ARTICLE IN PRESS

Journal of
Trace Elements
in Medicine and Biology
Journal of Trace Elements in Medicine and Biology 19 (2006) 243–249
www.elsevier.de/jtemb

BIOCHEMISTRY
Do indicators of maternal iron status reflect placental iron status
at delivery?
Silvia Haydee Langinia,,1, Marı́a Luz de Portelaa, Araceli Lázzarib,2,
Carlos Rafael Ortega Solerb,2, Bo Lönnerdalc,3
a
Department of Nutrition, School of Pharmacy and Biochemistry, University of Buenos Aires, Buenos Aires,
Junı´n 956-2do (1113) Buenos Aires, Argentina
b
Diego Paroissien Hospital, La Matanza, Argentina
c
Department of Nutrition, University of California, Davis, CA 95616, USA

Received 19 September 2005; accepted 14 November 2005

Abstract

Indicators of maternal iron (Fe) status were studied in relation to placental Fe (Pl-Fe) status. Placental (Pl) and
maternal (M) venous blood samples were obtained from primiparous women (n ¼ 38), with normal delivery at
Paroissien Hospital, Argentina. Maternal hemoglobin (M Hb), soluble transferrin receptor (M sTfR) (ELISA) and
serum ferritin (M S-Ft) were studied in relation to Pl-Fe, ferritin (Pl-Ft) and transferrin receptor (Pl-TfR). Pl-TfR was
measured by dot blot assay, Pl-Ft and M S-Ft by immunoassay (IRMA) and Pl-Fe by atomic absorption spectrometry.
Fe status indicators were, respectively, (mean7SD): M Hb 113716 g/L; M S-Ft 36742 mg/L; M sTfR 6.373.1 mg/L;
Pl-Fe 170756 mg/g placenta; Pl-Ft 33718 mg/g placenta; Pl-TfR 18718 (range 0–58) mg/g placenta. Pl-Fe, Pl-Ft and
Pl-TfR did not correlate to M Hb, M S-Ft and M sTfR. Women with Pl- Fe, Pl-Ft and Pl-TfR above or below the
corresponding median values did not show any statistical significant difference in M Hb, M sTfR or M S-Ft values.
Pl-Ft concentration was lower in women with Hbo110 g/L than in women with normal values: 26713 vs. 38720 mg/g,
respectively (p ¼ 0:021). When Pl-TfR, Pl-Ft and Pl-Fe were compared in women with M S-Ft above or below the cut-
off point of 10 or 20 mg/L, no significant difference was found for Pl-TfR neither for Pl-Ft nor Pl-Fe. These results
suggest that maternal indicators of Fe status, particularly M sTfR and M S-Ft, do not reflect Fe status of the placenta
at delivery.
r 2005 Elsevier GmbH. All rights reserved.

Keywords: Placental iron; Placental ferritin; Placental transferrin receptor; Maternal iron status; Dot blot assay

Introduction
Corresponding author.
E-mail address: slangini@ffyb.uba.ar (S.H. Langini). Iron (Fe) deficiency anemia is one of the most
1
Cátedra de Nutrición. Facultad de Farmacia y Bioquı́mica. common nutritional problems in the world and remains
Universidad de Buenos Aires. Junı́n 956-2do (1113) Buenos Aires, a major public health problem in vulnerable groups,
Argentina. such as infants and pregnant women, mainly in
2
Hospital Diego Paroissien, La Matanza, Provincia de Buenos
Aires, Argentina. developing countries [1].
3
Department of Nutrition, University of California, One Shields The laboratory tests used in the diagnosis of anemia
Avenue, Davis, CA 95616–8966, USA. and Fe deficiency include analysis of hematocrit (Hct),

0946-672X/$ - see front matter r 2005 Elsevier GmbH. All rights reserved.
doi:10.1016/j.jtemb.2005.11.004
 ARTICLE IN PRESS
244 S.H. Langini et al. / Journal of Trace Elements in Medicine and Biology 19 (2006) 243–249
hemoglobin (Hb), mean cell volume, serum Fe, total Fe-
binding capacity, transferrin saturation, erythrocyte
protoporphyrin and serum ferritin (S-Ft) [2]. In addi-
tion, Fe status can also be assessed by measuring the
concentration of the soluble transferrin receptor (sTfR)
[3], a truncated form of the receptor, which is present in
soluble form in the circulation.
There are contradictory opinions with respect to the
influence of maternal Fe status on fetal Fe status. It has
been believed for a long time that maternal Fe deficiency
has little or no effect on the acquisition of Fe by the fetus
[4,5]. However, a number of investigators have found a
positive correlation between maternal and newborn Fe
status, suggesting that the fetus is vulnerable to Fe
deficiency during intrauterine life [6], particularly with
increasing severity of maternal anemia [7].
Furthermore, the effects of maternal Fe status on Fe
status of the placenta, the organ supplying the fetus with
Fe, have not been extensively studied or understood.
The placenta is the point of interchange between
maternal and fetal circulation, where oxygen and
nutrients are transferred to the fetus and fetal waste
products are removed. All these activities are essential
for maintaining pregnancy and promoting fetal devel-
opment [8]. Placental Fe content at term was shown to
correlate with birth weight, gestational age and placental
weight [9] thus affecting fetal outcome. However,
placenta is not usually analyzed in clinical practice.
Therefore, the aim of this study was to evaluate
whether accessible parameters of maternal Fe nutri-
tional status, assessed in blood samples, could be a
useful approach to evaluate placental Fe status at
delivery. We studied the maternal Fe status in relation
to placental Fe (Pl-Fe), placental ferritin (Pl-Ft) and
placental transferrin receptor (Pl-TfR) at delivery in a
group of healthy women.
Materials and methods
Subjects
The study was carried out in 38 pregnant women
assisted at delivery at the Obstetric Service of Diego
Paroissien Hospital, in Greater Buenos Aires, Argenti-
na. The study protocol was conducted in agreement with
local ethical standards (Paroissien Hospital Committee,
September 8th, 1997 and University of Buenos Aires,
Argentina) according to Helsinki Declaration.
Selection of the women was based on the following
criteria: parity, mode of delivery and age. Only
primiparous healthy women with normal deliveries
and older than 15 years were included. Delivery
gestational age was calculated as from the last menstrual
period and through ecography. Maternal pre- and post-
Table 1. Characteristics of the participating women and
newborns
Pre-partum weight (kg) 68.7711.3 (47–93)
Post-partum weight (kg) 62.1711.1 (40–85.5)
Height (cm) 15977 (138–175)
Age (years) 2075 (16–38)
Gestational age (weeks) 3972 (31–41)
Infants birth weight (g) 31357519 (1565–4100)
Apgar score 9 (8–10)
Female:Male 22:16
Values are means7SD (range).
partum weights were recorded. Infant birth weight, sex
and Apgar score were registered by the physician. The
characteristics of the participating women and newborns
are shown in Table 1.
Blood sampling and hematologic assessment
Maternal (M) venous blood samples were collected
just before delivery for the hematologic assessment.
Hct, Hb, red blood cells (RBC) and white blood cells
(WBC) were determined by an electronic counter (Mega,
Bitex SA, Argentina).
S-Ft and sTfR were measured by immunoradiometric
assay (IRMA; Diagnostic Products, San Diego, CA,
USA) and enzyme-linked immunosorbent assay (ELI-
SA; Ramco Laboratories, Inc. Houston, TX, USA),
respectively.
The following cut-off values were used: Hct (%)o33;
Hb (g/L)o110; and S-Ft (mg/L)o10 [10]. Values of
sTfR between 2.9 mg/L and 8.3 mg/L were considered in
the normal range according to the manufacturer
(Ramco).
Placenta samples
Placenta samples were collected immediately after
delivery. The whole placenta was weighed and a small
piece (
10 g) was excised from the portion nearest to the
site of implantation of the cord. Samples analyzed for
Pl-Fe content, Pl-Ft and Pl-TfR were obtained from the
identical portion of the placental plate, as regional
variations in the levels of trace elements have been
reported [11]. A visual inspection of the placenta for
necrosis or any other abnormality was made by the
physician. Samples were kept frozen at 20 1C until
analysis.
Placental transferrin receptor determination
Pl-TfR was measured by dot blot assay [12]. Placental
homogenates were obtained in phosphate buffered
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S.H. Langini et al. / Journal of Trace Elements in Medicine and Biology 19 (2006) 243–249
saline (PBS), pH 7.4 (Sigma). Homogenization was done
in an Ultra-Turrax Tissumizer, Janke & Kunkel, IKA-
Werk. The mixture was centrifuged (Sorvall RG-5B
Refrigerated Superspeed Centrifuge) at 2000g for 15 min
and the supernatant was centrifuged again (IEC
Micromax RF) at 21 000g and 4 1C for 60 min. The
pellet was re-suspended in PBS buffer. Protein content
in the pellet and in the supernatant was determined by
Lowry assay [13].
A volume of pellet containing 0.5 mg of protein was
blotted onto nitrocellulose membrane (Hybond ECL
Nitrocellulose Membrane, Amersham Pharmacia Bio-
tech) in a Microfiltration Apparatus (Bio-Rad). The
membrane was placed in a 5% powdered milk blocking
solution overnight at 4 1C. After three 10-min washes
with PBS/Tween solution, a monoclonal mouse anti-
human TfR antibody (Zymed Laboratories, INC)
(dilution 1/1000) was applied for the detection of TfR
protein followed by three 10-min washes with PBS/
Tween solution. The blots were afterwards incubated
with an appropriate peroxidase-conjugated secondary
antibody (DAKO) (dilution 1/10000) followed again by
three 10-min washes with PBS/Tween solution. Visua-
lization of the immunologically detected proteins was
achieved using the SuperSignal West Femto detection
system (Pierce, Rockford, IL). Processed blots were
exposed to X-ray film and analyzed in the ChemiDoc
System (Bio-Rad). The amount of TfR protein was
assessed by the Quantity One Software (Bio-Rad). A
standard curve (0–400 ng/mL) (Ramco Laboratories,
Inc.) was run to determine the concentration of the TfR
protein in the sample.
Placental ferritin determination
Pl-Ft was measured by immunoradiometric assay
(Coat-A-Count Ferritin IRMA) (Diagnostic Products)
in the 21 000g placental homogenate supernatant.
Placental Fe content
Pl-Fe was measured by atomic absorption spectro-
metry (AAS) using the Smith-Hieftje 4000 instrument,
following wet-ashing in ultrapure nitric acid. The
National Bureau of Standard0 s bovine liver (1577a)
was used as a standard.
Statistical analysis
Statistical analysis was performed using Excel 6.0
(Microsoft, Seattle, WA, USA). Correlation analysis
(r, p) was performed for the association between each of
the measured variables. Data sets were compared
according to Student’s t test or Mann–Whitney test
when appropriate.
245
Table 2. Hematologic values in maternal venous blood just
before delivery
Hct (%) 3574 (26–43)
RBC  103/mm3 39487530 (2900–5300)
MCV (fL) 9075 (76–100)
Hb (g/L) 113716 (75–140)
WBC/mm3 10 08173433 (3500–17 800)
S-Ft (mg/L) 36742 (5–189)
sTfR (mg/L) 6.373.1 (2–16)
Values are means+SD (range).
MCV: mean corpuscular volume.
Results
Hct, Hb, sTfR, S-Ft and WBC count in maternal
venous blood just before delivery are shown in
Table 2. M Hb concentration was o110 g/L in 36%
of the women, while M sTfR was 48.3 mg/L in 23%
and M S-Ft was o10 mg/L in 20% of the women
(Fig. 1).
The mean values 7SD in the placenta were: Pl-TfR,
Pl-Ft and Pl-Fe concentrations: 18718; 33718 and
170756 mg/g placenta, respectively; placental weight:
5857105 g, with a range of 400–800 g; placental total
TfR, ferritin and Fe content: 10710; 20712 and
102744 mg, respectively. The distribution of total
Pl-TfR, Pl- Ft and Pl-Fe in the studied women is shown
in Fig. 2.
Correlation analysis showed that Pl-TfR correlated
inversely with placental total Fe content (r ¼ 0:43;
p ¼ 0:007) (Fig. 3a). Furthermore, the Pl-Ft content
correlated positively with the Pl-Fe content (r ¼ 0:392;
p ¼ 0:015) (Fig. 3b). However, Pl-TfR did not correlate
with Pl-Ft (Fig. 4).
No statistically significant correlations were found
between Pl-TfR, Pl-Ft or Pl-Fe total content or
concentration and maternal M Hb, M sTfR or M S-Ft.
Discussion
The Fe status of human placenta is important with
regard to nutrition of the developing fetus [14].
Pregnancy outcome in the studied group showed no
fetal growth impairment as infants’ birth weights were
adequate for gestational age and Apgar scores ranged
between 8 and 10, with a mean value of 9 (Table 1).
Although gestational age was o37 weeks in 3 out of 38
newborns, according to the guidelines of the Argentine
Society of Pediatrics, their body weights were within
normal values compared with a weight/age ratio
nomogram [15,16]. Pre-maturity was not due to
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246 S.H. Langini et al. / Journal of Trace Elements in Medicine and Biology 19 (2006) 243–249

40
Hb (g/L)
sTfR (mg/L)
35
S-Ft (ug/L)

30

25
% of women

20

15

10

0
10

0
2
32

3. 5
5. .0

8. 3
12

0
0
0
0
0
0
0
12
13

2.
3.

8.

>1

<1

-2
-3
-5
-7
-9
>9
5
<1

>1

4-
9-
6-
1-

11
21
31
51
71
0-
1-

<
2.
11
12

Fig. 1. Distribution of hemoglobin, soluble transferrin receptor and serum ferritin in maternal venous blood.

60
Pl- TfR (ug/g)
Pl-Ft (ug/g)
50 Pl-Fe (ug/g)

40
% of women

30

20

10

0
8
17

13

10

0
-2

-3

-4

-5

-3

-5

-7

-9

17

23

29
<
8-

-1
<
18

29

39

49

13

34

54

74

1-

1-

1-
50
11

17

23

Fig. 2. Distribution of transferrin receptor, ferritin and Fe in placenta samples at delivery.

maternal Fe deficiency as M Hb was 4120 g/L and M S- The fetus has a high requirement of Fe for normal
Ft and M sTfR were within normal ranges in the 3 development. In most mammalian species, fetal Fe is
mothers. derived from maternal transferrin Fe, which delivers Fe
 ARTICLE IN PRESS
S.H. Langini et al. / Journal of Trace Elements in Medicine and Biology 19 (2006) 243–249 247

70 70
y = -0.1372x + 41.689 y = 0.1082x + 8.5957
60 r= -0.43; p= 0.007 60 r= 0.392; p=0.015
Pl- TfR (µg/ g placenta)

50 50

Pl-Ferritin (mg)
40 40

30 30

20 20

10 10

0 0
0 50 100 150 200 250 300 0 50 100 150 200 250
(a) Pl- Fe (µg / g placenta) (b) Pl-Fe (mg)

Fig. 3. (a) Placental transferrin receptor and placental Fe. (b) Placental ferritin and placental Fe.

70 3
y = -0.9318Ln(x) + 5.2819
60 2.5
r = - 0.538
Pl-TfR (µg / g placenta)

50 2
Pl - TfR/Ft

40 1.5

30 1

20 0.5

10 0
0 50 100 150 200 250 300
0 Pl-Fe (µg/g placenta)
0 20 40 60 80 100
Pl-Ft (µg / g placenta) Fig. 5. Placental TfR/Ft ratio and placental Fe.

Fig. 4. Placental transferrin receptor and placental ferritin. this may be a mechanism that seems to provide a proper
amount of Fe to the fetus, reducing the risk of fetal Fe
deficiency or toxicity, probably playing a regulatory role
to TfR on the layer of fused cells that separates the in the process of Fe uptake by the placenta. In the
maternal and fetal circulation [17]. Placental tissue present study, although placental non-heme Fe was not
extracts have been used for the purification and determined, a similar correlation was observed between
biochemical characterization of TfR, as high amounts TfR, measured in placental tissue by the slot-blot
of TfR are present, particularly on the microvillous method, and Pl-Fe, as well as between Pl-Ft and Pl-Fe
surface of the syncytiotrophoblast. The Pl-TfR content supporting Bergamaschi’s results for the role of Pl-Fe
has been assayed indirectly in a study by Bergamaschi content in the expression of Pl-TfR and Pl-Ft protein
et al. [18] by evaluating the capacity of a placental (Figs. 3a and b). However, Pl-TfR and Pl-Ft were not
extract to bind diferric transferrin. However, in our correlated to each other (Fig. 4) suggesting that other
study, the Pl-TfR content was measured directly in factors also affect the expression of these proteins. The
placental homogenates by an immunodetection method serum transferrin receptor-ferritin ratio (TfR/Ft) pro-
(slot-blotting) [12] using a monoclonal mouse anti- posed by Cook et al. [3] as an indicator of Fe stores was
human TfR antibody. This methodology does not calculated for the placental tissue in this study, giving
appear to have been undertaken previously for the an inverse correlation to total Fe content (r ¼ 0:538)
measurement of the TfR protein in placental tissue. (Fig. 5). The correlation between TfR/Ft and Pl-Fe is
In the study by Bergamaschi et al. [18], the amount of mostly due to the increase in Pl-TfR at lower Pl-Fe
TfR in the placenta was found to be inversely correlated concentrations.
to the amount of non-heme Fe, which represents the Early studies found that maternal serum Fe in
storage form of this element. The authors suggested that maternal hypoferremia is positively correlated with
 ARTICLE IN PRESS
248 S.H. Langini et al. / Journal of Trace Elements in Medicine and Biology 19 (2006) 243–249

placental tissue Fe concentration [19], suggesting that 100

the placenta extracted Fe in amounts proportional to M Hb > 110 g/L
90 M Hb < 110 g/L
circulating levels in the mother. In the present study, no
correlation was found between Pl-TfR, Pl-Ft and Pl-Fe 80
and maternal Hb, sTfR and S-Ft. These results may be
70
related to the limited sample size which did not allow
comparisons across a wider spectrum of placental Fe 60

Pl-Ft (µg /g)

indicators.
As shown in Fig. 2, the distribution of TfR, Ft and Fe 50
in the placenta samples was not Gaussian. Besides, no 40
cut-off points or reference values regarding placental Fe
indicators are available. Therefore, in order to elucidate a 30
relationship between placental and maternal Fe status, 20
Hb, sTfR and S-Ft were compared above and below
Pl-Fe, Pl-Ft and Pl-TfR median values. Women with Pl- 10 p = 0.021
Fe, Pl-Ft and Pl-TfR above or below the corresponding 0
median values, did not show any statistical significant
difference in M Hb, M sTfR or M S-Ft values (Table 3). Fig. 6. Placental ferritin in women with hemoglobin values
However, the arbitrary choice of a midpoint may obscure above and below the cut-off point.
associations between maternal and placental indicators.
Moreover, Pl-TfR, Pl-Ft and Pl-Fe were compared in significant difference was found for Pl-TfR, neither for
women with M Hb, M S-Ft and M sTfR above and Pl-Ft nor Pl-Fe.
below the corresponding cut-off points, Pl-Ft was lower Furthermore, no significant differences were found
(p ¼ 0:021) in women with low M Hb values than in between Pl-TfR, Pl-Ft or Pl-Fe in women with M sTfR
women with normal values at delivery: 26713 vs. concentrations above or below 8.3 mg/L, according to
38720 mg/g placenta, respectively (Fig. 6). the normal range for M sTfR in healthy male and female
The appropriate cut-off point for M S-Ft is con- volunteers, as measured by the Ramco TfR assay. Choi
troversial and may be affected by infections or et al. studied sTfR concentrations during normal
inflammation. As shown in Table 2, WBC count was pregnancy by ELISA (Orion Diagnostica) [22]. They
in the normal range accepted during the puerperium reported an sTfR reference interval of 3.52–5.94 mg/L
[20], therefore ferritin values would not be affected. for the 3rd trimester of pregnancy. No significant
Recent results of our group in pregnant women after differences were found between Pl-TfR, Pl-Ft or Pl-Fe
delivery showed that M S-Ft correlated inversely with M in women with sTfR concentrations above or below
sTfR and with sTfR/SF ratio when the WBC count was 5.94 mg/L.
in the range of the present study [21]. When Pl-TfR, The results of the present study suggest that, at
Pl-Ft and Pl-Fe were compared in women with M S-Ft delivery, low maternal Hb levels (o110 g/L) are
above or below the cut-off point of 10 or 20 mg/L, no associated with a decrease in Pl-Ft concentration. This
finding may be in agreement with an increased efficiency
of transfer of Fe to the fetus rather than to the placenta
Table 3. Maternal hemoglobin, soluble transferrin receptor in maternal Fe deficiency, as hypothesized by Gambling
and serum ferritin in women with values above and below et al. in an experimental rat model [23], and occurs in
median placental iron, ferritin and transferrin receptor spite of the detriment for maternal erythropoiesis.
concentrations Moreover, data on transplacental transfer of B vitamins
suggests that the placenta extracts these essential
Median values M Hb (g/L) M sTfR (mg/L) M S-Ft (mg/L) micronutrients from the maternal circulation and
Pl-Feo159 mg/g 113714 6.072.7 44771 redistributes them, probably favouring the fetus [24].
Pl-Fe4159 mg/g 114719 6.673.4 35744 Overall, our results suggest that maternal sTfR and
p value 0.426 (ns) 0.277 (ns) 0.433 (ns) S-Ft do not reflect Fe status of the placenta at delivery,
Pl-Fto28 mg/g 110718 6.272.6 36746 although low maternal Hb may decrease placental Fe
Pl-Ft428 mg/g 117713 6.373.6 36739 stores.
p value 0.086 (ns) 0.457 (ns) 0.499 (ns)
Pl-TfRo15 mg/g 115714 6.373.0 40739
Pl-TfR415 mg/g 111719 6.373.2 31746 Acknowledgements
p value 0.222 (ns) 0.487 (ns) 0.271 (ns)

Values are means7SD. We are grateful to Dr. Marcelo Piñero for helping
ns: not significant. collecting the placenta and mother’s blood samples; to
 ARTICLE IN PRESS
S.H. Langini et al. / Journal of Trace Elements in Medicine and Biology 19 (2006) 243–249
Shannon Kelleher, Michel Crane and Weng-In-Leon for
their technical assistance.
Supported by grant UBA (University of Buenos
Aires) TB060 & B009, Argentina.
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