Acta Pdiatr 89: 6759.

2000

Erythropoietic activity and soluble transferrin receptor level in

neonates and maternal blood
JW Choi1, CS Kim2 and SH Pai1
Departments of Clinical Pathology1 and Internal Medicine2, College of Medicine, Inha University, Inha University Hospital, Inchon,
Korea

Choi JW, Kim CS, Pai SH. Erythropoietic activity and soluble transferrin receptor level in
neonates and maternal blood. Acta Pdiatr 2000; 89: 6759. Stockholm. ISSN 08035253
Serum transferrin receptor (sTfR) concentration reflects functional iron status and erythropoietic
activity. The aims of this study were to examine gender differences of erythropoiesis in newborns
and to evaluate the influences of maternal anaemia or iron deficiency on foetal cord blood
parameters for iron status and sTfR. In total, 527 newborns and their mothers were examined.
Reticulocytes were analysed by flow cytometry and sTfR was measured by an immunoenzymo-
metric method. There were no sex differences in haematological or iron parameters. However, the
reticulocyte maturity index (RMI) of male neonates was 37.45%, significantly higher than the
26.81% in female neonates (p < 0.01). The high fluorescence reticulocytes (HFR) and middle
fluorescence reticulocytes (MFR) of male neonates were 4.91% and 22.36%, respectively, while
those of female neonates were 3.31% and 17.83%, respectively (p < 0.01 for each gender). The
sTfR concentrations of male and female neonates were 6.27 mg/l and 5.09 mg/l, respectively
(p < 0.01). Values for serum iron, ferritin and reticulocyte subpopulations were significantly lower
in the newborns of anaemic mothers. However, newborns of iron-deficient mothers showed no
differences in iron parameters from those of non-iron-deficient mothers.
Conclusions: The higher values of RMI and sTfR observed in male neonates indicate that
erythropoietic activity is higher in this group. Iron transport to the foetus appears to be independent of
maternal iron deficiency. However, iron transport and erythropoiesis in newborns seems to decline
from the time that the mothers acquire frank iron deficiency anaemia.
Key words: Erythropoiesis, mother, neonate, transferrin receptor
JW Choi, Department of Clinical Pathology, Inha University Hospital, 7-206, 3-ga, Shinheung-
dong, Jung-gu, Inchon 400-103, Korea (Tel. 82 32 890 2503, fax. 82 32 890 2529, e-mail.
jwchoi@inha.ac.kr)

Reticulocyte analysis by flow cytometry is superior to
manual reticulocyte counting with respect to sensitivity
and precision (1). Since the fluorescence intensity of
reticulocytes is directly proportional to the erythrocyte
RNA content, flow cytometric analysis is able to
differentiate the following three reticulocyte subpopu-
lations according to their degree of maturity: low
fluorescence reticulocytes (LFR), middle fluorescence
reticulocytes (MFR) and high fluorescence reticulocytes
(HFR) (1, 2). The reticulocyte maturity index (RMI) is
calculated from the proportion of reticulocyte subpo-
pulations and is widely used as an early and very
sensitive predictor of erythropoiesis following bone
marrow transplantation (2).
Measurement of the concentration of the serum
transferrin receptor (sTfR) has been introduced recently
as a new diagnostic tool for the evaluation of iron status
(35). The extracellular transport of iron in the body is
accomplished by the binding of iron to a specific carrier
protein, transferrin (6). The transferrin receptor
mediates the flow of serum iron from the extracellular
pool into the cytoplasm by receptor-mediated endocy-
tosis (7). Virtually all mammalian cells have transferrin
receptor on their cell surfaces, although most of the
receptors are located on the erythroid precursors of bone
marrow (8). The erythropoietic cells of bone marrow
and the circulating reticulocytes eventually shed their
transferrin receptors into the blood during their matura-
tion sequence (8). Thus, the sTfR concentration
correlates directly with erythropoietic activity and
inversely with the amount of iron available for
erythropoiesis (9). Increased sTfR concentrations are
usually observed in iron deficiency, or in cases of iron
depletion in tissues, although this index is not always
specific for iron deficiency (10). Conditions associated
with erythroid hyperplasia, such as immune haemolytic
anaemia and thalassaemia, can also increase the value
of sTfR, irrespective of iron status (11, 12).
Previous studies have demonstrated that no gender
differences exist in sTfR concentrations of adults and

2000 Taylor & Francis. ISSN 0803-5253

676 JW Choi et al. ACTA PDIATR 89 (2000)

children (13, 14). In neonates, however, iron status and nostica, Orion Co., Finland). The sTfR test was
erythropoietic activity are different from those of adults performed as described previously (9). We diluted and
and children; active transfer of iron from the mother to reanalysed any sample that had a concentration higher
the foetus occurs continuously, and this transport has than the highest calibrating standard.
been reported to be independent of foetal erythropoiesis Newborns were divided into two groups according to
(15). In the present study, we investigated malefemale gender and were classified according to maternal
differences in neonates with respect to the three anaemia or maternal iron deficiency (ferritin
reticulocyte subpopulations, RMI, and sTfR. We also <12 mg/l). Reticulocytes, their subpopulations and sTfR
attempted to determine whether foetal cord blood levels were compared according to neonatal sex and
parameters for iron status and erythropoiesis were maternal iron status.
influenced, on the one hand, by a maternal state of iron Data analysis was performed using the SAS statistical
deficiency, and on the other hand, by frank anaemia. computing software package (version 6.12 for win-
dows; SAS Institute Inc., Cary, NC, USA). The com-
parison of means was analysed by a non-parametric
method (Mann-Whitney test) when data were not
Subjects and methods normally distributed (serum iron, ferritin and sTfR).
The study population consisted of 608 mothers and their To determine differences between two independent
neonates, admitted for delivery to Inha University groups (haemoglobin, reticulocytes and their subpopu-
Hospital. Out of the 608 newborns, only 527 were lations), Students t-test was used. Any p-values less
investigated for reticulocyte subpopulations and sTfR, than or equal to 0.01 were considered statistically
as well as iron parameters. Among the 81 subjects significant.
excluded from the study population, 39 newborns had a
low birthweight <2500 g and 6 had foetal anomalies.
The remaining 35 were subjects who had incomplete or
non-recorded data in the medical records and 1 mother Results
who had a haematological malignancy. The Ethics Of the 527 neonates tested in the study, male neonates
Committee of Inha University Hospital approved the comprised 51.9% of the total. The clinical features and
study and informed consent was obtained from all birth history of the newborns are summarized in Table
subjects. 1. Among the 527 mothers, 186 (35.3%) were anaemic
The medical charts of all neonates and their mothers subjects (haemoglobin <110 g/l) and 229 (43.5%) were
were reviewed to assess the birth history and clinical iron-deficient. A total of 318 (60.3%) mothers included
features of the subjects. Blood specimens were drawn in this study had a history of iron supplementation. Out
before any blood transfusion. On admission for labour, of these 318 iron-treated mothers, 86 (27.0%) exhibited
5 ml of maternal blood was obtained by venipuncture. iron deficiency anaemia. Birthweights and placental
For the examination of neonates, 3 ml of foetal blood weights for male neonates were slightly higher than
was drawn from the umbilical vein in the cord within those for female neonates; however, no statistical
5 min of delivery. Complete blood cell count (CBC) and
reticulocyte subpopulations were measured with
EDTA-anticoagulated blood within 3 h of collection. Table 1. Clinical features and birth history of the neonates included
Sera for the measurement of sTfR and ferritin were in this study.
stored in 500-ml aliquots at 70 C until analysis. Female
Male neonates neonates
Anaemia of pregnancy was defined as a haemoglobin Parameters (n = 274) (n = 253) p-value
level of less than 110 g/l, according to WHO criteria
Birthweight (kg) 3.11  0.54 3.07  0.44 0.41
(16). Non-anaemic mothers who had a serum ferritin Placenta weight (kg) 0.66  0.13 0.65  0.14 0.56
concentration of less than 12 mg/l were classified as iron Cord length (m) 0.56  0.08 0.57  0.09 0.42
deficient. Routine CBC and red cell indices were Apgar score (mean)
determined with an electronic counter (SE 90002, 5 min 8.6  0.5 8.5  0.4 0.63
Sysmex, Toa, Japan). Reticulocytes and their subpopu- 10 min 9.6  0.3 9.4  0.3 0.40
Route of delivery (n)
lations were analysed automatically by flow cytometry Normal 205 192 0.27
using an R-30002 (Sysmex). RMI was calculated C-section 69 61 0.34
according to the equation RMI = (MFR HFR)  100/ Maternal anaemia 97 89 0.21
LFR, and was expressed as a percentage (17). (Hb <110 g/l, n)
Maternal iron deficiency 119 110 0.36
Serum iron and total iron-binding capacity (TIBC) (ferritin <12 mg/l, n)
were assayed with an automatic chemical analyser Iron-treated mothers (n) 167 151 0.29
(Hitachi 7472, Hitachi, Tokyo, Japan) and ferritin was Maternal anaemia in iron 46 40 0.48
measured by radioimmunoassay. Serum transferrin treated group (n)
receptor levels were determined by an immunoenzymo- Gestational age (wk) 38.64  2.59 38.93  1.91 0.62
29.97  3.51 29.94  3.92
metric method using IDeA2 sTfR kits (Orion Diag- Maternal age (y) 0.85
ACTA PDIATR 89 (2000) Difference of erythropoietic activity in neonates 677

Table 2. Maternal blood values for reticulocyte subpopulations and Table 4. Differences in red blood cell counts and reticulocyte
sTfR between mothers bearing male or female neonates. subpopulations between male and female neonates.
Maternal blood (n = 527) Male neonates Female neonates
Parameters (n = 274) (n = 253) p-value
Bearing male Bearing female
Parameters of mothers neonates neonates p-value RBC (n, 1012/l) 4.5884  0.3701 4.5378  0.3623 0.29
Reticulocytes (%) 3.91  0.26 3.12  0.21 <0.01
RBC (n, 10 /l)
12
4.0154  0.3610 4.0232  0.3611 0.23 Reticulocytes (n, 10 /l) 0.1793  0.0113 0.1415  0.0103
12
<0.01
Reticulocytes (%) 1.87  0.39 1.84  0.49 0.67 LFR (%) 72.81  2.08 78.85  2.73 <0.01
Reticulocytes (n, 10 /l) 0.0751  0.0123 0.0740  0.0119
12
0.21 MFR (%) 22.36  1.73 17.83  1.91 <0.01
LFR (%) 89.50  5.52 88.89  4.47 0.34 HFR (%) 4.91  0.94 3.31  0.91 <0.01
MFR (%) 9.93  4.95 10.55  4.03 0.25 RMI (%) 37.45  3.94 26.81  3.91 <0.01
HFR (%) 0.57  0.36 0.56  0.35 0.71
RMI (%) 11.73  4.71 12.49  4.80 0.30 Abbreviations: see Table 2.
s-iron (mg/l) 732.6  378.1 783.3  364.1 0.42
TIBC (mg/l) 4745.7  755.1 4719.2  768.3 0.41
TS (%) 15.41  7.92 16.67  6.70 0.69 neonates were 17.83% and 3.31%, respectively
Ferritin (mg/l) 18.18  9.56 19.98  9.75 0.38
sTfR (mg/l) 4.19  0.73 4.15  0.61 0.12 (p < 0.01 in each case). The RMI of male neonates
was 37.45%, significantly higher than the 26.81% in
LFR: low fluorescence reticulocytes; MFR: middle fluorescence female neonates (p < 0.01). The mean sTfR concentra-
reticulocytes; HFR: high fluorescence reticulocytes; RMI: reticulocyte
maturity index; s-iron: serum iron level; TIBC: total iron binding
tions of male and female neonates were 6.27  0.51 mg/
capacity; TS: transferrin saturation; sTfR: serum transferrin receptor. l and 5.09  0.43 mg/l, respectively (p < 0.01). How-
ever, there were no differences in iron parameters, CBC
or red cell indices between the two groups (Table 5).
significance was noted. There were no differences in Tables 6 and 7 summarize the changes in reticulocyte
gestational age and Apgar score between the two subpopulations and sTfR concentrations of newborns
groups. Maternal blood values for reticulocyte sub- according to the presence of maternal anaemia or
populations and sTfR showed no significant differences maternal iron deficiency. Reticulocyte subpopulations,
between mothers bearing male or female newborns serum iron and ferritin concentrations were significantly
(Table 2). lower in the newborns of mothers who had iron
The results for iron parameters and sTfR levels in deficiency anaemia than those of non-anaemic mothers
neonates and their mothers are summarized in Table 3. (Table 6). However, there were no significant differ-
The mean sTfR concentration in neonates was 5.68 mg/ ences in reticulocyte subpopulations and ferritin in
l, significantly higher than the concentration of 4.17 mg/ cases of maternal iron deficiency (Table 7). On the other
l in maternal blood (p < 0.01). Serum iron and ferritin hand, the sTfR value for newborns of mothers with iron
levels in newborns were 1969.2 mg/l and 183.27 mg/l, deficiency was significantly higher (6.32 mg/l) than that
respectively. These values were also significantly for newborns of non-iron-deficient mothers (5.04 mg/l;
higher than the serum iron value (767.6 mg/l) and p < 0.01; Table 7).
ferritin concentration (19.08 mg/l) of maternal blood
(p < 0.01 in each case).
Table 4 summarizes the differences in red blood cell
counts and reticulocyte subpopulations between male Discussion
and female neonates. There were no differences in red According to recent studies, there is no significant
blood cell counts between the two groups (p = 0.29).
However, both the reticulocyte count and the reticulo-
cyte subpopulations showed significant differences Table 5. Comparison of sTfR concentrations, iron parameters and red
cell indices between the two groups.
(p < 0.01). The MFR and HFR of male neonates were
Male neonates Female neonates
22.36% and 4.91%, respectively, while those of female Parameters (n = 274) (n = 253) p-value
sTfR (mg/l) 6.27  0.51 5.09  0.43 <0.01
s-iron (mg/l) 1962.8  523.1 1962.2  501.5 0.81
Table 3. Results for iron parameters and sTfR levels in neonates and TIBC (mg/l) 3096.1  768.6 3062.1  723.6 0.52
their mothers. TS (%) 63.31  11.72 64.08  14.30 0.45
Ferritin (mg/l) 182.65  55.20 183.89  53.70 0.93
Neonates Maternal blood
Haemoglobin (g/l) 159.3  10.3 158.7  9.5 0.44
Parameters (n = 527) (n = 527) p-value
Haematocrit (%) 49.86  5.09 49.17  3.87 0.47
sTfR (mg/l) 5.68  0.64 4.17  0.62 <0.01 MCV (fL) 109.35  5.30 110.14  5.19 0.12
Iron parameter MCH (pg) 36.12  1.73 36.23  1.50 0.19
s-iron (mg/l) 1969.2  508.9 767.6  329.8 <0.01 MCHC (g/dl) 32.80  0.92 32.71  0.92 0.46
TIBC (mg/l) 3077.1  713.4 4739.6  741.1 <0.01 RDW (%) 16.24  0.91 16.17  0.84 0.21
TS (%) 63.92  13.82 16.21  7.91 <0.01
Ferritin (mg/l) 183.27  54.65 19.08  8.43 <0.01 sTfR: serum transferrin receptor; MCV: mean corpuscular volume;
MCH: mean corpuscular haemoglobin; MCHC: mean corpuscular
Abbreviations: see Table 2. haemoglobin concentration; RDW: red cell distribution width.
678 JW Choi et al. ACTA PDIATR 89 (2000)

Table 6. Changes in reticulocyte subpopulations and sTfR concen- of erythropoiesis. In our study, the number of reticulo-
trations of neonates according to the presence of maternal anaemia. cytes, their subpopulations and the RMI of male
Neonates (n = 527) neonates were all significantly higher than the equiva-
Without lent values in female neonates. Moreover, male
With maternal maternal neonates showed significantly higher sTfR concentra-
anaemia anaemia tions than did female neonates. Contrary to Yeung and
Parameters of neonate (n = 186) (n = 341) p-value Zlotkins finding (13), our data showed definite gender
RBC (n, 1012/l) 4.4017  0.4611 4.6421  0.3473 0.11 differences in sTfR concentration. The reason seems to
Reticulocytes (%) 3.16  0.23 3.87  0.17 <0.01 be that we analysed only newborns (as described
Reticulocytes (n, 1012/l) 0.1391  0.0137 0.1796  0.0106 <0.01
LFR (%) 78.63  2.94 71.65  2.58 <0.01
above).
MFR (%) 18.42  1.43 22.69  1.82 <0.01 In another of our studies on age- and sex-related
HFR (%) 2.95  1.19 5.65  0.93 <0.01 differences in sTfR (18), male infants aged 46 mo also
RMI (%) 27.17  4.23 39.55  3.19 <0.01 showed higher values of sTfR than female infants of the
s-iron (mg/l) 1721.2  571.6 2212.4  514.3 <0.01 same age group. Therefore, we speculate that erythro-
TIBC (mg/l) 3313.6  741.5 2876.8  678.1 <0.01
TS (%) 51.86  17.75 76.47  16.01 <0.01 poietic activity in male neonates is greater than in
Ferritin (mg/l) 161.62  56.38 215.91  47.35 <0.01 female neonates, at least for a short period after birth.
sTfR (mg/l) 6.51  0.67 4.85  0.63 <0.01 These results can be partly explained by the observa-
Abbreviations: see Table 2.
tions of Kuiper-Kramer et al. (19), who found day-to-
day variations in sTfR concentration shortly after birth.
In our study, erythropoietic activity was higher in male
neonates, whereas the haematocrit level was not higher
difference in sTfR concentration between adult men and in this group. It is possible that male infants may
women (13, 14). Yeung and Zlotkin (13) found no experience longer labour or more perinatal hypoxia,
difference in sTfR concentration between male and resulting in higher sTfR concentrations and a higher
female infants aged 915 mo. However, the haemato- RMI (which rises fairly quickly), although not a higher
logical and iron parameters of newborns are different haematocrit level (which takes longer to rise). However,
from those of children and adults because newborns are this hypothesis cannot be verified by the data presented
in a state of rapid growth and active haematopoiesis. in this study.
Moreover, there are few studies on gender differences in Iron deficiency may occur due to blood loss, an
erythropoiesis and sTfR concentration of newborns. increased demand for iron, malabsorption or poor diet.
To evaluate the erythropoietic activity of newborns in Iron deficiency develops in sequential stages over a
this study, we focused on measuring reticulocyte period of negative iron balance (20). In our study, we
subpopulations and sTfR concentration, because the investigated changes in iron status and reticulocyte
reticulocyte number is a good indicator of effective production in newborns according to the presence of
erythropoiesis and sTfR reflects bone marrow erythro- maternal anaemia or an iron-deficient state. The levels
poietic activity. The RMI calculated from reticulocyte of serum iron, ferritin and reticulocytes were signifi-
subpopulations is an especially valuable early predictor cantly lower in newborns whose mothers had iron
deficiency anaemia than in those of non-anaemic
mothers. These findings are in accord with a previous
Table 7. Changes in reticulocyte subpopulations and sTfR concen- study showing that maternal anaemia adversely affected
trations of neonates according to the presence of maternal iron the iron status of newborns (21).
deficiency. However, our study shows that maternal iron
Neonates (n = 527) deficiency has no influence on the iron status and
reticulocyte subpopulations of neonates. Even in
Maternal serum Maternal serum
ferritin <12 mg/l ferritin 12 mg/l
mothers with decreased ferritin levels, the cord blood
Parameters of neonate (n = 229) (n = 298) p-value demonstrated high levels of serum iron and an elevated
RBC (n, 1012/l) 4.4742  0.4328 4.5986  0.3448 0.21
ferritin concentration. These results are consistent with
Reticulocytes (%) 3.46  0.31 3.57  0.21 0.16 Singla et al.s finding (22). On the basis of our results,
Reticulocytes (n, 1012/l) 0.1548  0.0211 0.1642  0.0113 0.23 we believe that the active transfer of iron from mother to
LFR (%) 76.72  3.29 74.45  2.37 0.30 foetus occurs even when the mother is in an iron-
MFR (%) 20.02  1.81 20.74  1.41 0.54 deficient state. Once a mother has attained a state of
HFR (%) 3.31  1.13 4.79  1.75 0.12
RMI (%) 30.49  4.11 34.27  3.17 0.09 frank anaemia, iron transport and erythropoiesis are
s-iron (mg/l) 1924.1  540.2 2034.2  345.9 0.29 eventually reduced. In our study, however, we were
TIBC (mg/l) 3084.5  713.1 3048.7  777.2 0.41 unable to clarify whether a mothers iron endowment to
TS (%) 62.37  13.12 66.72  14.89 0.35 the neonate still occurs in cases of severe iron
Ferritin (mg/l) 182.76  58.23 187.06  54.07 0.28
sTfR (mg/l) 6.32  0.62 5.04  0.51 <0.01
deficiency.
The number of transferrin receptors expressed on the
Abbreviations: see Table 2. cell surface reflects the iron requirements of a tissue
ACTA PDIATR 89 (2000)
(9, 23). Iron deprivation induces a prompt synthesis of
the transferrin receptor (9). Increased blood sTfR values
are usually observed in iron-depleted states, whereby
the concentration of sTfR correlates inversely with the
amount of iron available for erythropoiesis (24). sTfR
concentrations may also be reduced in iron overload
conditions (25). In our study, we investigated cord
blood sTfR and ferritin concentration. The cord blood
iron and ferritin values were several times higher than
those of the mothers. Moreover, the cord sTfR con-
centration was significantly higher than the maternal
sTfR value. Since sTfR levels reflect erythropoiesis and
iron deficiency, the elevated cord sTfR concentration of
newborns, who exhibited no evidence of functional iron
deficiency, seems to represent an increased erythro-
poietic activity in this period.
We also evaluated changes in cord sTfR concentra-
tion according to maternal iron status. The mean sTfR
concentration was significantly higher in neonates born
to anaemic mothers than in those born to non-anaemic
mothers. These results are quite similar to the findings
of Rusia et al. (26). However, in our study, newborns of
iron-deficient mothers also showed high values of sTfR.
Contrary to the iron parameters, the sTfR levels of
newborns were changed by maternal iron deficiency, as
well as by maternal anaemia. Therefore, cord blood
sTfR appears to be a more sensitive indicator of
maternal iron status than cord blood iron parameters.
In conclusion, we found that erythropoietic activity
does exhibit gender-related differences in newborns:
erythropoietic activity is higher in male neonates than in
female neonates. Iron transport from the mother to the
foetus persists even when the mother is suffering from
iron deficiency. However, once a mother acquires iron
deficiency anaemia, then iron transport and erythro-
poiesis seems to be eventually reduced in the offspring.
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