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European Journal of Obstetrics & Gynecology and Reproductive Biology 150 (2010) 126–131

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European Journal of Obstetrics & Gynecology and


Reproductive Biology
journal homepage: www.elsevier.com/locate/ejogrb

Prevalence and risk factors for early postpartum anemia


Renate L. Bergmann *, Rolf Richter, Karl E. Bergmann, Joachim W. Dudenhausen
Department of Obstetrics, Charité University Medicine, Augustenburger Platz 1, 13353 Berlin, Germany

A R T I C L E I N F O A B S T R A C T

Article history: Objective: To assess the prevalence and evaluate the most important risk factors for early postpartum
Received 8 June 2009 anemia.
Received in revised form 29 January 2010 Study design: The perinatal process data of 43 807 women delivering between 1993 and 2008 (90.1% of
Accepted 10 February 2010
all deliveries) in the largest university obstetric department in Germany were analyzed, and the
associations of Hb < 8 g/dl with maternal characteristics, pregnancy risks, delivery mode and estimated
Keywords: delivery blood loss were calculated. Multivariable logistic regression models were applied to compute
Early postpartum anemia
odds ratios. Additionally, the impact of these risk factors for delivery blood loss was estimated with
Obstetric blood loss
Iron deficiency
multivariable linear regression analysis.
Results: Twenty-two percent of mothers had Hb < 10 g/dl, and 3% had Hb < 8 g/dl. The adjusted odds
ratios (OR) for Hb < 8 g/dl were 4.8 (p = 0.001) for placenta previa, 2.9 (p < 0.001) for mothers of African
origin, 2.7 (p < 0.001) for diagnosed anemia in pregnancy, 2.2 (p < 0.001) for multiple pregnancy, and 2.1
(p = 0.021) for bleeding in late pregnancy. However, the delivery blood loss was the most important risk
factor for postpartum anemia. The adjusted OR for an estimated blood loss of 500–1000 ml was 15.3
(p < 0.001), and for a loss of >1000 ml was 74.7 (p < 0.001).
Conclusion: The estimated obstetric blood loss is the most important risk factor for severe postpartum
anemia, and the volume of blood lost is especially high in cesarean deliveries, which should be
considered when electing delivery procedures. Also, measures to boost iron stores in pregnancy should
be established.
ß 2010 Elsevier Ireland Ltd. All rights reserved.

1. Introduction States showed increasing rates from 12.2 to 15.6% during the years
1998 through 2003 [12].
Iron deficiency and anemia in pregnancy are prevalent even in Most mothers recover from postpartum anemia during the
developed countries [1–3]. In contrast, the postpartum period is weeks or sometimes months after delivery. But when recovery
considered to be characterized by physiologically low iron takes a long time, e.g. with an unfavorable baseline Hb around
requirements, particularly because the expanded red cell mass delivery, functional consequences of iron deficiency and anemia
contracts after delivery, and its iron can be utilized and stored [4]. may appear or worsen: depressive symptoms, deficits in cognitive
But low iron stores during pregnancy may be carried over into the function, fatigue, lower work performance, impaired immune
postpartum period, and therefore iron supplements after delivery function [13,14]. Also, poorer functioning of mother–child inter-
enhance the postpartum recovery of hematological values [5–7]. action and even delayed infant development were related to
However, these physiological regulations, the underlying nutri- maternal postpartum iron deficiency anemia [15,16].
tional deficits and their control will be overridden by obstetric In view of these consequences, it is important to monitor the
hemorrhage, which is not a rare event even in developed countries, prevalence and time trends of postpartum anemia in any setting,
and presents the major risk factor for maternal deaths in and to evaluate the most important risk factors for low hemoglobin
developing countries [8–10]. In 2003, around 6% of pregnancy- values after delivery.
related hospital discharges in the USA had a diagnosis of obstetric
bleeding, and one in five of them an anemia diagnosis [10]. In 2. Methods
Australia the rate of obstetric hemorrhage was estimated to
amount to 13.1% of deliveries [11]. The prevalence of postpartum The Virchow Hospital of the Charité University Medicine is
anemia (Hb < 10 g/dl) on discharge in one of the German Federal located in a low income district of Berlin with a high fluctuation
rate, which is the prevailing catchment area of our obstetric
department, the largest in Germany. The perinatal process data are
* Corresponding author. Tel.: +49 30 450 564 101; fax: +49 30 450 564 908. collected and electronically stored in the hospital documentation;
E-mail address: renate.bergmann@charite.de (R.L. Bergmann). most of them are collected on a standard form for the purpose of

0301-2115/$ – see front matter ß 2010 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.ejogrb.2010.02.030
R.L. Bergmann et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 150 (2010) 126–131 127

Fig. 1. Distribution of hemoglobin concentrations the first day after delivery (n = 43 807 deliveries).

bench marking obstetric wards in Berlin regarding their clinical volume lost as a continuous variable, according to pregnancy risk
performance. Medical history data were transferred from the factors and mode of delivery The data were analyzed with SPSS
record of pregnancy care (filled in during antenatal care by 14.0 (SPSS Inc., Chicago, IL), and p < 0.05 was considered
practicing gynecologists), and medical history, obtained at statistically significant.
admission, as well as delivery and birth characteristics were
electronically recorded by our obstetric team. The term ‘‘nullipar- 3. Results
ity’’ in the records of pregnancy care was changed to ‘‘primiparity’’
in the electronic record after delivery, but we used the term The distribution of postpartum Hb, and the percentile values
‘‘primiparity’’ throughout. were skewed to the left with a mean of 11.0 g/dl and a median of
The data were checked twice before they were compiled and 11.2 g/dl (Fig. 1). About one in five women was anemic (Hb < 10 g/
stored. We received the data for the period 01 April 1993 through dl), and one in 30 was severely anemic (Hb < 8 g/dl) on the second
31 March 2008 from our IT department on 48 623 deliveries of day after delivery. The prevalence of anemia increased slightly and
40 263 women, containing basic characteristics of the mothers, significantly over the observed time period, while there was no
recorded pregnancy risks, and main characteristics of the delivery significant change in severe anemia (Fig. 2).
and of the newborn. Some mothers had delivered repeatedly in our
hospital, and therefore were recorded several times, according to 3.1. Univariable analysis
the number of their deliveries. Our evaluation is based on
deliveries or births. Hb values were available on 43 807 mothers Data over the observed 16 years were combined and associa-
after delivery (90.1% of deliveries), determined from venous blood tions calculated between low postpartum Hb values and different
sampled on the morning of the second postpartum day, i.e. factors of potential influence. There was no significant association
between 24 and 48 h, with an automated analyzer (Cell Dyn 3500) between low Hb values on one hand, and marital status, diabetes,
by our central clinical laboratory. Anemia was defined as an Hb anticipated hemorrhage risk, history of recurrent abortions, short
below 10.0 g/dl, and severe anemia as a value below 8.0 g/dl [17]. birth spacing, fetal malpresentation, and nicotine or alcohol
Blood loss at delivery was visually estimated and recorded by dependency, on the other (data not shown). Other factors turned
the delivery team from the staining of sheets, pads, containers and out to be significantly associated at least with Hb values < 8 g/dl
other materials used during delivery and in the delivery area, by (Table 1): young, short, non-German and primiparous mothers,
rules passed from one team to the other over the years. with an anemia diagnosis in pregnancy, bleeding after 28
Mothers were observed postpartum for about 2 h in the pregnancy weeks, placenta previa, hypertension, multiple preg-
delivery area, before they were transferred to the ward. Any nancy, and those delivering prematurely or post-term, assisted or
complication with larger blood loss postponed their transfer, and
the respective blood loss was added to the total loss.

2.1. Statistical methods

The associations of anemia or severe anemia with maternal


characteristics, pregnancy risks from the record of pregnancy care,
delivery mode and estimated delivery blood loss were univariably
assessed by chi2-test for nominal data and by Kendall’s tau b for
ordinal data, and by multivariable logistic regression analysis.
Odds ratios (OR) adjusted for all other influential variables were
calculated. The variables were entered into the equation in four
blocks: first maternal characteristics, second antenatal history,
pregnancy risks, and newborn characteristics, third mode of
delivery, and fourth estimated delivery blood loss. Less important
risk factors of the univariable analysis were excluded. Multi- Fig. 2. Secular trend in the prevalence of low values and anaemia immediately after
variable linear regression analysis was applied to estimate blood delivery. Hb < 10 g/dl: p < 0.001, Hb < 8 g/dl: n.s.
128 R.L. Bergmann et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 150 (2010) 126–131

Table 1
Prevalence of low postpartum hemoglobin (Hb < 8 g/dl) according to parameter values. Odds ratios (OR) and their significance (p) for Hb < 8 g/dl by risk factors I n
multivariable logistic regression. Model 1 shows the results for maternal characteristics, pregnancy risks, birth outcomes, and delivery mode, and model 2 delivery blood loss
additionally to the other factors. p in first line applies to the difference of all parameter values, p in respective line to the difference against the reference group (Ref.) of each
parameter category. ns = non-significant. n = 43 807.

Hb < 8 g/dl Model 1 Model 2

% p OR p OR p

Age mother [years] ns 0.044 0.005


<18 (Ref.) 4.6 1 1
18–35 3.4 0.702 0.082 0.620 0.023
>35 3.1 0.601 0.020 0.503 0.003

Height mother [cm] <0.001 <0.001 <0.001


<160 (Ref.) 3.8 1 1
161–170 3.2 0.798 0.001 0.768 0.000
>170 2.8 0.680 0.000 0.616 0.000

Pregnancy weight gain [kg] <0.05 0.454 0.346


0 4.2 1.453 0.185 1.423 0.236
1–10 3.2 1.065 0.390 1.089 0.265
11–15 (Ref.) 3.1 1 1
16–20 3.3 0.979 0.784 0.939 0.437
>20 4.1 1.100 0.324 1.046 0.658

Nationality <0.001 <0.001 <0.001


German (Ref.) 3.1 1 1
Turkish/Near East 3.4 1.293 0.000 1.473 0.000
Africa 8.4 2.891 0.000 2.684 0.000
Other 3.6 1.149 0.093 1.180 0.054

Anemia in pregnancy 10.1 <0.001 2.675 <0.001 2.724 <0.001


Hemorhage/thrombosis risk 5.0 ns 1.749 0.013 1.519 0.079
Bleeding > 28 [weeks] 8.5 <0.01 2.097 0.021 1.896 1.896
Placenta previa 17.8 <0.001 4.835 <0.001 2.527 0.004
Hypertension 5.1 <0.05 1.204 0.419 1.013 0.957

Parity <0.001 0.001 0.001


1 4.0 1.234 1.236
1 (Ref.) 2.8 1 1

Multiple pregnancy 7.7 <0.001 2.247 <0.001 1.539 0.001

Pregnancy duration [weeks] <0.001 0.074 0.451


Term (37–41) 3.1 1 1
Premature (<37) 4.5 1.220 0.082 1.148 0.254
Post-term (>41) 4.5 1.211 0.121 1.080 0.555

Birth weight [g] <0.001 <0.001 0.024


<2500 (Ref.) 4.2 1 1
2500–4000 3.1 1.171 0.282 1.126 0.445
>4000 4.6 1.806 0.001 1.487 0.034

Newborn length [cm] <0.001 0.090 0.327


45 (Ref.) 4.3 1 1
46–54 3.2 0.920 0.609 0.811 0.222
55 4.5 1.158 0.033 1.102 0.388

Delivery mode <0.001 <0.001 <0.001


Vaginal (Ref.) 2.2 1 1
Manual support/extraction 1.9 1.048 0.927 0.787 0.650
Vacuum 7.9 3.627 0.000 2.361 0.000
Forceps 7.7 3.850 0.000 2.509 0.000
Elective cesarean 4.5 1.883 0.000 0.909 0.382
Emergency cesarean 5.1 2.055 0.000 0.936 0.462

Blood loss [ml] <0.001 <0.001


<250 (Ref.) 1.0 1
251–500 3.3 3.278 0.000
501–1000 13.0 15.263 0.000
>1000 43.6 74.670 0.000

by operation, and with a high estimated blood loss, were Table 1): mothers of African origin had the highest risk of becoming
significantly more often anemic. Pregnancy weight gain and anemic after delivery. Of the pregnancy risk factors and birth
weight or length of the newborn showed a U-shaped association outcomes, placenta previa increased the postpartum anemia risk
with low Hb values. about fivefold. A diagnosis of anemia in pregnancy increased it
Because many of the risk factors in the univariable analysis nearly threefold; multiple pregnancy, bleeding after 28 weeks, and
were interrelated, we conducted a multivariable analysis to a high birthweight nearly twofold. Compared to spontaneous
simultaneously evaluate the importance of the risk factors for a deliveries, cesarian deliveries increased the anemia risk twofold,
mother to have a postpartum Hb < 8 g/dl (Table 1). Some of the and vacuum or forceps deliveries nearly fourfold (model 1 in
maternal characteristics were related to severe anemia (model 1 in Table 2).
R.L. Bergmann et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 150 (2010) 126–131 129

Fig. 3. Distribution of estimated delivery blood loss (n = 43 807 deliveries).

Model 2 in Table 1 introduces estimated delivery blood loss as after adjustment cesarean was no longer an independent factor for
an independent variable: after adjusting for the estimated delivery severe anemia in our data set (model 2 in Table 1).
blood loss, some of the other risks were displaced downward. But In view of the importance of the estimated delivery blood loss
forceps and vacuum extraction remained factors of high risk, while for the risk of immediate postpartum anemia, we explored the
estimated blood loss (Fig. 3). One percent of mothers lost more
Table 2
than 1000 ml. In a multivariable linear regression analysis we
Multivariable regression analysis for the change in delivery blood loss (in ml)
compared to the reference group (Ref.) of each parameter. B: regression coefficient
evaluated the additional volume (ml) of blood lost in the risk group
(blood loss change in ml); Beta: standardized regression coefficient; p: probability. compared to the respective reference group, simultaneously
n = 43 807. adjusting for the other factors (Table 2). Although multiple
Influential variable B [ml] Beta p
pregnancy remained an important risk factor, placenta previa
and operative deliveries were the most important factors for an
Age of mother [years], <18 (Ref.)
obstetric blood loss exceeding the blood loss under normal
18–35 0.05 0.000 0.989
>35 3.18 0.006 0.372 conditions. Especially high was the blood volume lost with
emergency and elective cesarean deliveries, which means more
Height of mother [cm], <160 (Ref.)
than 200 ml compared to uncomplicated deliveries.
161–170 5.68 0.015 0.012
>170 8.92 0.021 0.001 By adding the delivery mode to the other factors in the final
model, the explained proportion of the overall variance in obstetric
Pregnancy weight gain [kg], 11–15 (Ref.)
0 3.93 0.009 0.053
blood loss increased from 7.2 to 24.4%. The high beta value for
1–10 4.92 0.011 0.023 operative deliveries indicates that they are not only important but
16–20 6.63 0.010 0.026 also prevalent risk factors for the estimated delivery blood loss.
>20 11.46 0.026 <0.001 The rate of operative deliveries increased over the observed
Nationality, German (Ref.) time period, for cesarean deliveries from 18.5% in 1993 to 30.8% in
Turkish/Near East 23.56 0.016 <0.001 2008 (p < 0.001). The rate of vacuum deliveries remained constant
African 0.26 0.000 0.023 at around 9%, while the forceps delivery rate decreased signifi-
Other 6.08 0.003 0.026
cantly to 0.1% in 2008 (p < 0.001). On the other hand, we found no
Primiparity 5.23 0.002 <0.001 time trend for an estimated obstetric blood loss over 1000 ml, but a
Anemia in pregnancy 5.23 0.002 0.628 decreasing trend for an estimated blood loss between 501–
Heamorrhage/thrombosis risk 31.84 0.017 <0.001
1000 ml (p = 0.002), and for 251–500 ml (p < 0.001), while a low
History of 2 abortions 8.58 0.013 0.002
Bleeding < 28 weeks 29.63 0.017 <0.001 estimated blood loss of <250 ml occurred significantly more often
Bleeding > 28 weeks 16.90 0.005 0.208 from year to year (p < 0.001).
Placenta praevia 206.01 0.053 <0.001 To get an impression of the distribution of Hb values in low risk
Hypertension 19.59 0.011 0.011
mothers, we excluded mothers with an estimated blood loss over
Multiple pregnancy 78.87 0.074 <0.001
Premature (<37 weeks) 8.05 0.014 0.020
500 ml (90th percentile), and mothers with operative delivery,
Post-term (>42 weeks) 16.68 0.018 <0.001 with anemia in pregnancy and with placenta previa. The mean Hb
in these low risk mothers was only slightly higher than in the total
Birth weight [g], 2500–4000 (Ref.)
<2500 7.18 0.015 0.105 sample, i.e. 11.4 (1.4) g/dl vs.11.0 (1.5) g/dl. However, in the low
>4000 30.89 0.046 <0.001 risk mothers the prevalence of low values was markedly reduced:
Hb < 8 g/dl occurred in 1.3% instead of 3.4%, and Hb < 10 g/dl in
Birth length [cm], 46–54 (Ref.)
45 13.11 0.016 0.009 13.9% instead of 22.7%.
55 18.24 0.026 <0.001
4. Comment
Delivery mode, vaginal (Ref.)
Extraction/manual support 27.15 0.010 0.021
Vacuum 80.07 0.117 <0.001 The main strength of this study is the large sample size
Forceps 73.02 0.050 <0.001 originating from a single institution, which means that policies and
Elective cesarean 208.51 0.298 <0.001
procedures were likely to be more consistent than when they come
Emergency cesarean 217.07 0.373 <0.001
from multiple institutions. However, it cannot be expected that the
130 R.L. Bergmann et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 150 (2010) 126–131

precision of process data, which in our case was collected for Carolina [29]. The other risk factors in this prospective study were
clinical bench marking, can be as high as standards for prospective similar to our findings. According to the present study, only 0.6% of
studies. Especially the estimation of obstetric blood loss in a mothers came in with a diagnosis of ‘‘anemia during pregnancy’’, a
clinical setting is imprecise, and underestimation up to 50% may prevalence that probably is highly underestimated by our
occur, although training can somewhat improve the precision [18– practicing gynecologists. Our own findings showed that in 1999,
21]. Additionally, our data file did not include all important of around 400 mothers coming in for delivery 3.6% were anemic,
predictors for obstetric hemorrhage, like preeclampsia, duration of and 41% were iron deficient [3].
labor, episiotomy, uterine atony, retained placenta or treatment A diagnosis of anemia in women with obstetric bleeding was
procedures like blood transfusions [9,22]. Nevertheless, it is associated with increased costs for hospitalization beside the
possible to get some insight into the prevalence of such a adverse impact on postpartum health status [10]. Treatment of
significant clinical problem as post delivery anemia and to delivery blood loss is cost intensive, and prevention is usually less
recognize attributable risk factors. expensive. As the volume of blood lost is closely related to labor
Hb values below 10 g/dl during the second postpartum day management, especially with cesarean deliveries, potential blood
were found in 22% of mothers, i.e. about one in five mothers was loss should be included in the decisions on delivery procedures.
anemic according to this definition, with a slightly increasing trend Also, measures to boost iron stores before and during pregnancy
over the years. Severe anemia, which was defined as Hb < 8 g/dl, should be implemented [2,4,5].
was found in around 3% of the mothers, and the trend did not
change significantly. Since we did not receive Hb values in 10% of Conflicts of interest
mothers because they were discharged early after uncomplicated
deliveries, the anemia prevalence may be slightly overestimated. No conflicts of interest.
There are marked changes in fluid dynamics after delivery, and
therefore for Hb determinations between 24 and 48 h after Contributions
delivery, a cut-off value of 8 g/dl is probably more predictive of
sustained anemia than the traditional postpartum anemia thresh- Prof. Dr. med. Renate L. Bergmann wrote the manuscript, all of
old of 10.0 g/dl [23]. We used Hb < 8 g/dl for the multivariable the authors participated in the interpretation of the data, in
analysis. In Germany, the prevalence of cesarean deliveries repeated critical revisions of the manuscript, and in the final
increased from 18% in 1995 to 28% in 2005 [24]. Although our approval. Dr. Rolf Richter performed the statistical analysis and
large obstetric department is part of a high risk perinatology produced the figures.
center, it has a relatively low cesarian rate, comparable to the
overall rate in Germany. Given the increase in cesarean deliveries, Ethical approval
the declining obstetric blood loss in our department may explain
why we found a nearly constant rate for severe anemia over the Not required for the analysis of anonymised process data.
years.
A blood loss over 500 ml was observed in 13.1% of all deliveries
Funding
in New South Wales, Australia, compared to 7.9% of the deliveries
in our institution, which could be due to underestimation in our
Supported by a Grant to the Charité University Hospitals Berlin
data [11]. On the other hand, among all mothers delivering in
by Vifor Pharma, Germany.
Norway from 1999 to 2004, severe obstetric hemorrhage of
>1500 ml (delivery to 24 h postpartum) occurred in only 1.1%,
Acknowledgements
which is closer to our value, and similar risk factors as in our study
were observed [22]. In both studies cesarean deliveries had a
We thank the obstetric teams of our department for their
higher odds ratio for severe obstetric hemorrhage than forceps and
persistently devoted work!
vaginal deliveries. But surprisingly, we found higher postpartum
anemia rates after forceps and vacuum deliveries than after
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