Prediction of Hemorrhage in Placenta Previa - Taiwanese Journal of Obstetrics & Gynecology
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This article reviews ultrasonographic findings associated with the prediction of massive bleeding in cases of placenta previa, which poses a high risk for massive hemorrhage, from the antenatal period until after Cesarean section. The article discusses the mechanisms of hemorrhage resulting from placenta previa during pregnancy and the risk of massive bleeding during Cesarean section. The article also reviews the prenatal prediction of sudden bleeding during pregnancy and blood loss during Cesarean section, and the assessment of risk for adherence of the placenta using an ultrasound examination, which can improve the perinatal outcome.
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Prediction of hemorrhage in placenta previa
Article in Taiwanese journal of obstetrics & gynecology · March 2012
DOI: 10.1016/j.tjog.2012.01.002 · Source: PubMed
CITATIONS
13
READS
313
7 authors, including:
Some of the authors of this publication are also working on these related projects:
placentaView project
prenatal diagnosisView project
Junichi Hasegawa
St. Marianna University School of Medicine
168PUBLICATIONS999CITATIONS
SEE PROFILE
Masamitsu Nakamura
Showa University
93PUBLICATIONS654CITATIONS
SEE PROFILE
Ryu Matsuoka
Showa University
114PUBLICATIONS1,150CITATIONS
SEE PROFILE
Kiyotake Ichizuka
Showa University
117PUBLICATIONS1,055CITATIONS
SEE PROFILE
Prediction of hemorrhage in placenta previa
Article in Taiwanese journal of obstetrics & gynecology · March 2012
DOI: 10.1016/j.tjog.2012.01.002 · Source: PubMed
CITATIONS
13
READS
313
7 authors, including:
Some of the authors of this publication are also working on these related projects:
placentaView project
prenatal diagnosisView project
Junichi Hasegawa
St. Marianna University School of Medicine
168PUBLICATIONS999CITATIONS
SEE PROFILE
Masamitsu Nakamura
Showa University
93PUBLICATIONS654CITATIONS
SEE PROFILE
Ryu Matsuoka
Showa University
114PUBLICATIONS1,150CITATIONS
SEE PROFILE
Kiyotake Ichizuka
Showa University
117PUBLICATIONS1,055CITATIONS
SEE PROFILE
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Review Article
Prediction of hemorrhage in placenta previa
Junichi Hasegawa*, Masamitsu Nakamura,Shoko Hamada,Ryu Matsuoka,Kiyotake Ichizuka,
Akihiko Sekizawa,Takashi Okai
Department of Obstetrics and Gynecology,Showa University School of Medicine,Tokyo,Japan
Accepted 18 October 2011
Abstract
Placenta previa poses a high risk for massive hemorrhage, from the antenatal period until after Cesarean section. This c
risk of maternal and neonatal mortality and morbidity. In cases of placenta previa, the prenatal prediction of sudden bleed
and blood loss during Cesarean section, and the assessment of risk for adherence of the placenta using an ultrasound exa
the perinatal outcome.Therefore,ultrasonographic findings associated with the prediction of massive bleeding in cases of placen
reviewed in this article.
Copyright Ó 2012,Taiwan Association of Obstetrics & Gynecology.Published by Elsevier Taiwan LLC.All rights reserved.
Keywords: placenta previa; Cesarean section; bleeding; ultrasound; placenta accreta
Introduction
Placenta previa increases the risk of maternal and neonatal
mortality and morbidity due to massive hemorrhage. Problems
of massive bleeding associated with placenta previa occur not
only during pregnancy,but also at and shortly afterthe
Cesarean operation.The morbidities associated with placenta
previa include hysterectomy [relative risk (RR) ¼ 33.26, 95%
confidence interval (CI) ¼ 18.19e60.89], antepartum bleeding
(RR ¼ 9.81, 95% CI ¼ 8.92e10.79), intrapartum (RR ¼ 2.48,
95% CI ¼ 1.55e3.98),and postpartum (RR ¼ 1.86,95%
CI ¼ 1.46e2.36) hemorrhages,as well as the need for blood
transfusion (RR ¼ 10.05,95% CI ¼ 7.45e13.55) [1].
Prenatal assessment of factors associated with a high risk of
excessive blood loss during pregnancy, and around the Cesarean
section,would improvethe preparationand management
of surgery,including the necessity for admission to hospital,
preservation of autologous blood, and the timing of the Cesarean
section.Therefore,in this article,we review and discuss the
ultrasonographic findings that can be used to predict a m
hemorrhage associated with placenta previa.
Hemorrhage during pregnancy
The mechanismsof hemorrhage resulting from placenta
previa during pregnancy are notclearly known.However,
when the placenta is present in a low uterine segment, it
easily detached from the decidua basalis,even when only
slightuterine contraction and effacementoccur.Abnormal
placentation and a poor blood supply from the uterine wa
the lower segmentof the uterus,may lead to active hemor-
rhage during pregnancy.
In our experience,an emergency Cesarean section was
needed due to uncontrollable hemorrhage in 66.7% of pa
who had antenatal bleeding.An emergency Cesarean section
was performed in 3.2% ofpatients who had no episode of
antenatal bleeding,due to uncontrollable uterine contraction
before the date of the planned Cesarean section [2].Thus,it
would improve the antenatalmanagementof patientswith
placenta previa if the risk of bleeding during pregnancy c
be predicted.
Saitoh et al [3] demonstrated that the risk of antenata
hemorrhage is higher (83.3%) in cases with an echo-free
* Corresponding author.Department of Obstetrics and Gynecology,Showa
UniversitySchool of Medicine,1-5-8 Hatanodai,Shinagawa-ku,Tokyo
142-8666, Japan.
E-mail address: hasejun@oak.dti.ne.jp (J.Hasegawa).
Available online at www.sciencedirect.com
Taiwanese Journal of Obstetrics & Gynecology 51 (2012) 3e6
www.tjog-online.com
1028-4559/$ - see front matter Copyright Ó 2012,Taiwan Association of Obstetrics & Gynecology.Published by Elsevier Taiwan LLC.All rights reserved.
doi:10.1016/j.tjog.2012.01.002
Prediction of hemorrhage in placenta previa
Junichi Hasegawa*, Masamitsu Nakamura,Shoko Hamada,Ryu Matsuoka,Kiyotake Ichizuka,
Akihiko Sekizawa,Takashi Okai
Department of Obstetrics and Gynecology,Showa University School of Medicine,Tokyo,Japan
Accepted 18 October 2011
Abstract
Placenta previa poses a high risk for massive hemorrhage, from the antenatal period until after Cesarean section. This c
risk of maternal and neonatal mortality and morbidity. In cases of placenta previa, the prenatal prediction of sudden bleed
and blood loss during Cesarean section, and the assessment of risk for adherence of the placenta using an ultrasound exa
the perinatal outcome.Therefore,ultrasonographic findings associated with the prediction of massive bleeding in cases of placen
reviewed in this article.
Copyright Ó 2012,Taiwan Association of Obstetrics & Gynecology.Published by Elsevier Taiwan LLC.All rights reserved.
Keywords: placenta previa; Cesarean section; bleeding; ultrasound; placenta accreta
Introduction
Placenta previa increases the risk of maternal and neonatal
mortality and morbidity due to massive hemorrhage. Problems
of massive bleeding associated with placenta previa occur not
only during pregnancy,but also at and shortly afterthe
Cesarean operation.The morbidities associated with placenta
previa include hysterectomy [relative risk (RR) ¼ 33.26, 95%
confidence interval (CI) ¼ 18.19e60.89], antepartum bleeding
(RR ¼ 9.81, 95% CI ¼ 8.92e10.79), intrapartum (RR ¼ 2.48,
95% CI ¼ 1.55e3.98),and postpartum (RR ¼ 1.86,95%
CI ¼ 1.46e2.36) hemorrhages,as well as the need for blood
transfusion (RR ¼ 10.05,95% CI ¼ 7.45e13.55) [1].
Prenatal assessment of factors associated with a high risk of
excessive blood loss during pregnancy, and around the Cesarean
section,would improvethe preparationand management
of surgery,including the necessity for admission to hospital,
preservation of autologous blood, and the timing of the Cesarean
section.Therefore,in this article,we review and discuss the
ultrasonographic findings that can be used to predict a m
hemorrhage associated with placenta previa.
Hemorrhage during pregnancy
The mechanismsof hemorrhage resulting from placenta
previa during pregnancy are notclearly known.However,
when the placenta is present in a low uterine segment, it
easily detached from the decidua basalis,even when only
slightuterine contraction and effacementoccur.Abnormal
placentation and a poor blood supply from the uterine wa
the lower segmentof the uterus,may lead to active hemor-
rhage during pregnancy.
In our experience,an emergency Cesarean section was
needed due to uncontrollable hemorrhage in 66.7% of pa
who had antenatal bleeding.An emergency Cesarean section
was performed in 3.2% ofpatients who had no episode of
antenatal bleeding,due to uncontrollable uterine contraction
before the date of the planned Cesarean section [2].Thus,it
would improve the antenatalmanagementof patientswith
placenta previa if the risk of bleeding during pregnancy c
be predicted.
Saitoh et al [3] demonstrated that the risk of antenata
hemorrhage is higher (83.3%) in cases with an echo-free
* Corresponding author.Department of Obstetrics and Gynecology,Showa
UniversitySchool of Medicine,1-5-8 Hatanodai,Shinagawa-ku,Tokyo
142-8666, Japan.
E-mail address: hasejun@oak.dti.ne.jp (J.Hasegawa).
Available online at www.sciencedirect.com
Taiwanese Journal of Obstetrics & Gynecology 51 (2012) 3e6
www.tjog-online.com
1028-4559/$ - see front matter Copyright Ó 2012,Taiwan Association of Obstetrics & Gynecology.Published by Elsevier Taiwan LLC.All rights reserved.
doi:10.1016/j.tjog.2012.01.002
![Document Page](https://desklib.com/media/document/docfile/pages/hemorrhage-placenta-previa/2024/09/08/95768076-d749-4e66-944b-6e2b62643a6f-page-3.webp)
the placentaledge overlying the internalos compared to the
other locations (7.7e10%).They suggested that the echo-free
space in the marginal area of the placenta (an area associated
with a turbulentblood flow)was either a placentalsinus or
varices thatdeveloped in the decidualtissue.Our previous
retrospective study also demonstrated that in ultrasonographic
findings at 20 weeks of gestation, the frequency of a marginal
sinus (similar to the findings reported by Saitoh et al [3]) was
slightly higher (16%) in cases with bleeding episodes compared
to those without(0%) [2]. Although the pathophysiological
changes associated with the marginal sinus have not been well
clarified,we hypothesized thatan expanded marginalsinus
indicates the retention of maternal blood flow in the intervillous
space and decidualtissue,which may collapse occasionally
due to uterine contraction,thus resulting in a large amount of
hemorrhage during pregnancy.
Contractions, cervical effacement, and dilatation during the
third trimester, may cause the separation of the placenta, leading
to unavoidableabnormalantenatalbleeding in caseswith
placenta previa [4].It is common practice to measure the
cervical length using transvaginal ultrasound to predict preterm
delivery. It is interesting to note that Ghi et al reported a possible
association between the cervical length and the risk of preterm
hemorrhage in patientswith complete placenta previa [5].
Although the cervical length did not differ significantly between
cases with and without prepartum bleeding, it was significantly
shorter among patients who underwent an emergency Cesarean
section at<34 weeks,due to massive hemorrhage compared
with patients who underwent an elective Cesarean section.In
our previous study [2],we found that the cervical length just
prior to delivery was not different between the cases, with and
withoutan emergencyCesareansectionin subjectswith
complete, partial and marginal placenta previa. Stafford et al [6]
recently demonstrated that a third trimester cervical length of
30 mm or less was associated with an increased risk for
hemorrhage (76% vs. 28%) in pregnancies with placenta previa,
and that tocodynamometerevidenceof regularuterine
contractions was more common in subjects with a short cervix
(69%) than in those with a longer cervix (21%).
It was reported by Ghourab that patients who had a low-lying
placenta with a thick edge,had a significantly higher rate of
antepartum hemorrhage (88.2%) compared with those who had
a thin edge (40.7%), and who required an emergency Cesarean
section before 36 weeks of gestation (64.7% vs.29.6%) [7].
Ghourab speculated that this might be explained by the abun-
dantvasculature ofthe lowerplacentaledge and the sub-
placental zone, and interference of a thick-edged placenta with
the descent of the fetal head.On the other hand,although the
placenta generally grows preferentially toward a better vascu-
larized field (trophotropism),a placenta overlying a less vas-
cularized cervix may undergo atrophy [8].Becausesome
vascular and placentalstructuralabnormalities,such as vela-
mentouscord insertions(vasaprevia),abruptio placentae,
placenta accretae,accessory placentas,and placentalinfarc-
tions, are frequently seen in cases with cord insertion or when
the placentais located onthe lower uterus[9e15], we
hypothesized thatplacentascoexisting with such placenta
abnormalities were more likely to detach from the decidua
basalis,resulting in frequent antenatal bleeding.However,the
frequencies ofbleeding were notdifferentbetween subjects
with and without such placental complications [2].
Oyelese and Smulian have mentioned that contractions a
cervicaleffacementand dilatation during the third trimester,
can cause separation ofthe placenta,which leads to small
amountsof bleeding.This bleeding may stimulate further
placentalseparation and unavoidable bleeding [4].However,
these placentalseparations are notclearly predictable using
ultrasonography, because the adaptation of the placenta a
uterine isthmusmay vary from case to case in advancing
gestation.Though some ultrasonographic findings,such as
a short uterine cervix and marginal sinus,are associated with
antenatalbleeding from placenta previa,these findings were
evaluated in the third trimester.Therefore,the obstetrician
should be aware that sudden bleeding during pregnancy m
occur in patients with placenta previa,even if no such ultra-
sonographic findings are detected during the second trime
Hemorrhage during Cesarean section
Patients with placenta previa often have a risk of massiv
bleeding during Cesarean section.According to a univariate
analysisof predisposingfactorsfor massivehemorrhage
during Cesarean section in patients with placenta previa in
institution [16],advanced maternalage (OR ¼ 3.1, 95%
CI ¼ 1.3e7.5) and a history of a previous Cesarean section
(OR ¼ 7.3, 95% CI ¼ 1.9e28.2) were associated with massi
bleeding. The frequencies of massive bleeding were higher
cases in which the placentas were located on the anterior w
(OR ¼ 3.5,95% CI ¼ 1.1e11.2) and/or were located on the
previousCesarean wound.The presence oflacunae in the
placenta (OR ¼ 2.8, 95% CI 1.0e7.6), sponge-like findings i
the cervix (OR 4.6,95% CI 1.7e11.9) and a lack of a clear
zone were also associated with massive bleeding during th
Cesarean operation.Adherence of the placenta diagnosed at
Cesarean was also associated with massive bleeding,and had
the highestodds ratio among these variables (OR 18.2,95%
CI 1.9e170.7).
Placenta accreta is one of the leading reasons for perform
a Cesarean hysterectomy [17]. The risk of placenta accreta is
relatedto maternal age and to the number of previous Cesar
deliveries[18e20]. The risk of havingplacentaaccrete
increased from 24% in patients with one prior Cesarean sec
to 67% in those with 3 or more prior Cesarean sections [20
Numerousreportshaveaddressed theantenatalultrasonic
prediction ofplacentaladherence[3,7,18,21].Irregularly-
shaped placentallacunae within the placenta,thinning of the
myometrium overlying the placenta, loss of the retroplacen
clearzone,protrusion ofthe placenta into the bladder,and
increased vascularity ofthe uterine serosa/bladderinterface
were reportedto be sonographicfeaturessuggestiveof
placental adherence [4,21,22]. Placenta accreta is thought
due to an absence ordeficiency ofNitabuch’s layeror the
spongiosus layer of the decidua. Histology usually shows th
the trophoblasts have invaded the myometrium withoutany
4 J. Hasegawa et al./ Taiwanese Journal of Obstetrics & Gynecology 51 (2012) 3e6
other locations (7.7e10%).They suggested that the echo-free
space in the marginal area of the placenta (an area associated
with a turbulentblood flow)was either a placentalsinus or
varices thatdeveloped in the decidualtissue.Our previous
retrospective study also demonstrated that in ultrasonographic
findings at 20 weeks of gestation, the frequency of a marginal
sinus (similar to the findings reported by Saitoh et al [3]) was
slightly higher (16%) in cases with bleeding episodes compared
to those without(0%) [2]. Although the pathophysiological
changes associated with the marginal sinus have not been well
clarified,we hypothesized thatan expanded marginalsinus
indicates the retention of maternal blood flow in the intervillous
space and decidualtissue,which may collapse occasionally
due to uterine contraction,thus resulting in a large amount of
hemorrhage during pregnancy.
Contractions, cervical effacement, and dilatation during the
third trimester, may cause the separation of the placenta, leading
to unavoidableabnormalantenatalbleeding in caseswith
placenta previa [4].It is common practice to measure the
cervical length using transvaginal ultrasound to predict preterm
delivery. It is interesting to note that Ghi et al reported a possible
association between the cervical length and the risk of preterm
hemorrhage in patientswith complete placenta previa [5].
Although the cervical length did not differ significantly between
cases with and without prepartum bleeding, it was significantly
shorter among patients who underwent an emergency Cesarean
section at<34 weeks,due to massive hemorrhage compared
with patients who underwent an elective Cesarean section.In
our previous study [2],we found that the cervical length just
prior to delivery was not different between the cases, with and
withoutan emergencyCesareansectionin subjectswith
complete, partial and marginal placenta previa. Stafford et al [6]
recently demonstrated that a third trimester cervical length of
30 mm or less was associated with an increased risk for
hemorrhage (76% vs. 28%) in pregnancies with placenta previa,
and that tocodynamometerevidenceof regularuterine
contractions was more common in subjects with a short cervix
(69%) than in those with a longer cervix (21%).
It was reported by Ghourab that patients who had a low-lying
placenta with a thick edge,had a significantly higher rate of
antepartum hemorrhage (88.2%) compared with those who had
a thin edge (40.7%), and who required an emergency Cesarean
section before 36 weeks of gestation (64.7% vs.29.6%) [7].
Ghourab speculated that this might be explained by the abun-
dantvasculature ofthe lowerplacentaledge and the sub-
placental zone, and interference of a thick-edged placenta with
the descent of the fetal head.On the other hand,although the
placenta generally grows preferentially toward a better vascu-
larized field (trophotropism),a placenta overlying a less vas-
cularized cervix may undergo atrophy [8].Becausesome
vascular and placentalstructuralabnormalities,such as vela-
mentouscord insertions(vasaprevia),abruptio placentae,
placenta accretae,accessory placentas,and placentalinfarc-
tions, are frequently seen in cases with cord insertion or when
the placentais located onthe lower uterus[9e15], we
hypothesized thatplacentascoexisting with such placenta
abnormalities were more likely to detach from the decidua
basalis,resulting in frequent antenatal bleeding.However,the
frequencies ofbleeding were notdifferentbetween subjects
with and without such placental complications [2].
Oyelese and Smulian have mentioned that contractions a
cervicaleffacementand dilatation during the third trimester,
can cause separation ofthe placenta,which leads to small
amountsof bleeding.This bleeding may stimulate further
placentalseparation and unavoidable bleeding [4].However,
these placentalseparations are notclearly predictable using
ultrasonography, because the adaptation of the placenta a
uterine isthmusmay vary from case to case in advancing
gestation.Though some ultrasonographic findings,such as
a short uterine cervix and marginal sinus,are associated with
antenatalbleeding from placenta previa,these findings were
evaluated in the third trimester.Therefore,the obstetrician
should be aware that sudden bleeding during pregnancy m
occur in patients with placenta previa,even if no such ultra-
sonographic findings are detected during the second trime
Hemorrhage during Cesarean section
Patients with placenta previa often have a risk of massiv
bleeding during Cesarean section.According to a univariate
analysisof predisposingfactorsfor massivehemorrhage
during Cesarean section in patients with placenta previa in
institution [16],advanced maternalage (OR ¼ 3.1, 95%
CI ¼ 1.3e7.5) and a history of a previous Cesarean section
(OR ¼ 7.3, 95% CI ¼ 1.9e28.2) were associated with massi
bleeding. The frequencies of massive bleeding were higher
cases in which the placentas were located on the anterior w
(OR ¼ 3.5,95% CI ¼ 1.1e11.2) and/or were located on the
previousCesarean wound.The presence oflacunae in the
placenta (OR ¼ 2.8, 95% CI 1.0e7.6), sponge-like findings i
the cervix (OR 4.6,95% CI 1.7e11.9) and a lack of a clear
zone were also associated with massive bleeding during th
Cesarean operation.Adherence of the placenta diagnosed at
Cesarean was also associated with massive bleeding,and had
the highestodds ratio among these variables (OR 18.2,95%
CI 1.9e170.7).
Placenta accreta is one of the leading reasons for perform
a Cesarean hysterectomy [17]. The risk of placenta accreta is
relatedto maternal age and to the number of previous Cesar
deliveries[18e20]. The risk of havingplacentaaccrete
increased from 24% in patients with one prior Cesarean sec
to 67% in those with 3 or more prior Cesarean sections [20
Numerousreportshaveaddressed theantenatalultrasonic
prediction ofplacentaladherence[3,7,18,21].Irregularly-
shaped placentallacunae within the placenta,thinning of the
myometrium overlying the placenta, loss of the retroplacen
clearzone,protrusion ofthe placenta into the bladder,and
increased vascularity ofthe uterine serosa/bladderinterface
were reportedto be sonographicfeaturessuggestiveof
placental adherence [4,21,22]. Placenta accreta is thought
due to an absence ordeficiency ofNitabuch’s layeror the
spongiosus layer of the decidua. Histology usually shows th
the trophoblasts have invaded the myometrium withoutany
4 J. Hasegawa et al./ Taiwanese Journal of Obstetrics & Gynecology 51 (2012) 3e6
![Document Page](https://desklib.com/media/document/docfile/pages/hemorrhage-placenta-previa/2024/09/08/d75eaa4a-6988-4917-8e5d-913af5c9011c-page-4.webp)
intervening deciduas[8]. Pasto etal [23] madethe first
suggestion thata lack of retroplacentalclear space detected
using ultrasonography mightbe an abnormal sign in patients
with placenta accreta. This area is seen beginning in week 12
and was thoughtto correspond to the dilated vessels of the
decidua basalis [22].A lack of a clear zone has often been
suggested as one of the ultrasonographic findings which may
prompt suspicion of the pathological adherence of the placenta
[4,16,22e24].In regard to the ultrasonic findings,the lack of
a clear zone was found to have a sensitivity of only 57% and
a false-positive rate of 48.4% [22]. After 20 weeks of gestation,
the sensitivity of this finding increased, with values of 80% [22].
Placenta lacunae have also been discussed as one ofthe
ultrasonographicfindingsfor predictingplacentaaccreta
[4,16,21,22,25e28].Intraplacentallacunae are vascular lakes
of various sizes and shapes seen within the placentalparen-
chyma.Comstock et al[22] found that at15 to 20 weeks of
gestation, the presence of lacunae in the placenta was the most
predictive sonographic sign of a placenta accreta, with a sensi-
tivity of 79% and a positive predictive value of 92%.Finberg
and Williams [25] demonstrated that the number of lacunae was
associated with complications related to placentaladherence.
Yang etal [27]classified the sonographic findings ofintra-
placental lacunae into one of four grades, and demonstrated that
the presence of Grade 2þ lacunae (defined as four to six larger
or more irregular lacunae present) was strongly associated with
placental adherence.
For such ultrasonographic findings, our multivariable anal-
ysis showed that a placenta located on the previous Cesarean
section wound (OR ¼ 123.1,95% CI ¼ 4.5e3395.2) and the
lack of a clear zone (OR ¼ 48.0, 95% CI ¼ 3.8e604.7) were
associated with placental adherence [16].On the other hand,
Hamadaet al. demonstratedthat placentalacunaewere
observed in 31.4% and 9.7% of cases with and without placenta
previa (OR ¼ 4.2, 95% CI ¼ 2.3e7.9). The lack of a clear zone
was observed in 5.7% and 0.9% ofcases with and without
placenta previa (OR ¼ 7.0,95% CI ¼ 1.5e32.0).Since the
decidua basalis is thinner in the lower uterine segment than in
the uterine body, the finding of the lack of a clear zone would
be more frequently observed in cases with placenta previa,
even without adherence.The contraction and cervical efface-
mentand dilatation thatoccurin the third trimestercause
separation of the placenta,which leads to a small amount of
bleeding in placenta previa cases [4]. Such bleeding might also
cover the presence of the retro-placental clear zone.
A logistic regression analysis in our previous study revealed
thatadvanced maternalage,previousCesarean section and
sponge-like findings of the cervix were associated with massive
bleeding during Cesarean section [16]. Sponge-like findings are
defined at our institution when five or more hypo-echoic areas
>5 mm in diameter are detected in the cervix. Additionally, the
correlation between sponge-like findings and perinatal maternal
massive hemorrhage has been reported previously [3,29,30].
Both the incidence of preterm delivery, due to sudden massive
hemorrhage,and the amountof bleeding during Cesarean
section, were significantly higher in cases in which two-thirds
of the placenta covered the internalos and a sponge-like
echo were found [3].Hurton et al [31] reported that the area
with sponge-like echoes were most likely composed of clu
of richly-developed blood vessels(presumably variceswith
variousdegreesand patternsof dilatation).Two reports
presumed thatthe sponge-like findings were cervicalvarices
[29,30].The sponge-like findings seems to be associated w
massive intraoperative hemorrhage in cases with placent
via, regardless of the placental adherence.
Mimuraet al [32] demonstrated asignificantnegative
correlation between the amountof bleeding and the cervical
length(r ¼ e0.344, p < 0.001), regardless of the existence
placentaladherence.The oddsratio for massive bleeding
(>2500 mL) in cases with shortcervicallengths (<25 mm)
was 7.6 (95% CI ¼ 2.4e23.8) in comparison to cases with
long cervicallengths.Postpartum hemorrhage is caused by
uterine atony, contributing to about 80% of the cases, an
causes include genital tract trauma, pathological placent
and so on [33]. Reynolds et al noted that contractions sta
the fundus and progressively propagate toward the cervi
that the strength of contractions was greatest at the fund
least at the cervix [34]. Margono et al. reported the relati
between the upper and lower uterine contractions in diffe
subsets of patients [35]. They noted that the contraction
uterine low segment after placenta removal may be weak
that of upper part of the uterus [34].Most of the hemorrhage
during Cesarean section isuterine incisionalbleeding and
bleeding from the surface of the placental separation. In
with placenta previa,because the placenta is located on the
loweruterine segment,the bleeding during surgery may be
greaterdue to uterine atony around the cervicalos, than in
cases where the placenta is on the uterine body. Furtherm
when the cervix is shortened,this could mean that the lower
segment is widely extended, making the contraction wea
is plausible that a short cervical length in cases with plac
previa isassociated with the massive bleeding during the
operation.
Similarto placenta previa,a low-lying placenta isalso
associated with massive bleeding around delivery, due to
in the lower uterine segment. However, we recommend v
delivery even in cases with a low-lying placenta, to reduc
amountof bleeding during delivery,especially from uterine
incisional bleeding,based on the report from Nakamura et a
[36] who demonstrated that 86.9% of cases with a low-ly
placenta and non-reassuring fetal status had successful t
vaginal deliveries without increased bleeding during labo
Conclusion
Although sudden massive bleeding during pregnancy m
occur in patients with placenta previa,regardless of the pres-
ence orabsence ofany abnormalultrasonographic findings,
a short uterine cervical length in the third trimester and s
venosus at the margin of the placenta may predict an inc
risk of antenatalbleeding in pregnantwomen demonstrating
placenta previa.
During a Cesareansection,advancedmaternalage,
a history of a previous Cesarean section,and the presence of
5J. Hasegawa et al./ Taiwanese Journal of Obstetrics & Gynecology 51 (2012) 3e6
suggestion thata lack of retroplacentalclear space detected
using ultrasonography mightbe an abnormal sign in patients
with placenta accreta. This area is seen beginning in week 12
and was thoughtto correspond to the dilated vessels of the
decidua basalis [22].A lack of a clear zone has often been
suggested as one of the ultrasonographic findings which may
prompt suspicion of the pathological adherence of the placenta
[4,16,22e24].In regard to the ultrasonic findings,the lack of
a clear zone was found to have a sensitivity of only 57% and
a false-positive rate of 48.4% [22]. After 20 weeks of gestation,
the sensitivity of this finding increased, with values of 80% [22].
Placenta lacunae have also been discussed as one ofthe
ultrasonographicfindingsfor predictingplacentaaccreta
[4,16,21,22,25e28].Intraplacentallacunae are vascular lakes
of various sizes and shapes seen within the placentalparen-
chyma.Comstock et al[22] found that at15 to 20 weeks of
gestation, the presence of lacunae in the placenta was the most
predictive sonographic sign of a placenta accreta, with a sensi-
tivity of 79% and a positive predictive value of 92%.Finberg
and Williams [25] demonstrated that the number of lacunae was
associated with complications related to placentaladherence.
Yang etal [27]classified the sonographic findings ofintra-
placental lacunae into one of four grades, and demonstrated that
the presence of Grade 2þ lacunae (defined as four to six larger
or more irregular lacunae present) was strongly associated with
placental adherence.
For such ultrasonographic findings, our multivariable anal-
ysis showed that a placenta located on the previous Cesarean
section wound (OR ¼ 123.1,95% CI ¼ 4.5e3395.2) and the
lack of a clear zone (OR ¼ 48.0, 95% CI ¼ 3.8e604.7) were
associated with placental adherence [16].On the other hand,
Hamadaet al. demonstratedthat placentalacunaewere
observed in 31.4% and 9.7% of cases with and without placenta
previa (OR ¼ 4.2, 95% CI ¼ 2.3e7.9). The lack of a clear zone
was observed in 5.7% and 0.9% ofcases with and without
placenta previa (OR ¼ 7.0,95% CI ¼ 1.5e32.0).Since the
decidua basalis is thinner in the lower uterine segment than in
the uterine body, the finding of the lack of a clear zone would
be more frequently observed in cases with placenta previa,
even without adherence.The contraction and cervical efface-
mentand dilatation thatoccurin the third trimestercause
separation of the placenta,which leads to a small amount of
bleeding in placenta previa cases [4]. Such bleeding might also
cover the presence of the retro-placental clear zone.
A logistic regression analysis in our previous study revealed
thatadvanced maternalage,previousCesarean section and
sponge-like findings of the cervix were associated with massive
bleeding during Cesarean section [16]. Sponge-like findings are
defined at our institution when five or more hypo-echoic areas
>5 mm in diameter are detected in the cervix. Additionally, the
correlation between sponge-like findings and perinatal maternal
massive hemorrhage has been reported previously [3,29,30].
Both the incidence of preterm delivery, due to sudden massive
hemorrhage,and the amountof bleeding during Cesarean
section, were significantly higher in cases in which two-thirds
of the placenta covered the internalos and a sponge-like
echo were found [3].Hurton et al [31] reported that the area
with sponge-like echoes were most likely composed of clu
of richly-developed blood vessels(presumably variceswith
variousdegreesand patternsof dilatation).Two reports
presumed thatthe sponge-like findings were cervicalvarices
[29,30].The sponge-like findings seems to be associated w
massive intraoperative hemorrhage in cases with placent
via, regardless of the placental adherence.
Mimuraet al [32] demonstrated asignificantnegative
correlation between the amountof bleeding and the cervical
length(r ¼ e0.344, p < 0.001), regardless of the existence
placentaladherence.The oddsratio for massive bleeding
(>2500 mL) in cases with shortcervicallengths (<25 mm)
was 7.6 (95% CI ¼ 2.4e23.8) in comparison to cases with
long cervicallengths.Postpartum hemorrhage is caused by
uterine atony, contributing to about 80% of the cases, an
causes include genital tract trauma, pathological placent
and so on [33]. Reynolds et al noted that contractions sta
the fundus and progressively propagate toward the cervi
that the strength of contractions was greatest at the fund
least at the cervix [34]. Margono et al. reported the relati
between the upper and lower uterine contractions in diffe
subsets of patients [35]. They noted that the contraction
uterine low segment after placenta removal may be weak
that of upper part of the uterus [34].Most of the hemorrhage
during Cesarean section isuterine incisionalbleeding and
bleeding from the surface of the placental separation. In
with placenta previa,because the placenta is located on the
loweruterine segment,the bleeding during surgery may be
greaterdue to uterine atony around the cervicalos, than in
cases where the placenta is on the uterine body. Furtherm
when the cervix is shortened,this could mean that the lower
segment is widely extended, making the contraction wea
is plausible that a short cervical length in cases with plac
previa isassociated with the massive bleeding during the
operation.
Similarto placenta previa,a low-lying placenta isalso
associated with massive bleeding around delivery, due to
in the lower uterine segment. However, we recommend v
delivery even in cases with a low-lying placenta, to reduc
amountof bleeding during delivery,especially from uterine
incisional bleeding,based on the report from Nakamura et a
[36] who demonstrated that 86.9% of cases with a low-ly
placenta and non-reassuring fetal status had successful t
vaginal deliveries without increased bleeding during labo
Conclusion
Although sudden massive bleeding during pregnancy m
occur in patients with placenta previa,regardless of the pres-
ence orabsence ofany abnormalultrasonographic findings,
a short uterine cervical length in the third trimester and s
venosus at the margin of the placenta may predict an inc
risk of antenatalbleeding in pregnantwomen demonstrating
placenta previa.
During a Cesareansection,advancedmaternalage,
a history of a previous Cesarean section,and the presence of
5J. Hasegawa et al./ Taiwanese Journal of Obstetrics & Gynecology 51 (2012) 3e6
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sponge-like findings,are risk factors for massive bleeding in
patients with placenta previa,regardless ofthe existence of
placentaladherence.The ultrasound findingsof a placenta
located on the previous Cesarean section wound, and a lack of
a clear zone,are serious risk factors for placental adherence.
References
[1] Crane JM, Van den Hof MC, Dodds L, Armson BA, Liston R. Maternal
complications with placenta previa.Am J Perinatol 2000;17:101e5.
[2] HasegawaJ, Higashi M, TakahashiS, Mimura T, NakamuraM,
Matsuoka R,et al. Can ultrasonography of the placenta previa predict
antenatal bleeding? J Clin Ultrasound 2011;39:458e62.
[3] Saitoh M, Ishihara K, Sekiya T, Araki T. Anticipation of uterine bleeding
in placenta previa based on vaginalsonographic evaluation.Gynecol
Obstet Investig 2002;54:37e42.
[4] Oyelese Y,Smulian JC. Placenta previa,placenta accreta,and vasa
previa.Obstet gynecol 2006;107:927e41.
[5] Ghi T, Contro E, Martina T, Piva M, Morandi R, Orsini LF, et al. Cervical
length and risk of antepartum bleeding in women with complete placenta
previa.Ultrasound Obstet Gynecol 2009;33:209e12.
[6] Stafford IA, DasheJS, ShivversSA, AlexanderJM, McIntireDD,
Leveno KJ.Ultrasonographic cervical length and risk of hemorrhage in
pregnancies with placenta previa.Obstet Gynecol 2010;116:595e600.
[7] Ghourab S.Third-trimestertransvaginalultrasonography in placenta
previa:doesthe shape ofthe lowerplacentaledge predictclinical
outcome? Ultrasound Obstet Gynecol 2001;18:103e8.
[8] Benirschke K,Kaufmann P.In: Pathology of the human placenta.New
York: Springer; 2000.
[9] Hasegawa J, Matsuoka R, Ichizuka K, Otsuki K, Sekizawa A, Farina A,
et al. Cord insertion into the lower third of the uterus in the first trimester
is associated with placental and umbilical cord abnormalities. Ultrasound
Obstet Gynecol 2006;28:183e6.
[10] Hasegawa J,Matsuoka R,Ichizuka K,Sekizawa A,Farina A,Okai T.
Velamentous cord insertion into the lower third of the uterus is associated
with intrapartum fetalheartrate abnormalities.UltrasoundObstet
Gynecol 2006;27:425e9.
[11] SchachterM, Tovbin Y,Arieli S, FriedlerS, Ron-El R, Sherman D.
In vitro fertilization is a risk factor for vasa previa. Fertil Steril 2002;78:
642e3.
[12] Oyelese KO,Turner M,Lees C,Campbell S.Vasa previa: an avoidable
obstetric tragedy.Obstet Gynecol Surv 1999;54:138e45.
[13] Francois K, Mayer S, Harris C, Perlow JH. Association of vasa previa at
delivery with a history of second-trimester placenta previa. J Reprod Med
2003;48:771e4.
[14] Lee W, Lee VL, Kirk JS, Sloan CT,Smith RS,Comstock CH.Vasa
previa:prenataldiagnosis,naturalevolution,and clinicaloutcome.
Obstet Gynecol 2000;95:572e6.
[15] Fung TY, Lau TK. Poor perinatal outcome associated with vasa previa: is
it preventable? A reportof three cases and review ofthe literature.
Ultrasound Obstet Gynecol 1998;12:430e3.
[16] Hasegawa J, Matsuoka R, Ichizuka K, Mimura T, Sekizawa A, Farina A,
et al. Predisposing factorsfor massive hemorrhage during Cesarean
section in patientswith placenta previa.Ultrasound ObstetGynecol
2009;34:80e4.
[17] KastnerES, Figueroa R,Garry D,Maulik D. Emergency peripartum
hysterectomy:experienceat a community teaching hospital.Obstet
Gynecol 2002;99:971e5.
[18] Miller DA,Chollet JA,Goodwin TM.Clinical risk factors for placenta
previa-placenta accreta.Am J Obstet Gynecol 1997;177:210e4.
[19] Wu S, Kocherginsky M,Hibbard JU.Abnormalplacentation:twenty-
year analysis. Am J Obstet Gynecol 2005;192:1458e61.
[20] Clark SL, Koonings PP,Phelan JP.Placenta previa/accreta and prior
cesarean section.Obstet Gynecol 1985;66:89e92.
[21] ComstockCH. Antenataldiagnosisof placentaaccreta:a review.
Ultrasound Obstet Gynecol 2005;26:89e96.
[22] Comstock CH, Love Jr JJ, Bronsteen RA, Lee W, Vettraino IM, Huang RR
et al.Sonographic detection of placenta accreta in the second and thir
trimesters of pregnancy. Am J Obstet Gynecol 2004;190:1135e40.
[23] Pasto ME, Kurtz AB, Rifkin MD, Cole-BeugletC, WapnerRJ,
Goldberg BB. Ultrasonographic findings in placenta increta. J Ultrasoun
Med 1983;2:155e9.
[24] Khong TY,Robertson WB.Placenta creta and placenta praevia creta.
Placenta 1987;8:399e409.
[25] Finberg HJ,WilliamsJW. Placenta accreta:prospective sonographic
diagnosis in patients with placenta previa and prior cesarean section.J
Ultrasound Med 1992;11:333e43.
[26] Chou MM, Ho ES, Lee YH. Prenatal diagnosis of placenta previa accret
by transabdominal color Doppler ultrasound. Ultrasound Obstet Gynec
2000;15:28e35.
[27] Yang JI, Lim YK, Kim HS, Chang KH,Lee JP,Ryu HS.Sonographic
findings of placental lacunae and the prediction of adherent placenta
women with placenta previa totalis and prior Cesarean section.Ultra-
sound Obstet Gynecol 2006;28:178e82.
[28] Sumigama S, Itakura A, Ota T, Okada M, Kotani T, Hayakawa H, et al.
Placenta previa increta/percreta in Japan: a retrospective study of ultr
sound findings,management and clinical course.J Obstet Gynecol Res
2007;33:606e11.
[29] Kumazawa Y,Shimizu D,Hosoya N,Hirano H,Ishiyama K,Tanaka T.
Cervical varix with placenta previa totalis.J Obstet Gynecol Res 2007;
33:536e8.
[30] YoshimuraK, Hirsch E, Kitano R, KashimuraM. Cervicalvarix
accompanied by placenta previa in twin pregnancy. J Obstet Gynecol
2004;30:323e5.
[31] Hurton T,Morrill H, Mascola M,York C, Bromley B. Cervical varices:
an unusual etiology for third-trimester bleeding. J Clin Ultrasound 1998
26:317e9.
[32] Mimura T, HasegawaJ, NakamuraM, MatsuokaR, IchizukaK,
Sekizawa A,et al. Correlation between the cervicallength and the
amount of bleeding during cesarean section in placenta previa.J Obstet
Gynecol Res 2011;37:830e5.
[33] Oyelese Y,Scorza WE,Mastrolia R,Smulian JC.Postpartum hemor-
rhage. Obstet Gynecol Clin North Am 2007;34:421e41.x.
[34] Reynolds SR,Hellman LM,Bruns P.Patterns of uterine contractility in
women during pregnancy.Obstet Gynecol Surv 1948;3:629e46.
[35] Margono F,Minkoff H,Chan E.Intrauterine pressure wave character-
istics of the upper and lower uterine segments in parturients with acti
phase arrest.Obstet Gynecol 1993;81:481e5.
[36] Nakamura M,Hasegawa J,Mimura T,Matsuoka R,Ichizuka K,Seki-
zawa A, et al. Amount of hemorrhage during vaginal delivery correlate
with the length from placental edge to external os in low-lying placent
Obstet Gynecol Res,in press.
6 J. Hasegawa et al./ Taiwanese Journal of Obstetrics & Gynecology 51 (2012) 3e6
View publication statsView publication stats
patients with placenta previa,regardless ofthe existence of
placentaladherence.The ultrasound findingsof a placenta
located on the previous Cesarean section wound, and a lack of
a clear zone,are serious risk factors for placental adherence.
References
[1] Crane JM, Van den Hof MC, Dodds L, Armson BA, Liston R. Maternal
complications with placenta previa.Am J Perinatol 2000;17:101e5.
[2] HasegawaJ, Higashi M, TakahashiS, Mimura T, NakamuraM,
Matsuoka R,et al. Can ultrasonography of the placenta previa predict
antenatal bleeding? J Clin Ultrasound 2011;39:458e62.
[3] Saitoh M, Ishihara K, Sekiya T, Araki T. Anticipation of uterine bleeding
in placenta previa based on vaginalsonographic evaluation.Gynecol
Obstet Investig 2002;54:37e42.
[4] Oyelese Y,Smulian JC. Placenta previa,placenta accreta,and vasa
previa.Obstet gynecol 2006;107:927e41.
[5] Ghi T, Contro E, Martina T, Piva M, Morandi R, Orsini LF, et al. Cervical
length and risk of antepartum bleeding in women with complete placenta
previa.Ultrasound Obstet Gynecol 2009;33:209e12.
[6] Stafford IA, DasheJS, ShivversSA, AlexanderJM, McIntireDD,
Leveno KJ.Ultrasonographic cervical length and risk of hemorrhage in
pregnancies with placenta previa.Obstet Gynecol 2010;116:595e600.
[7] Ghourab S.Third-trimestertransvaginalultrasonography in placenta
previa:doesthe shape ofthe lowerplacentaledge predictclinical
outcome? Ultrasound Obstet Gynecol 2001;18:103e8.
[8] Benirschke K,Kaufmann P.In: Pathology of the human placenta.New
York: Springer; 2000.
[9] Hasegawa J, Matsuoka R, Ichizuka K, Otsuki K, Sekizawa A, Farina A,
et al. Cord insertion into the lower third of the uterus in the first trimester
is associated with placental and umbilical cord abnormalities. Ultrasound
Obstet Gynecol 2006;28:183e6.
[10] Hasegawa J,Matsuoka R,Ichizuka K,Sekizawa A,Farina A,Okai T.
Velamentous cord insertion into the lower third of the uterus is associated
with intrapartum fetalheartrate abnormalities.UltrasoundObstet
Gynecol 2006;27:425e9.
[11] SchachterM, Tovbin Y,Arieli S, FriedlerS, Ron-El R, Sherman D.
In vitro fertilization is a risk factor for vasa previa. Fertil Steril 2002;78:
642e3.
[12] Oyelese KO,Turner M,Lees C,Campbell S.Vasa previa: an avoidable
obstetric tragedy.Obstet Gynecol Surv 1999;54:138e45.
[13] Francois K, Mayer S, Harris C, Perlow JH. Association of vasa previa at
delivery with a history of second-trimester placenta previa. J Reprod Med
2003;48:771e4.
[14] Lee W, Lee VL, Kirk JS, Sloan CT,Smith RS,Comstock CH.Vasa
previa:prenataldiagnosis,naturalevolution,and clinicaloutcome.
Obstet Gynecol 2000;95:572e6.
[15] Fung TY, Lau TK. Poor perinatal outcome associated with vasa previa: is
it preventable? A reportof three cases and review ofthe literature.
Ultrasound Obstet Gynecol 1998;12:430e3.
[16] Hasegawa J, Matsuoka R, Ichizuka K, Mimura T, Sekizawa A, Farina A,
et al. Predisposing factorsfor massive hemorrhage during Cesarean
section in patientswith placenta previa.Ultrasound ObstetGynecol
2009;34:80e4.
[17] KastnerES, Figueroa R,Garry D,Maulik D. Emergency peripartum
hysterectomy:experienceat a community teaching hospital.Obstet
Gynecol 2002;99:971e5.
[18] Miller DA,Chollet JA,Goodwin TM.Clinical risk factors for placenta
previa-placenta accreta.Am J Obstet Gynecol 1997;177:210e4.
[19] Wu S, Kocherginsky M,Hibbard JU.Abnormalplacentation:twenty-
year analysis. Am J Obstet Gynecol 2005;192:1458e61.
[20] Clark SL, Koonings PP,Phelan JP.Placenta previa/accreta and prior
cesarean section.Obstet Gynecol 1985;66:89e92.
[21] ComstockCH. Antenataldiagnosisof placentaaccreta:a review.
Ultrasound Obstet Gynecol 2005;26:89e96.
[22] Comstock CH, Love Jr JJ, Bronsteen RA, Lee W, Vettraino IM, Huang RR
et al.Sonographic detection of placenta accreta in the second and thir
trimesters of pregnancy. Am J Obstet Gynecol 2004;190:1135e40.
[23] Pasto ME, Kurtz AB, Rifkin MD, Cole-BeugletC, WapnerRJ,
Goldberg BB. Ultrasonographic findings in placenta increta. J Ultrasoun
Med 1983;2:155e9.
[24] Khong TY,Robertson WB.Placenta creta and placenta praevia creta.
Placenta 1987;8:399e409.
[25] Finberg HJ,WilliamsJW. Placenta accreta:prospective sonographic
diagnosis in patients with placenta previa and prior cesarean section.J
Ultrasound Med 1992;11:333e43.
[26] Chou MM, Ho ES, Lee YH. Prenatal diagnosis of placenta previa accret
by transabdominal color Doppler ultrasound. Ultrasound Obstet Gynec
2000;15:28e35.
[27] Yang JI, Lim YK, Kim HS, Chang KH,Lee JP,Ryu HS.Sonographic
findings of placental lacunae and the prediction of adherent placenta
women with placenta previa totalis and prior Cesarean section.Ultra-
sound Obstet Gynecol 2006;28:178e82.
[28] Sumigama S, Itakura A, Ota T, Okada M, Kotani T, Hayakawa H, et al.
Placenta previa increta/percreta in Japan: a retrospective study of ultr
sound findings,management and clinical course.J Obstet Gynecol Res
2007;33:606e11.
[29] Kumazawa Y,Shimizu D,Hosoya N,Hirano H,Ishiyama K,Tanaka T.
Cervical varix with placenta previa totalis.J Obstet Gynecol Res 2007;
33:536e8.
[30] YoshimuraK, Hirsch E, Kitano R, KashimuraM. Cervicalvarix
accompanied by placenta previa in twin pregnancy. J Obstet Gynecol
2004;30:323e5.
[31] Hurton T,Morrill H, Mascola M,York C, Bromley B. Cervical varices:
an unusual etiology for third-trimester bleeding. J Clin Ultrasound 1998
26:317e9.
[32] Mimura T, HasegawaJ, NakamuraM, MatsuokaR, IchizukaK,
Sekizawa A,et al. Correlation between the cervicallength and the
amount of bleeding during cesarean section in placenta previa.J Obstet
Gynecol Res 2011;37:830e5.
[33] Oyelese Y,Scorza WE,Mastrolia R,Smulian JC.Postpartum hemor-
rhage. Obstet Gynecol Clin North Am 2007;34:421e41.x.
[34] Reynolds SR,Hellman LM,Bruns P.Patterns of uterine contractility in
women during pregnancy.Obstet Gynecol Surv 1948;3:629e46.
[35] Margono F,Minkoff H,Chan E.Intrauterine pressure wave character-
istics of the upper and lower uterine segments in parturients with acti
phase arrest.Obstet Gynecol 1993;81:481e5.
[36] Nakamura M,Hasegawa J,Mimura T,Matsuoka R,Ichizuka K,Seki-
zawa A, et al. Amount of hemorrhage during vaginal delivery correlate
with the length from placental edge to external os in low-lying placent
Obstet Gynecol Res,in press.
6 J. Hasegawa et al./ Taiwanese Journal of Obstetrics & Gynecology 51 (2012) 3e6
View publication statsView publication stats
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