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Gazz Med Ital - Arch Sci Med-3099 - Proof in PDF - V1 - 2014-10-30
Gazz Med Ital - Arch Sci Med-3099 - Proof in PDF - V1 - 2014-10-30
Gazz Med Ital - Arch Sci Med-3099 - Proof in PDF - V1 - 2014-10-30
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GAZZ MED ITAL - ARCH SCI MED 2014;173:1-2
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Aim. Aim of the study was to measure the Laboratory Medicine Department
prevalence and types of thyroid disorders us- Faculty of Applied Medical Sciences
ing the American Thyroid Association guide- Umm Al‑Qura University
lines and to investigate their relationship Al Abdeyah, Makkah, KSA
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with anemia frequency in primigravida fe-
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males during the first trimester.
Methods. Blood samples were collected from
500 primigravida females with no history
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of thyroid disease, chronic diseases and/
T hyroid dysfunction is a worldwide phe-
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or anaemia to measure serum TSH, free T4, nomenon in women and the preva-
erythrocyte indices and iron parameters.
lence increases during pregnancy.1, 2 Mater-
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tin and total iron binding capacity (P<0.05). rum free thyroxin (FT4) and normal thyroid
Conclusion. Thyroid disorders are common stimulating hormone (TSH) levels.3
in primigravida Saudi females during the Thyroid dysfunctions have also been
first trimester and they are associated with
an increase in the frequency of anaemia. associated with the development of anae-
Further studies are needed to identify the mia 4-9 and it has been found that all haema-
mechanism(s) by which thyroid dysfunction tological parameters return to normal when
induces anaemia during pregnancy. a euthyroid state is achieved.10-14 Anaemia
Key words: Thyroid - Anemia - Pregnancy. is another major health problem affecting
women during pregnancy and the World
Corresponding author: B. Refaat, Department of Labora- Health Organization has estimated that 58%
tory Medicine, Faculty of Applied Medical Sciences, Umm
Al-Qura University, Makkah, PO Box 7607, KSA. of pregnant women are anaemic in devel-
E-mail: bassem.refaat@yahoo.co.uk oping countries.15 Anaemia during early
Vol. 173 - No. 1 GAZZETTA MEDICA ITALIANA - ARCHIVIO PER LE SCIENZE MEDICHE 1
REFAAT Thyroid disorders and anaemia in pregnancy
pregnancy is also associated with preterm tween 4 and 12 weeks) according to the in-
deliveries, low birth weight and perinatal clusion and exclusion criteria (Table I) dur-
mortality.15 ing their initial visit to the antenatal clinic in
Little is known about the prevalence of the University Health Care Centre. Half of
thyroid disorders and the characteristics of the blood sample (2.5 mL) was collected on
associated anaemia during pregnancy in EDTA and the rest was on plain tube.
Saudi Arabia. This trial is a cross-sectional study to
Therefore, the aim of the current study measure the prevalence of thyroid disorders
was to measure the prevalence of thyroid and the characteristics of their associated
disorders according to the new guidelines anaemia during pregnancy in Saudi females.
set by the American thyroid Association for Following the identification of thyroid dys-
the diagnosis and management of thyroid function, the participants were divided into
disease during pregnancy 16 and to study 2 groups according to their thyroid profile
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their relationship with types and frequency results. Females with normal thyroid profile
of anaemia, erythrocyte indices and iron served as “control group” and their haema-
parameters in primigravida females during tological results and iron parameters were
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the first trimester. O compared with those obtained from the
“thyroid disorder” group.
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Materials and methods Measurements of thyroid hormones
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Whole blood samples (2.5 mL) were col-
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Ethical approval
lected through venepuncture, centrifuged at
Ethical approval was obtained from Umm
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3000 rpm for 20 minutes, and then the ob-
Al-Qura Institution Review Ethics Commit- tained serum samples were frozen at -20 °C
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tee before starting the study and all blood for storage till used. The quantitative meas-
samples were collected following obtaining urement of thyroid stimulating hormone
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informed written consent from all the par- (TSH) and free thyroxin hormone (FT4) was
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Five millilitres of blood samples were col- The normal range according to the manu-
lected from 500 primigravida women (age facturer for TSH and free T4 was 0.27-4.20
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range between 22 and 34 years) during the µIU/mL and 12-22 pmol/L, respectively. The
first trimester (gestational age range be- detection sensitivity was 0.005 µIU/mL for
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TSH and 0.3 pmol/L for FT4. The intra- and defined by the manufacturer, sensitivity was
interassay coefficients of variations for FT4 16.8 µg/dL and the intra- and interassay was
were 1.7 and 3.9% and for TSH were 1.4% 1.6% and 2.4%, respectively. The normal
and 3.4%, respectively. range for the ferritin kit was 7-283 ng/mL,
The classification of thyroid dysfunctions sensitivity was 0.5 ng/mL and the intra- and
were based on the guidelines of the Ameri- interassay was 5.5% and 7.1%, respectively.
can thyroid Association for the diagnosis
and management of thyroid disease during Statistical analysis
pregnancy.16 The normal range for FT4 dur-
ing pregnancy (10.5 to 22.3 pmol/L) was Statistical analysis of the results was
adapted from the currently available report performed using SPSS version 16. Cross-
that included normal pregnant participants tabulation followed by Chi square (X2) test
from the Gulf Region.17 Hypothyroidism were used for frequency analysis. Normal-
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was considered when TSH >2.5 µIU/mL and ity and homogeneity of data were assessed
the level of FT4 defined the type as either with the Kolmogorov and Smirnoff test and
primary (FT4 <10.5 pmol/L) or subclinical Levene test, respectively. Student’s t test or
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(FT4 ≥10.5 pmol/L). Hyperthyroidism was
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considered for TSH ≤0.03 µIU/mL and/or tween 2 groups, based on normality. One
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FT4 >22.3 pmol/L. Hypothyroxinaemia was way ANOVA followed by LSD post hoc test
define by the presence of low FT4 (≤10.5 were used to compare between more than
pmol/L) with normal serum TSH levels 2 groups. Correlations were determined us-
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(<2.5 µIU/mL). ing Pearson’s test. P value < 0.05 was con-
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sidered significant.
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Determination of hematological profile
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Whole blood samples (2.5 mL) collected Results
on EDTA were processed on Sysmex XS 500
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with 5-parameter differential (Sysmex, IL, Prevalence and types of thyroid disorders
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(MCV) and mean corpuscular haemoglobin mia were detected in 162 (32.4%) and
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(MCH). Anaemia was defined by haemo- 118 (23.6%) out of 500 pregnant females,
globin level <11 g/dL, microcytosis by MCV respectively. Anaemia was detected in 52
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<80 fL, macrocytosis by MCV >98 fL, and out of 338 participants with normal thyroid
hypochromic by MCH <25 pg.18 profile (15.3%) and in 66 out 162 females
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Vol. 173 - No. 1 GAZZETTA MEDICA ITALIANA - ARCHIVIO PER LE SCIENZE MEDICHE 3
REFAAT Thyroid disorders and anaemia in pregnancy
Table II.—The prevalence and types of thyroid disorders and anaemia (a = P<0.05 compared to normal thyroid;
b = P<0.05 compared to primary hypothyroidism; c = P<0.05 compared to subclinical hypothyroidism and
d = P<0.05 compared to primary hyperthyroidism).
Thyroid disorder (162 females)
Normal thyroid Overt Occult
(n = 338) Hyperthyroidism Hypothyroxinaemia
hypothyroidism hypothyroidism (n = 6) (n = 24)
(n = 32) (n = 102)
Non-anaemic 286 females 16 females 66 females 6 females 10 females
(n = 382) (84.6%) (50%) (62.5%) a (100%) (41.6%) a
Anaemic Microcytic 40 females 12 females 32 females Zero female 2 females
(n = 118) Hypochromic (11.8%) (37.5%) a (31.4%) a (0%) (8.4%) b,c
(86 females)
Normocytic 12 females 4 females 4 females Zero female 12 females
Normochromic (3.6%) (12.5%) (3.9%) (0%) (50%) a,b,c
(32 females)
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Figure 1.—Mean ± SD of (1) RBCs count, (2) haemoglobin concentration, (3) PCV and (4) MCV in normal and abnor-
mal thyroid (* =P<0.05 compared to normal thyroid).
tion (SD) of RBCs count (4.1±0.5 X 106/µL), cantly higher (394.3 µg/dL; range: 200-889
haemoglobin concentration (11.5±1.3 gm/ µg/dL) in the ‘thyroid disorder’ group when
dL), PCV (35.7±1.3 %) (Figure 1), median of compared to the “control” group (Figure 2).
serum iron (67.2 µg/dL; range: 8-141 µg/dL), However, there was no significant differ-
ferritin (30.5 ng/mL; range: 3.15-200 ng/mL) ence for the MCV and MCH between the
and TfSat (21.2%; range: 1-45%) were signif- 2 groups. Significant differences were de-
icantly lower and median TIBC was signifi- tected between the different thyroid groups
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Figure 2.—Median of (1) serum iron, (2) TIBC, (3) ferritin and (4) transferrin saturation in normal and abnormal thy-
roid (* = P<0.05 compared to normal thyroid).
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in erythrocyte indices and iron parameters hypochromic anaemia (11.8%) and 12 fe-
(Table III). males with normocytic normochromic
In the 500 study participants, 32 females (3.6%). On the other hand, microcytic hy-
had primary hypothyroidism (6.4%), 102 pochromic anaemia was detected in 46 fe-
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“anaemic group” (118 participants) were: 86 (Figure 3). Furthermore, microcytic hy-
females with microcytic hypochromic (72.8%) pochromic anaemia was significantly more
and 32 normocytic normochromic (27.2%) prevalent within the ‘normal thyroid’ and
anaemia. The prevalence of microcytic hy- ‘thyroid disorder’ groups compared to nor-
pochromic anaemia was significantly higher mocytic normochromic anaemia (P<0.05).
(P=0.0003) compared to the other type. In the 32 females with primary hypothy-
roidism, anaemia was detected in 16 cases
Prevalence and types of anaemia according (50%). Twelve cases were diagnosed with
to thyroid profile microcytic hypochromic anaemia (37.5%)
and 4 females with normocytic normochro-
In participants with normal thyroid pro- mic anaemia (12.5%). Anaemia was detect-
file (N.=338), 40 females had microcytic ed in 36 out of 102 females with subclini-
Vol. 173 - No. 1 GAZZETTA MEDICA ITALIANA - ARCHIVIO PER LE SCIENZE MEDICHE 5
REFAAT Thyroid disorders and anaemia in pregnancy
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Figure 3.—Prevalence of anaemia according to (1) thyroid status, (2) the different types of thyroid disorders and (3)
types and prevalence of anaemia according the different types of thyroid disorder.
Table III.—Mean ±SD of erythrocyte indices and median of iron parameters (a = P< 0.05 compared to
normal thyroid; b = P < 0.05 compared to primary hypothyroidism; c = P < 0.05 compared to subclinical
hypothyroidism and d = P < 0.05 compared to primary hyperthyroidism).
Overt Occult
Normal thyroid Hyperthyroidism Hypothyroxinaemia
hypothyroidism hypothyroidism
RBCs count (X106/µL) 4.6 ±0.43 4.1 ±0.2a 4.3 ±0.3a 4.5 ±0.15b,c 3.9 ±0.5a,d
Hb (g/dL) 12.4 ± 1.1 11.3 ±0.7a 10.9 ±1.5a 12 ±1.3b,c 11.1 ±1.2a,d
PCV (%) 37.2 ±3.6 35.6 ±2.8a 37.3 ±3.5 37 ±1.6 33.8 ±3.5a,c,d
MCV (fL) 84.7 ±7.3 84.6 ±5.8 82.5 ±8.1 85.7 ±2.6 85.1 ±6.1
MCH (pg) 27.9 ±2.8 27.6 ±2 27 ±3 27.5 ±2.3 28.2 ±2.6
96.6 61.3 66 107.2 70
Serum iron (µg/dL)
(range: 5.6-155) (range: 8.6-132) a (range: 13-141) a (range: 45-120) (range: 11-108) a
352 386 398 357 375
TIBC (µg/dL)
(range: 198-889) (range: 200-821) (range: 226-821) (range: 319-375) (range: 259-889)
77 24.2 30.3 72.5 46.8
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Ferritin (ng/mL)
(range: 1-231) (range: 4-200) a (range: 3-199) a (range: 50-94) b,c (range: 3-178) a,d
25 16.9 19.7 26.3 21.8
Transferrin saturation (%)
(range: 1-55) (range: 1-37) a (range: 2-45.2) a (range: 11-43) b,c (range: 1-40) a,d
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cal hypothyroidism (35.3%) and according detected only in 6 females and all were not
to the type of anaemia 32 females had anaemic. In the hypothyroxinaemia group
microcytic hypochromic anaemia (31.4%) (N.=24), 14 females were found anaemic
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and 4 females had normocytic normochro- (58.3%), with 2 females diagnosed with mi-
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mic (3.9%). Primary hyperthyroidism was crocytic hypochromic anaemia (8.3%) and
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Figure 4.—Correlation of serum free T4 with (1) RBCs count, (2) haemoglobin concentration, (3) MCV; and (4) cor-
relation of serum TSH with serum ferritin.
Vol. 173 - No. 1 GAZZETTA MEDICA ITALIANA - ARCHIVIO PER LE SCIENZE MEDICHE 7
REFAAT Thyroid disorders and anaemia in pregnancy
Table IV.—Results of correlation analysis using Pearson’s test for the haematological indices with
TSH and FT4.
Transferrin
RBCs Hb HCT MCV MCH IRON TIBC Ferritin Saturation
R value -0.033 -0.052 -0.021 -0.033 -0.036 -0.166* 0.127* -0.230* -0.195*
TSH
P value 0.4 0.2 0.6 0.4 0.4 0.009 0.004 0.003 0.002
R value 0.335* 0.395* 0.402* 0.036 0.041 0.060 -0.136* 0.009 0.086
FT4 P value 0.0005 0.00002 0.00003 0.4 0.3 0.1 0.002 0.8 0.5
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pothyroidism groups while the prevalence Additionally, the prevalence of anaemia was
of normocytic normochromic was signifi- higher in the primary hypothyroidism and
cantly higher in the “hypothyroxinaemia” hypothyroxinaemia groups compared to
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group (P<0.05). Significant difference were
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also detected in the RBCs count, haemo- of anaemia was microcytic hypochromic
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globin concentrations, PCV, serum iron, and it was more prevalent in females with
ferritin and transferrin saturation between overt and occult hypothyroidism. Alterna-
the different types of thyroid disorders (Ta- tively, normocytic normochromic anaemia
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ble III). was more common in females with hy-
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tected for serum FT4 with RBCs count, tion and positively with TIBC.
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haemoglobin concentrations and PCV (Fig- The present results suggest that thyroid
ure 4). Additionally, TSH correlated posi- disorders are common in primigravida
tively with TIBC and negatively with se- Saudi women from the Western province
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rum iron, ferritin and transferrin saturation of the kingdom during the first trimester.
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The present study agrees with the pre- nancy without change in TSH level could
vious findings as it showed an overall be in part by the physiological effect of
prevalence of 32.4% for thyroid disorders. β-chorionic gonadotropin on the serum
The majority of cases were subclinical hy- level of thyroxin binding globulin and the
pothyroidism (20.4%) followed by primary subsequent increase in total T4 levels.20
hypothyroidism (6.4%). The frequency of The observed hypothyroxinaemia could
both types was significantly higher than also be due to iodine deficiency, which
hyperthyroidism (1.2%). have been reported either in patients with
Studies on the frequency of thyroid dis- hypothyroidism or during pregnancy in the
orders during pregnancy in the Middle same region of the Kingdom.35, 36 Hence,
East, specifically in Saudi Arabia, are limit- the present data should be interpreted in
ed in number. The prevalence of overt and the light that evaluation of iodine deficien-
occult hypothyroidism is in the present cy was not performed in the current study.
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study is higher than the previously report- Additionally, the applied normal range in
ed frequency from several Western socie- the current study for FT4 was adopted
ties (05-2.5% for overt and 4.6-12.5% for from a previous report from the United Ar-
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occult hypothyroidism).27 Nevertheless, re-
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sults from pregnant Jordanian women have knowledge, this is the only study generat-
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shown similar frequency rates to the cur- ed from the Gulf region till present. There-
rent study for hypothyroidism.28 Therefore, fore, the present report indicates the need
the observed high frequency of pregnancy for further studies to measure the iodine
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induced thyroid dysfunction merits further intake during pregnancy and to determine
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research and thyroid antibodies profile the normal range of thyroid hormones dur-
and urine iodine should be included to
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ing pregnancy in the Saudi population as
precisely identify the type and etiology of recommended by several scientific socie-
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thyroid disorder. ties.19, 27, 37-40
Additionally, the current data support Although anaemia was reported with
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the hypothesis that thyroid hormones the different types of thyroiditis, it is more
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the ‘thyroid disorder’ and ‘normal thyroid’ the observed increase in erythrocyto-
groups and anaemia was detected in 40.7% sis.5, 21 The current study correlates with
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of the females suffering from thyroid dis- the earlier observations as it demonstrates
orders compared to 15.3% in those with a significant increase in the prevalence of
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ated with pregnancy, was first described in the prevalence of anaemia in pregnant
by Evelyn Man almost 40 years ago.29 This females with overt hypothyroidism and
condition is considered a milder form of those with hypothyroxinaemia, support-
thyroid dysfunction and it is characterised ing the hypothesis that thyroid hormones
by a merely decrease in serum free T4 with play an important role in haematopoiesis.
normal serum TSH levels.3 The currently However, the present results suggest that
reported prevalence of hypothyroxinaemia the type of anaemia could be dependent
ranges between 1.3-30%.30-34 on the form of thyroid dysfunction as mi-
The prevalence of hypothyroxinaemia crocytic hypochromic anaemia was associ-
is the present study was 4.8% and it cor- ated with hypothyroidism and normocytic
relates with the aforementioned reports. normochromic anaemia was frequent with
The decrease in Free T4 during early preg- maternal hypothyroxinaemia.
Vol. 173 - No. 1 GAZZETTA MEDICA ITALIANA - ARCHIVIO PER LE SCIENZE MEDICHE 9
REFAAT Thyroid disorders and anaemia in pregnancy
Several types of anaemia have been re- Currently there no report on the prev-
ported with thyroid disorders and they alence and types of anaemia associated
include normocytic normochromic, mi- with hypothyroxinaemia. The present re-
crocytic and/or macrocytic hypochromic, sults showed that this thyroid disorder was
and the severity of anaemia is related to mainly associated with normocytic normo-
the degree of thyroid abnormality.12, 13 chromic anaemia, supporting the hypoth-
Anaemia of chronic disease, which is in esis that thyroxin plays a key role in the
the form of normocytic normochromic, is regulation of bone marrow activity and
the most frequently encountered type of erythropoiesis, which could be through
anaemia in non-pregnant females suffering stimulating the production of erythropoie-
from hypothyroidism.5, 21 It has been sug- tin hormone.11, 47 However, it appears from
gested that thyroid hormones deficiency the present study that this hormone does
may lead to bone marrow repression and/ not affect the iron metabolism during the
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or decrease in erythropoietin production first trimester of pregnancy as there was
due to the reduction of O2 requirements.11 no significant correlation between serum
Hypochromic microcytic anaemia is less
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free T4 and the iron parameters. Additional
frequently associated with hypothyroidism
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in non-pregnant females and it is mainly
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thyroxin on the production of erythropoi-
due to iron deficiency.11-13 etin and the metabolism of iron.
Although the types of anaemia detected In conclusion, thyroid disorders are com-
in the current study were similar to those
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mon in primigravida Saudi females in the
reported previously with hypothyroidism, western province of the kingdom and they
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the most common type was microcytic hy- are associated with a decrease in RBCs
pochromic followed by normocytic nor-
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count, haemoglobin concentration, haema-
mochromic anaemia. During pregnancy,
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tocrit value, iron parameters and increase
there is an increase demand for iron and in the frequency of anaemia. Further stud-
it has been reported that the thyroid hor-
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the combination of levothyroxine and iron 1. Lazarus JH, Thyroid function in pregnancy. Br Med
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Vol. 173 - No. 1 GAZZETTA MEDICA ITALIANA - ARCHIVIO PER LE SCIENZE MEDICHE 11
REFAAT Thyroid disorders and anaemia in pregnancy
indices in a cohort of euthyroid older subjects. Eur proaches for estimation. Indian J Clin Biochem
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pothyroid subjects in a tertiary care center in East- Acknowledgments.—The author would like to thank Ms.
ern India. Indian J Endocrinol Metab 2012;16:S361- Bashayer Al-Barakati and Ms. Athar Khojah from the Labo-
3. ratory Medicine Department, Faculty of Applied Medical
45. Bremner AP, Feddema P, Joske DJ, Leedman PJ, Sciences, Umm Al-Qura University for processing the sam-
O’Leary PC, Olynyk JK et al., Significant associa- ples.
tion between thyroid hormones and erythrocyte in- Conflicts of interest.—The authors certify that there is
dices in euthyroid subjects. Clin Endocrinol (Oxf) no conflict of interest with any financial organization re-
2012;76:304-11. garding the material discussed in the manuscript.
46. Patel M, Ramavataram DV. Non transferrin bound Received on July 17, 2014.
iron: nature, manifestations and analytical ap- Accepted for publication on October 20, 2014.
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