. The hemoglobin distribution of the Indonesian subjects
was compared with the distribution of the nonblack population from the
United States (Table 4
). The mean hemoglobin concentration of American men and women was
within the 95% confidence intervals for the mean of the respective
concentration of the Indonesian subjects. The mean value for the
American women was just below the upper border of the confidence
interval for the Indonesian mean. The percentiles of the hemoglobin
distribution were also compared. The percentile values for men were
largely similar in the Indonesians and Americans. The percentile values
of the Indonesian women were 3–8 g/L lower than the values of American
women. Using the mean hemoglobin concentration -2 SD as a
definition for anemia in the Indonesian subjects, the cut-off point
below which a person would be considered anemic was 113 g/L for women
and 130 g/L for men. The cut-off point for men was similar to that
defined by WHO, whereas the cut-off point for the women was lower
than the WHO cut-off point of 120 g/L.
|
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). The calculated cut-off point for the Indonesian women of 113 g/L
had lower sensitivity but a slightly higher specificity for detecting
iron deficiency than the WHO cut-off point for women of 120 g/L.
The sensitivity and specificty when 120 g/L was used to detect iron
deficiency were lower in the Indonesian subjects compared with the
American subjects. From the relatively low sensitivity (<50%), it
becomes clear that anemia is not related only to iron deficiency as
defined in this study. Among the anemic women, only 40.0% were iron
deficient, whereas in the nonanemic subjects, 15.4% were iron
deficient. Six men had anemia without iron deficiency.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). On the
basis of the WHO cut-offs points, in this study, the prevalence of
anemia was 15.9% for women, whereas only 3.9% of the men were anemic.
For men, the observed prevalence was near the expected level of
2.5–5% for an iron-replete population, based on the definition of
WHO anemia criteria. This was confirmed by the other iron biochemistry
tests. The lower prevalence of anemia for the women studied compared
with the overall prevalence in Indonesia is not surprising considering
the fact that subjects were university students and most of them came
from a relatively high socioeconomic background. It was also to be
expected that women would have a higher deficiency prevalence than men
for all iron-related tests. This can probably be attributed to the
50% higher iron requirement of women than men due to monthly menstrual
blood losses (Cheong et al. 1991
, Hallberg et al. 1995
) and a lower energy and iron intake from food. This study
also confirms a common finding that, in many parts of the world, even
when substantial anemia and iron deficiency are prevalent among women,
men do not suffer from iron deficiency because of their lower iron
requirement. This male and female differential in iron deficiency
indicates that dietary iron intake is the main factor responsible for
the anemia observed among women (Yip, 1994
).
Among the anemic women, 40.0% were iron deficient on the basis of a
strict criterion of having abnormal results for two or more of the
three tests (serum ferritin, zinc protoporphyryn and transferrin
saturation). It is very likely that there were some women who had
milder forms of iron deficiency but whose values did not meet the study
definition. This finding of the positive predictive value of anemia for
detecting iron deficiency (~40%) is similar to the previously
reported value for American women (Johnson-Spear and Yip 1994
). The relatively low positive predictive value of anemia
for detecting iron deficiency suggests that anemia is not a perfect
screening tool for iron deficiency, especially when the anemia is mild.
The remaining 60% includes subjects with mild iron deficiency or other
conditions that did not meet the study criteria such as mild hereditary
anemia, normal variations and mild infections not excluded on the basis
of the ESR criteria, or vitamin A and folate deficiency. Furthermore,
in a perfectly healthy population, 2.5–5% of the people would be
anemic by definition.
The mean hemoglobin concentration of American men was within the 95% confidence interval of the mean hemoglobin for Indonesian men, indicating similarities in mean values. The comparison of percentile values also suggested that there is no difference in mean hemoglobin concentrations of healthy Indonesian and American men. Among women, the mean hemoglobin concentration of the Americans was exactly at the higher border of the 95% confidence interval of the Indonesian population. The percentile values of the Indonesian population were lower than those of the American population, suggesting that there is difference between the two groups.
Because there was substantial iron deficiency among the women studied, it is not certain whether the recommended criterion for iron deficiency fully excluded most of those with some degree of iron deficiency. Therefore, the postexclusion hemoglobin distribution may not be a truly iron-replete sample. For this reason, it would be more accurate to use the male subsample of the study to contrast with the iron-replete sample from the United States. In doing so, we found the two distributions nearly identical. This finding strongly suggests that it would be appropriate to use the common anemia criterion recommended for those of European extraction for Indonesians also.
For the purpose of identifying the proportion of individuals at risk of
iron deficiency for possible intervention, a higher cut-off value
with greater sensitivity is generally desirable (Himes et al. 1997
). Using different hemoglobin cut-off points for the
assessment of iron deficiency showed that, compared with the WHO
cut-off points (120 g/L), the population-specific anemia
criterion of 113 g/L for Indonesian women, the mean -2 SD,
had a very low sensitivity for detecting iron deficiency. Only when the
cut-off approached that of the WHO criterion did the test
performance become similar to that for American women, which is based
on the NHANES II survey (Johnson-Spear and Yip, 1994
).
Because the prevalence of high zinc protoporphyrin was not similar to
the prevalence values of the other iron status indicators, we also
considered using 50 µmol/mol heme as a cut-off point
instead of 40 µmol/mol heme. This higher cut-off point
resulted in a lower estimated percentage of iron-deficient women.
However, when this elevated cut-off was also used for zinc
protoporphyrin, the sensitivity using 120 g/L as a borderline value for
hemoglobin concentration to detect iron deficiency was higher (40.6%)
than when using 116 g/L (31.3%) or 113 g/L (15.6%). For the
Indonesian population studied, the application of the WHO anemia
criterion will yield results for defining the extent of
iron-deficiency problems comparable to those in populations of
mainly European extraction.
This finding is similar to that of Charoenlarp and Polpothi (1987)
in Thailand. They investigated the distribution of
hemoglobin concentration in healthy Thai children and found that, after
excluding those having abnormal hemoglobin types, the hemoglobin
distribution was the same as that of the U.S. population.
This result suggests that there is no need to define separate cut-off criteria for anemia in the Indonesian population studied, most of whom originated from the western part of Indonesia.
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FOOTNOTES |
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2 Current address: UNICEF China, Beijing 100600,
China.
4 Abbreviations used: ESR, erythrocyte
sedimentation rate; Hb, hemoglobin; Ht, hematocrit; MCH, mean
corpuscular hemoglobin; MCHC, mean corpuscular hemoglobin
concentration; MCV, mean corpuscular volume; NHANES, National Health
and Nutrition Survey; RBC, red blood cell count; SF, serum ferritin;
SI, serum iron; TIBC, total iron-binding capacity; WBC, white blood
cell count; ZP, zinc protoporphyrin.
Manuscript received October 26, 1998. Initial review completed December 1, 1998. Revision accepted April 27, 1999.
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