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Department of Nutrition and Food Science, University of Maryland, College Park, MD 20742 * Nutrition Unit, Ministry of Health, Shaab, Kuwait
2To whom correspondence should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONPrevious studies in Kuwait.Background on Kuwait.SUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • anemia • iron deficiency • Kuwait • adolescent girls • hemoglobinopathies
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONPrevious studies in Kuwait.Background on Kuwait.SUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, DeMaeyer and Adiels-Tegman 1985
). Iron (Fe) deficiency is responsible for most anemia.
Deficiencies of other nutrients (including folic acid, protein, vitamin
B-12, vitamin A and copper) may also contribute (Viteri 1998
). Other causes include thalassemia, hemoglobin
(Hb)3
variants, as well as infection and inflammation. However, the
contribution that Hb variants make to anemia is rarely examined.
Worldwide, the prevalence of anemia in adolescents is largely unknown.
Few studies have been performed in the Arabian Gulf, and none in
Kuwait. |
Previous studies in Kuwait. |
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TOPABSTRACTINTRODUCTIONPrevious studies in Kuwait.Background on Kuwait.SUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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conducted a nationally representative study of 1582
pregnant women between the ages of 14 and 45 y living in Kuwait
and found that anemia was present in 36.8%. Al-Awadi et al. (1995)
studied 980 Kuwaiti women between the ages of 14 and
45 y. Their results indicated that 23.2% were anemic (Hb < 120 g/L). Eid et al. (1986)
examined 1208 children
between the ages of 6 and 17 y. Of the 593 males studied, 12.8%
were anemic; however, 26% of the 615 females were anemic. None of these studies focused on adolescents or examined etiological factors responsible for the low Hb concentrations. Consequently, we do not know the cause of the anemia in this population. Public health measures, instituted by the Kuwaiti government, coupled with a constellation of environmental factors (including extremely high ambient temperatures, aridity, paucity of vegetation and standing bodies of water) have eliminated the most common parasites as significant contributors to anemia.
The objectives of this study were to ascertain the prevalence of anemia in healthy adolescent girls attending secondary schools and to explore Fe deficiency and Hb variations as contributors to the anemia. We also wanted to identify regional variation in anemia prevalence in Kuwait.
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Background on Kuwait. |
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TOPABSTRACTINTRODUCTIONPrevious studies in Kuwait.Background on Kuwait.SUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Kuwait is divided into 5 administrative divisions, called governorates; all of its citizens enjoy a high standard of living that includes free education and medical care, among other amenities. The discovery of oil in the 1950s brought dramatic changes in living standards, including changes in lifestyle, diet and the transformation of the physical environment. The 1997 per capita income was ~$22,300, making it one of the wealthiest countries in the Gulf area and the world. The infant mortality rate is 10.7 and the life expectancy at birth is 76.8 y.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONPrevious studies in Kuwait.Background on Kuwait.SUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). The study protocol was reviewed and approved by the Kuwait Ministries of Health and Education, and was conducted after obtaining written consent from the parents of the school children.
Information was collected by interview onto structured questionnaires, pretested in a small group of subjects similar in characteristics to those in the study. A variety of social, economic, health and medical data were collected. Information on infections and illnesses diagnosed by a medical doctor within the preceding month, supplement usage and menstrual history was also obtained.
Blood collection and analyses.
Capillary blood was collected from the finger. Hb was assessed by the HemoCue method. HemoCue calibration was checked on a daily basis by using the control cuvette supplied with the photometer. Fe-deficient erythropoiesis was assessed by measurement of erythrocyte protoporphyrin (EP) using the zinc protoporphorin (ZPP) hematofluorometer (AVIV Biomedical, Lakewood, NJ).
Additional blood was obtained in capillary tubes from the first 228
unrelated girls who entered the study to determine Hb variation.
Hemolysates were prepared and Hb variant quantitation was carried out
with cation-exchange HPLC (Waters LC Module 1, Milford, MA) to
check for clinically important Hb variants (Bisse and Wieland 1988
).
The WHO definitions of anemia (Hb < 120 g/L) and severe anemia
(Hb < 70 g/L) were used (WHO 1996
). Normal EP
concentrations were <5 µg/g Hb, a level suggested by
AVIV Biomedical, the manufacturer of the ZPP hematofluorometer.
Standards (high, medium and low) for EP were obtained from the
manufacturer (AVIV Biomedical) and tested daily with the samples. There
are only four known causes of elevated ZPP levels, i.e., elevated Pb
burdens, a rare genetic disorder called erythropoietic protoporphyria,
Fe deficiency and chronic inflammatory diseases (Lamola et al. 1975
). EP is not elevated in thalassemia minor (Stockman et al. 1975
).
Statistical analysis.
Means were tested using Student’s t test and/or by ANOVA, e.g., average Hb concentration among the five Kuwait governorates. Correlations between variables such as mean duration of menses in days and Hb concentration, and EP value and Hb concentrations, were examined using the Pearson Product Moment Correlation test. EPIINFO was used to calculate odds ratio (OR), and a 95% confidence interval (CI) for the OR and for sample size calculations. Hb was regressed on EP using simple linear regression. Hb E and S phenotypic and gene frequencies were calculated using the trinomial expansion equation, p + q + r = 1, where p = gene frequency of Hb ß A, q = the gene frequency of Hb ß S, and r = gene frequency of Hb ß E, based on the Hardy-Weinberg Equilibrium. ß-Thalassemia gene frequency was estimated from the phenotypic prevalence of the trait. Gene frequencies of hereditary persistence of fetal hemoglobin were not calculated.
Statistical significance was accepted when P-values were
< 0.05. The analysis was conducted on a personal computer using
the Statistical Analysis System (SAS 1990
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONPrevious studies in Kuwait.Background on Kuwait.SUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The mean Hb concentration for the sample was 127 ± 16.5 g/L with a range from 57 to 174 g/L. Thirty percent had Hb < 120 g/L. Three subjects (0.3%) had Hb < 70 g/L. Of these three, two were from Farwania and one was from Ahmadi. All three subjects were 16 y old, had started menstruating at 13 y, reported a normal blood flow and did not use supplements. The EP values of these three girls ranged from 18.7 to 23.1 µg/g. None of the three subjects had an abnormal Hb variant.
Erythrocyte protoporphyrin (EP) values.
The mean and median EP values were 5.9 ± 2.3 and 5.5 µg/g Hb, respectively. Thirty two percent of all subjects had a normal EP level (i.e., below the manufacturers suggested normal of < 5 µg/g Hb).
We compared the Hb concentrations of the girls in three EP ranges.
Group 1 contained girls with EP < 5.0 µg/g, i.e.,
below the 25th percentile, (normal by AVIV standard). Group 2,
including the second and third quartiles (~50% of the sample), had
EP levels between 5.0 and 6.5 µg/g Hb. Group 3 contained
the remaining quartile with EP > 6.5 µg/g Hb. The
mean Hb concentrations for these three groups are shown in Table 1
. The differences in Hb concentration between Groups 1 and 3 and between
Groups 2 and 3 were significant. The overall correlation between the EP
and Hb values was r = -0.459, (P
= 0.0001, n = 1048).
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5.0 µg/g Hb) in all but 37.1%
of those with Hb concentrations 120 g/L (in the normal range).
However, EP was elevated in 81.1% of those with Hb concentrations
< 120 g/L. Seventy-five percent of the sample had EP 
6.5 µg/g Hb. Only 4.75% of this sample had EP levels >10
µg/g Hb. The percentage with elevated EP values varied by
governorate and was significantly lower in Ahmadi than in the other
regions (Table 2
).
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Most cases of anemia worldwide are due to Fe deficiency. Initially, Fe stores are depleted. This is followed by impaired Fe status, and finally the deficiency progresses to Fe deficiency anemia. A low Hb concentration is likely to be the result of Fe deficiency. However, Hb is not a sensitive indicator of Fe deficiency because reduced Hb occurs only in the later stages of iron depletion, and a low Hb concentration may be due to other causes.
Because EP was the only indicator of body Fe status measured, and an EP
of 5.0 µg/g was used as the cutoff to determine the
presence or absence of Fe deficiency, we examined the suitability of
this cut-off value in different ways. First, we compared the Hb
distribution of subjects having EP < 5.0 µg/g Hb
with those who had EP 5.0 µg/g Hb. Anemia (Hb
< 12.0 g/L) was present in only 18.2% of those with EP < 5
µg/g Hb. However, anemia was present in 34.9% of those
with EP 5.0 µg/g Hb. The mean Hb concentration of
the subjects with EP < 5.0 µg/g Hb was 132 g/L
(reference group) compared with 125 g/L for those with EP values
5.0 µg/g Hb. We also examined the ZPP
hematoflurometer cut-off point recommended by the manufacturer
using OR. The odds of being Fe deficient (given EP 5.0
µg/g Hb) was 2.44 times higher (95%, CI: 1.75, 3.39) in
anemic girls than in nonanemic girls. Figure 1
shows the scatter plot of EP and Hb values and the regression of Hb on
EP. The model was significant (P < 0.0001) and the
regression coefficient, b = -0.309, was significantly
different from zero.
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Table 2
provides the breakdown of Fe and anemia status by governorate
and shows that less than a third (26.2%) of the sample had
simultaneously normal Hb ( 120 g/L) and EP (<5.0 µg/g Hb).
Forty-four percent of the total sample had elevated EP values,
possibly due to Fe deficiency, but had normal Hb concentrations. Over
half of the girls with elevated EP values resided in two governorates,
Hawalli and Farwania. Nearly one quarter (23.9%) of the sample had
elevated EP values and low Hb concentrations, most likely due to Fe
deficiency anemia. Six percent of the girls were anemic, but had EP
values in the normal range. Over half of the latter were from Ahmadi,
and their anemia may be due to reasons other than Fe deficiency.
Hemoglobinopathies and anemia.
A number of Hb variants prevalent in this part of the world are
associated with anemia. In our study, screening for hemoglobinopathies
was conducted on the first 228 nonrelated subjects. Clinically
important Hb variants were present in nine of the 228 individuals; of
these, only three had Hb < 120 g/L. One had ß-thalassemia trait
and two had sickle cell trait (Table 3
).
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Ninety percent of the girls did not use hematinic supplements. Among those who did use supplements, roughly half used Fe tablets. The mean Hb values for supplement users (127 g/L) and nonusers (126 g/L) were not different (P > 0.05). Mean EP values of users and nonusers also were not different.
There were no significant differences between either the Hb or EP values of those who had been diagnosed as having a cold or flu by a physician within the last month (n = 270) and those who had not been "sick" (n = 780).
Ninety-two percent of the sample characterized their monthly menstrual blood losses as "normal," whereas 8.3% described them as "heavy." Neither the Hb (nor the EP) concentrations of those with "normal" (127 g/L) and "heavy" (125 g/L) blood flow were different (P > 0.05).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONPrevious studies in Kuwait.Background on Kuwait.SUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The mean Hb concentration of the entire sample was 127 g/L. After excluding those with EP < 5.0 µg/g, the mean Hb was 132 g/L. Thirty percent of the girls were anemic by WHO criteria. Severe anemia was present in only three girls (0.3%).
EP level is a measure of Fe-deficient erythropoiesis, the second stage of Fe deficiency. During the second stage of Fe deletion, the Hb concentration remains normal, but falls below normal levels during the third stage, known as Fe deficiency anemia. Overall, 68% of adolescents had elevated EP values, but very few had severely elevated levels. Only 25% of the girls had EP > 6.5 µg/g Hb; <5% had EP > 10 µg/g Hb. Of anemic adolescents, 81% had elevated EP levels.
One explanation for the mildly elevated EP values would be high blood
Pb concentrations or chronic infection. However, a substantial majority
of the schoolgirls reported being healthy and without infection or
other illness. Furthermore, the Hb and EP concentrations of those who
reported sickness and those who were not sick were not different.
Previous studies investigated Pb concentrations in the tissues (blood
and teeth) of Kuwaitis, but did not find them to be a public health
problem (Bu-Olayan and Thomas 1999
, Shaltout et al. 1989
). In our study, < 5% of adolescents had EP > 10 µg/g Hb, a figure once used as a diagnostic cutoff for
high blood Pb concentrations.
Nine girls (3.9%) had a Hb variant. However, of those, only three were
anemic. The high prevalence of elevated EP values in this sample is
more consistent with Fe deficiency than ß-thalassemia because EP
values have not been shown to be elevated in the latter
(Poh-Fitzpatrick and Lamola 1976
, Stockman et al. 1975
). The methodology used in this study could not identify
the 
-thalassemia trait, but it is clear that anemia in this sample
was not due to -thalassemia. -Thalassemia is relatively mild in
Kuwait and is thus unlikely to cause significant decrements in Hb or
other hematologic values.
The earliest report of hemoglobinopathies among Kuwaitis dates to 1969
(Ali 1969
) in a study of Hb H. The following year,
Ali (1970)
reported on the mildness of sickle cell
disease (SCD) in Kuwait and suggested that this was associated with an
unusually high level of fetal Hb. Subsequent clinical studies
(Al-Salem and Ismail 1990
) confirmed the milder course
and infrequent pathology of SCD among Kuwaiti children. A similarly
benign sickle cell anemia was also found in the eastern provinces of
Saudi Arabia (El-Hazmi and Warsy 1993
), the
geographic origin of several important Kuwaiti lineages
(Ministry of Information 1990
).
No field studies have been done to determine the frequencies of
hemoglobinopathies in Kuwait. However, several studies of hospitalized
populations offer insight into the course of the disease and its
prevalence in clinical settings. In Farwania Hospital,
hemoglobinopathies were encountered in 20% of a subsample of 1289
confined individuals (Ghosh et al. 1993
). Nearly all of
the common hemoglobinopathies were encountered, but -thalassemia was
surmised to be the most common hemoglobinopathy in Kuwait, as it is in
eastern Arabia in general (Pembrey et al. 1980
).
Adekile and Haider (1996) used polymerase chain reaction
to amplify and sequence -thalassemia and ß S haplotypes among a
group of hospitalized Kuwaitis. They found considerable homogeneity in
-thalassemia molecular variants and ß S haplotypes but
considerable heterogeneity in ß-thalassemia alleles. Adekile and Haider (1996)
reported that the high frequencies of ß S
haplotype 31 (Saudi Arabia/India variant) and -thalassemia in Kuwait
contribute to the mild nature of the SCD among Kuwaiti Arabs. A 30-y
study of 129 Kuwaiti children hospitalized with ß-thalassemia major
indicated that consanguinity may account in large part for the
frequency of this hemoglobinopathy in Kuwait (Al-Fuzae et al.
1998
).
The ß-thalassemias are heterogeneous with respect to molecular
pathogenesis (El-Hazmi et al. 1995a
). Among
Arabs, the predominate mutations differ by ethnic group
(El-Hazmi and Warsy 1996
, El-Hazmi et al. 1995b
). Only one individual had the ß-thalassemia
trait in this study. Our results (Table 3)
, as one would expect, showed
a lower frequency of these variants than previous studies in which
hospitalized patients were studied. Thus, we conclude that
hemoglobinopathies were not significant contributors to anemia or to
elevated EP values in this sample.
Kamal and Martinez (1984)
conducted a study of
500 adult males and females to describe food preparation methods,
dietary habits and nutrient intakes of Kuwaitis. They found that
cereals (wheat and rice) were important staples in the diet. Most
(81%) of those studied consumed bread once or more daily. Ninety
percent of the sample drank tea; 24% of the women drank three or more
cups (710 mL) of tea per day. That study also found that for
women, the intakes of vitamin A, Fe, Ca and Zn were below the U.S.
recommended daily allowance (RDA) and that the food preparation methods
employed involved prolonged boiling of meat and vegetable dishes. They
surmised that prolonged boiling of vegetables may decrease the vitamin
content (especially, folic acid) of foods consumed. In a more recent
diet study of 203 female college students using 3-d diet record
analyses, Al-Shawi (1992)
found that the intakes of Fe,
Zn, folacin and vitamin D were below the RDA. The diets of these women
were also high in caffeine.
Despite one of the highest per capita incomes in the world, anemia and
probably Fe deficiency remain important public health problems in
Kuwait. The 30% of adolescent Kuwaiti schoolgirls who were anemic by
WHO epidemiologic criteria for the classification of countries
(WHO 1996
) by anemia prevalence, places Kuwait in the
moderate prevalence category (10–39.9%). Twenty-four percent of
the girls had Hb and EP values suggestive of Fe deficiency anemia.
Hemoglobinopathies associated with anemia exist but at very low
frequencies in this sample. On the other hand, anemia is unexpectedly
high and exceeds levels that can be accounted for by the frequency of
hemoglobinopathies or blood Pb. Thus, Fe deficiency is strongly
suspected, given the large percentage of subjects with slightly
elevated EP values and the significant differences between the mean Hb
concentrations of those with normal (132 g/L) and high (125 g/L) EP
values. Although we surmise that much of the anemia is due to Fe
deficiency, other factors (such as deficiencies of folic acid) likely
also contribute to the anemia of these subjects. Caution should be used
in interpreting the EP results because no single test can identify
impaired Fe status unequivocally (Expert Scientific Working Group 1985
), and other causes of nutritional anemia were not investigated.
Further studies using several Fe status indicators to elucidate the
causes of anemia and Fe deficiency in particular are warranted.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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3 Abbreviations used: CI, confidence interval; EP,
erythrocyte protoporphyrin; Hb, hemoglobin; OR, odds ratio; RDA,
recommended daily allowance; SCD, sickle cell disease; ZPP, zinc
protoporphyrin.
Manuscript received April 9, 1999. Initial review completed May 8, 1999. Revision accepted January 19, 2000.
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TOPABSTRACTINTRODUCTIONPrevious studies in Kuwait.Background on Kuwait.SUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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