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Ultrasound Obstet Gynecol 2000; 15: 2835.

Prenatal diagnosis of placenta previa accreta by


transabdominal color Doppler ultrasound
M.M. CHOU, E.S.C. HO and Y.H. LEE
Division of MaternalFetal Medicine, Department of Obstetrics and Gynecology, Taichung Veterans General Hospital, Chung Shan Medical and
Dental College, Taichung, Taiwan, Republic of China

KE YW OR D S : Color Doppler ultrasound, Placenta previa accreta, Prenatal diagnosis

ABS TRACT
Objective The aim of this study was to evaluate the
efficacy of transabdominal color Doppler ultrasound in
diagnosing placenta previa accreta.
Design Eighty patients with persistent placenta previa
underwent transabdominal B-mode and color Doppler
ultrasound evaluation in the second and third trimesters
because they had a high risk of placenta accreta. Color
Doppler imaging criteria used included diffuse intraparenchymal placental lacunar flow; focal intraparenchymal
placental lacunar flow; bladderuterine serosa interphase
hypervascularity; prominent subplacental venous complex;
and loss of subplacental Doppler vascular signals. The
color Doppler images were interpreted prospectively for
signs of placenta previa accreta according to the exhibited
color Doppler sonographic features.
Results Sixteen of the 80 patients exhibited characteristic
color Doppler imaging patterns highly specific for placenta
accreta according to the preceding criteria, and 14 of these
had histopathological proof of placenta accreta. Two
patients had false-positive color Doppler imaging evidence
mistaken for interphase hypervascularity caused by bladder varices. Thirteen patients underwent hysterectomy in
the group suspicious for accreta. Of the 64 patients with
negative color Doppler imaging results, three had placenta
accreta, while two required cesarean hysterectomy; the
remaining patient underwent uterine artery ligation for
bleeding from the lower uterine segment. The sensitivity of
color Doppler imaging in the diagnosis of placenta previa
accreta was 82.4% (14/17) and the specificity was 96.8%
(61/63). The positive and negative predictive values were
87.5% (14/16) and 95.3% (61/64), respectively.
Conclusions Variable vascular morphological patterns of
placenta previa accreta were exhibited and categorized by
transabdominal color Doppler sonography in the antenatal
period. The identification of these specific vascular

patterns had a positive impact on the peripartum clinical


management of the affected patients.

INTR OD U CTI ON
Massive obstetric hemorrhage is still the leading cause of
pregnancy-related deaths, and placenta previa accreta
remains one of the major predisposing factors1. With the
increasing rate of cesarean delivery, the incidence of both
placenta previa and placenta accreta is steadily increasing
in frequency2,3. We therefore anticipate more cases of
placenta previa accreta in our obstetric practice. In several
recent series, placenta accreta has emerged as the major
indication for peripartum hysterectomy, accounting for
4060% of cases3,4. It has, therefore, become a challenging
problem of increasing clinical significance in obstetrics.
The diagnosis of placenta previa accreta using grayscale sonography has been previously described48. More
recently, color Doppler ultrasound has been suggested to
aid in the diagnosis of placenta previa accreta because it
highlights abnormal areas of hypervascularity with
dilated blood vessels within the placental and uterine
tissues914. In this study, we evaluated the uteroplacental
vascular morphological manifestations of placenta previa
accreta with the use of transabdominal color Doppler
ultrasound and attempted to correlate them with the
clinical outcomes of this potentially life-threatening
obstetric disorder.

MATE RIAL S AND M E THOD S


Eighty patients with persistent placenta previa in the
second and third trimesters who were admitted to the
maternity unit at the Taichung Veterans General Hospital
from July 1994 to July 1998 underwent a transabdominal
B-mode and color Doppler evaluation using an Acuson 128
XP/10 (Acuson Corp., Mountain View, CA, USA) ultrasound machine and a 3.5-MHz transabdominal curvilinear
transducer. The majority of patients at risk for suspected

Correspondence: Dr M. M. Chou, Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, Taichung Veterans General
Hospital, Chung Shan Medical and Dental College, 160 Taichungkang Road, Section 3, Taichung 407, Taiwan, Republic of China
Received 301198, Revised 28499, Accepted 13599

ORIG INAL PAPER

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Placenta previa accreta


placenta accreta were referred to us for detailed color
Doppler evaluations because regional obstetricians were
aware of our study interest. Forty out of 80 patients had
had a cesarean section with their first pregnancies. The

c
Figure 1 Diffuse vascular pattern of placenta previa increta.
(a) Transabdominal gray-scale scan at 30 weeks gestation showing
multiple large irregular sonolucent spaces traversing the entire
placenta. (b) Color Doppler imaging showing an extensive hypervascularization pattern. (c) Pulsed Doppler interrogation of lacunae
showing turbulent high-velocity (15 cm/s) venous-type flow.
F femur; PL placenta.

Ultrasound in Obstetrics and Gynecology

M.M. Chou et al.


mean age of the patients was 30.8 years (range 21
43 years). The mean parity was 1.2.
Gray-scale B-mode sonography was first used to screen
the placental tissue in a systematic fashion. Careful
attention was paid to homogeneity and echogenicity
patterns of the placenta. If note was taken of absence of
normal subplacental venous complex, placental sonolucent
lakes and/or irregularities of bladderuterine serosa,
assessment of the placenta was performed using superimposed color-coded flow and spectral Doppler flow. In
the last 2 years of the study period, color Doppler flow
patterns were further evaluated using power Doppler
(Color Doppler Energy, Acuson) as an aid to prenatal
diagnosis for the patients with sonographic findings
suggestive of placenta accreta. Doppler gain and flow
velocity settings were adjusted until maximum color
Doppler signals were obtained without producing diffuse
artifacts. The ALARA principle (as low as reasonably
achievable) was implemented to ensure the safe color
Doppler imaging in fetal tissues. The highest peak velocity
of pulsatile venous flow within the sonolucent placental
vascular lakes was obtained using angle correction, and the
resistance index of the neovascularized arterial blood flow
within the uterine serosaposterior bladder wall boundary
zone was recorded in definitely abnormal patients.
The color Doppler criteria suggestive of placenta previa
accreta that we assessed included the following:
1. A diffuse lacunar flow pattern exhibiting diffusely
dilated vascular channels scattered throughout the whole
placenta and the surrounding myometrial or cervical
tissues. High-velocity pulsatile venous-type flow was
found in the sonolucent vascular spaces (Figure 1).
2. A focal lacunar flow pattern showing irregular
sonolucent vascular lakes with turbulent lacunar flow
distributed regionally or focally within the intraparenchymal placental area (Figure 2).
3. Interphase hypervascularity with abnormal blood
vessels linking the placenta to the bladder with high
diastolic arterial blood flow (Figure 3).
4. Markedly dilated peripheral subplacental vascular
channels with pulsatile venous-type flow over the uterine
cervix (Figure 4).
5. Absence of subplacental vascular signals in the areas
lacking the peripheral subplacental hypoechoic zone.
The color Doppler observations in patients not suspected
of having placenta accreta included the following characteristic features:
1. Discrete branching of surface chorionic arteries and
intraplacental villous arteries clearly visualized within the
homogeneous placental substance with typical flow velocity waveforms.
2. Central cotyledonary sonolucent avillous cavities
identified by real-time imaging, containing a non-pulsatile
low-velocity venous flow pattern.
3. The presence of a normal subplacental venous
complex with non-pulsatile low-velocity venous blood
flow waveforms.
During this study period, one patient with abdominal
pregnancy and another with a term pregnancy in a

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Placenta previa accreta

M.M. Chou et al.

a
Figure 2 Focal lacunar flow pattern of placenta previa accreta. (a) Color Doppler imaging showing pulsatile blood flow in the focal area of the
lower uterine segment and subplacental space. (b) Pulsed Doppler showing high-velocity turbulent venous-type flow (13 cm/s). B bladder;
H head; PL placenta.

Figure 3 Interphase (bladderuterine wall junction) vascular pattern of placenta previa increta. (a) Gray-scale scan showing absence of
intervening myometrium between the placenta and the uterine serosa. (b) Color Doppler imaging showing abdominal blood vessels linking the
placenta to the bladder. Focal intraplacental lacunar flow was also detected. (c) Color Doppler energy further defining the abnormal bladder
uterine wall hypervascularity. (d) Pulsed Doppler imaging showing low-impedance arterial flow (resistance index 0.25). B bladder; H head;
PL placenta.

30

Ultrasound in Obstetrics and Gynecology

Placenta previa accreta

b
Figure 4 Prominent subplacental vascularity of placenta previa
accreta. (a) Gray-scale scan showing prominent anechoic zone in
regions adjacent to the focally adherent placenta (arrowheads).
(b) Color Doppler imaging confirming that the anechoic zone
corresponds to markedly dilated venous channels. Low-velocity
(5 cm/s) venous-type flow was detected by pulsed Doppler.
B bladder; P adherent placenta; PL placenta; V venous
channels.

rudimentary horn were encountered. We believe that it is


worthwhile to describe the color Doppler vascular pattern
to illustrate the differential diagnostic considerations for
placenta previa accreta. Follow-up clinical data were
obtained from the obstetricians at the time of delivery
and from histopathological reports.

RE SU LTS
A summary of patient history, color Doppler features and
outcome is shown in Table 1. All abnormally adherent
placentas, which were predominantly anterior or central
placenta previa, were correctly identified; two patients
with purely posterior placenta previa accreta and one
with lateral placenta previa accreta were misdiagnosed in
this study. All diagnoses except for one were made in the
third trimester, at a mean gestational age of 30.5 weeks
(range 1636 weeks). Nine of the 16 patients in the
group suspicious for accreta had a history of cesarean
sections, 31 of 64 of the patients in the group that was

Ultrasound in Obstetrics and Gynecology

M.M. Chou et al.


not suggested of having accreta had a history of cesarean
section.
Among the six patients who were proved to have
placenta increta, two had diffuse-type lacunar flow and
extensive vascularity throughout the whole placenta and
surrounding myometrial tissues; two had focal lacunar
flow within the suspicious region. In the remaining two
patients, one had marked vascularity within the uterine
serosabladder junction and focal placental area, and one
had prominent subplacental vascularity. Of the eight
patients who had placenta accreta, six had focal-type
lacunar flow and two had markedly dilated venous
channels within the subplacental hypoechoic zone.
Hysterectomy was performed immediately in 13 patients
to achieve haemostasis after delivery by cesarean section.
Patient no. 1 was hospitalized in the antenatal ward
because of several episodes of vaginal bleeding in the early
third trimester. Diffuse lacunar flow pattern was detected
by transabdominal color Doppler ultrasound. A sudden
onset of massive vaginal bleeding occurred at 31 weeks;
the patient was in shock and was rushed into the operating
room. Emergency cesarean hysterectomy was performed
immediately. Estimated blood loss was 15 000 ml. Postoperative convalescence was uneventful. Patient no. 13
underwent uterine packing and hypogastric artery embolization initially after cesarean delivery because of persistent vaginal bleeding. A hysterectomy was performed 84 h
after cesarean delivery to achieve hemostasis. In this case,
the venous flow into the dilated subplacental vascular
channels was low.
Two patients with false-positive results had color
Doppler evidence of mistaken interphase hypervascularity
caused by bladder varices. Both of these patients had had
a previous cesarean section with uneventful repeat
cesarean deliveries. Sixty-four patients were considered
negative for placenta accreta by the aforementioned color
Doppler criteria. Three had placenta accreta, while two
required cesarean hysterectomy; the remaining patient
underwent uterine artery ligation for bleeding from a
non-contractile lower uterine segment. In these three
patients with false-negative color Doppler results, one
patient had a twin pregnancy with two separate anterior
and lateral placentas and the other two patients had
posterior placenta previa.
The mean estimated blood loss among the patients with
lacunar flow was 4446 ml (range 104015 000 ml), while
the mean estimated blood loss among the patients with
non-lacunar flow was 882 ml (range 3002500 ml). There
was no long-term maternal morbidity and there were no
maternal deaths in the series. All infants were alive and
well. The average birth weight for the lacunar flow group
was 2512 g (range 16553305 g) and for the group that
was not suggestive of having accreta 2687 g (range 1105
4045 g). Histopathological examination of all placentas
revealed chorionic villi penetrating to variable depths into
the myometrium.
In this series, the sensitivity of transabdominal color
Doppler imaging in the diagnosis of placenta previa accreta
was 82.4% (14/17) and the specificity 96.8% (61/63). The

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Placenta previa accreta

32
Table 1 A summary of patient history, color Doppler imaging (CDI) features and outcome of 14 cases of placenta accreta. Outcome is shown as birth weight, with Apgar scores at 1 and 5 min in parentheses
Gestational age
at diagnosis
(weeks)

CDI features

Gestational age
at delivery
(weeks)

2 LSCS

30

Diffuse LF

31

2*
3

None
1 LSCS

34
35

Diffuse LF
Focal LF

37
38

4
5
6
7
8

1
2
1
2
1

LSCS
LSCS
D&C
D&C
D&C

36
28
34
32
16

Focal
Focal
Focal
Focal
Focal

9
10
11

3 LSCS
1 LSCS
1 LSCS

27
34
28

12
13
14

2 D&C
2 D&C
3 D&C

32
29
32

Focal LF
Focal LF
UB hypervascularity,
focal LF
Dilated SPC
Dilated SPC
Dilated SPC

LF
LF
LF
LF
LF

Estimated
blood loss
(ml)

Complications

Pathology

Outcome

Indication for
delivery

Operative management

Increta

1655 g (6/8)

APH

CH

9400
6200

Cystotomy, wound
infection
None
None

Increta
Accreta

2985 g (7/8)
3090 g (8/9)

APH
APH

38
34
38
36
31

4000
4000
3200
2400
2300

None
Cystotomy
None
None
None

Accreta
Accreta
Accreta
Increta
Accreta

2670
2140
3050
2535
1670

(8/9)
(7/8)
(8/9)
(8/9)
(2/5)

Elective
APH
Elective
Elective
APH

35
38
32

2000
1040
1800

None
None
None

Accreta
Increta
Increta

3305 g (6/8)
2885 g (8/9)
1960 g (6/7)

Elective
Elective
Elective

CH
Attempt to remove
placenta; CH
CH
CH
CH
CH
Attempt to remove
placenta; defect oversewn
CH
CH
CH

34
32
37

4900
4000
2000

None
None
None

Increta
Accreta
Accreta

2390 g (7/9)
1920 g (6/7)
2910 g (7/9)

APH
APH
Elective

CH
CH
CH

15 00
0

g
g
g
g
g

LSCS low segment cesarean section; LF lacunar flow; APH antepartum hemorrhage; CH cesarean hysterectomy; D&C dilatation and curettage; UB uterusbladder interphase;
SPC subplacental venous channels; *, case of term pregnancy in rudimentary horn

M.M. Chou et al.

Ultrasound in Obstetrics and Gynecology

No.

Prior
surgery

Placenta previa accreta


positive and negative predictive values were 87.5% (14/16)
and 95.3% (61/64), respectively.

D I S CU S SI O N
Sonography is useful in screening for placenta previa
accreta. Previous reports have emphasized the B-mode
gray-scale sonographic findings58, and others have emphasized the color and power Doppler findings914. The
conventional gray-scale ultrasonographic assessment of
placenta previa accreta relies on the demonstration of
morphological features, such as loss of a normal subplacental anechoic zone, sonolucent placental lakes, abnormal
bladderuterine wall interphase and pulsatile flow into
hypoechogenic spaces48,14. These features have been
shown to be highly specific for placenta previa accreta,
and were adequate for the evaluation of most placentas.
Finberg and Williams found that gray-scale ultrasound had
a sensitivity of 93% (14/15) and a specificity of 79%
(15/19) in the diagnosis of placenta accreta7. However, they
suggested that a simple yesno declaration as to the presence
of placenta accreta was inadequate. They recommended
that a tentative diagnostic probability statement be given.
With the advent of color Doppler technology, several
authors have described the color Doppler sonographic
features of placenta previa accreta:
1. Diffuse or focal intraplacental lacunar flow with
high-velocity turbulent venous-type flow.
2. Abnormal blood vessels linking the placenta to the
bladder, with high diastolic arterial blood flow.
3. Dilated peripheral subplacental vascular channels
with pulsatile venous-type flow over the uterine cervix,
or absence of subplacental vascular signals in the areas
lacking the peripheral subplacental hypoechoic zone914.
In our study, we found that the variable vascular
morphological manifestations of placenta previa accreta
were exhibited and could be correctly identified by
transabdominal color Doppler ultrasound. The sensitivity
and specificity of color Doppler imaging for diagnosing
placenta previa accreta, especially anterior placenta
accreta, have been high, because abnormal uteroplacental
hypervascularity caused by the angiogenesis of placental
invasion can be detected with a high level of confidence.
Lerner and colleagues12 reported the sensitivity as 100%
(5/5) and the specificity as 94% (15/16). Levine and
colleagues14 found that color Doppler imaging had a
sensitivity of 86% (6/7) and a specificity of 92% (11/12).
Our transabdominal color Doppler diagnostic efficacy was
comparable with that of previous reports. At this time,
color Doppler evaluation of a placenta accreta has not
been shown to have superior sensitivity to gray-scale Bmode sonographic evaluation. However, the advantages
that color Doppler ultrasound provide are a greater
specificity in the diagnosis of placenta accreta and a better
assessment of the depth of myometrial or serosal invasion15.
In this study, two patients had false-positive results and
presented with color Doppler evidence of abnormal
bladderuterine serosa interphase hypervascularity which
was assumed to be placenta accreta. This mistaken

Ultrasound in Obstetrics and Gynecology

M.M. Chou et al.


interphase hypervascularity was actually caused by bladder
varices, possibly due to neovascularized vessels from
previous cesarean deliveries. Therefore, we suggest that,
in such patients with findings suggestive of interphase
hypervascularity, color Doppler imaging should clearly
demonstrate that there are abnormal blood vessels linking
the placenta to the bladder. In addition, focal lacunar flow
around the suspicious placentamyometrial region must be
specifically sought. In the three patients with false-negative
color Doppler results, one had a twin pregnancy with
breech and transverse malpresentation and two separate
anterior and lateral placentas. In this patient, the color
Doppler imaging diagnostic errors were due to shadowing
by fetal parts and lateral placenta location. The remaining
two patients had posterior-type placenta previa. The
posterior and lateral uterine wall invasion was difficult to
evaluate by ultrasound. Levine and colleagues14 suggested
that, in those patients with posteriorly implanted placenta
at risk for accreta, magnetic resonance imaging should be
used when ultrasound could not rule out the presence of
accreta.
The placenta in abdominal pregnancy and rudimentary
horn pregnancy should also cause concern. Abdominal
pregnancy is considered by some to be a form of placenta
accreta, because the placenta does not deliver spontaneously8,16. According to Benirschke16, the placental floor
lacks decidua and a large vascular supply supports the
intervillous circulation. Our color Doppler studies of one
patient with term abdominal pregnancy showed placental
tissue impinging upon the urinary bladder simulating
placenta previa. Placental hypervascularization was also
detected by transabdominal color Doppler ultrasound
(Figure 5). These sonographic features confirmed that
an extraordinary local vascular development of the
placental circulation occurs in abdominal pregnancy.
Therefore, we advise that the sonographer should carefully
search for a displaced uterus elsewhere if placenta previa
accreta is suspected, as illustrated in our patient.
Placenta accreta in a rudimentary horn pregnancy was
reported for the first time by Heinonen in 198317. In a
MEDLINE review by Basbug and coworkers18 of the 51
cases with rudimentary horn pregnancies, seven cases were
associated with placenta accreta (13.7%), suggesting that
rudimentary horn pregnancy is more likely to be associated
with placenta accreta than with an intrauterine pregnancy.
In our study, we encountered one case of term pregnancy in
the rudimentary horn of a unicornuate uterus. The
characteristic color Doppler features were multiple areas
of placenta implantation with a diffuse-type lacunar flow
pattern19.
Color power Doppler ultrasonography, a new diagnostic
modality, has been used to define and clarify the color
Doppler imaging findings for placenta accreta13,14. In our
study, the preliminary results showed that it could be
utilized as an adjunct to existing gray-scale B-mode and
color Doppler imaging in evaluating the vascular morphological patterns of placenta previa accreta.
Our study indicated that, if the transabdominal color
Doppler showed a diffuse lacunar flow pattern and a

33

Placenta previa accreta

b
Figure 5 Placenta accreta in an advanced abdominal pregnancy.
(a) Midline sagittal scan of the pelvis at 36 weeks gestation showing
placenta impinging upon the bladder without an intervening hypoechoic
zone. (b) Color Doppler energy further defining the extraordinary
placental vascular development. B bladder; P placenta.

bladderuterine serosa interphase hypervascularity pattern,


urological assessment, including cystoscopy and pre- or
intraoperative placement of a ureteral stent should be
considered. We suggest that the technique of cesarean
hysterectomy as described by Catanzarite and co-workers4
should be performed. If there are large engorged blood
vessels seen within the visceral peritoneum covering the
lower uterine segment, extending to the top of the bladder,
we would perform a high fundal classical incision at least
2 cm above the upper margin of the adherent placenta to
avoid injuring the hypervascularity region in the lower
uterine segment. In such a case, we would not attempt to
remove the placenta. At the beginning of this study, in
patient no. 3, we attempted to remove the placenta because
of lack of clinical experience, which caused massive
vaginal bleeding of 800 ml/min. The uterine blood
invisibly drained away from the vagina down the operating
table and the delivery floor was flooded with the blood,
causing a life-threatening hemorrhagic complication. Since
this painful experience, we have learned that, if the
combination of the color Doppler findings and the clinical
uterine hypervascularity appearance during surgery are

34

M.M. Chou et al.


highly suggestive of a placenta previa accreta, we strongly
advise against trying to remove the placenta4. During
hysterectomy, we often use intentional cystotomy and
place two fingers downward to guide the dissection of the
adherent bladder wall, applying the Penrose drain tourniquet technique to compress the lower uterine segment in an
attempt to reduce blood flow to the uterus. Furthermore, a
ureteral stent passage is often made preoperatively (via
cystoscopy) or intraoperatively (via cystotomy) to facilitate
recognition of the ureters; this may prevent the ureteral
injuries and the trigone of the bladder. Additional reported
procedures used to reduce intraoperative blood loss
include balloon occlusion and embolization of the internal
iliac arteries and two-stage conservative management
(hysterectomy at 24 weeks postpartum)20,21.
Our results also showed that there was a significant risk
of life-threatening hemorrhagic complication, particularly
among patients with a diffuse lacunar flow pattern. Ideally,
the delivery should be performed electively at the gestational age of proven lung maturity8. Often, however,
bleeding will prompt surgical intervention sooner4. Therefore, we suggest that the timing of cesarean hysterectomy
should be made according to the hemodynamic morphological features found on color Doppler imaging. We
suggest that it may be appropriate to consider performing
the elective cesarean hysterectomy at 34 weeks of gestation
or even earlier in some cases, irrespective of fetal lung
maturity, in patients with a diffuse lacunar flow pattern
particularly associated with strong evidence of extensive
placenta incretapercreta and episodes of antepartum
hemorrhage, in order to decrease the incidence of maternal
morbidity and mortality associated with emergency
surgery. OBrien and colleagues22 reported that 50% of
maternal deaths secondary to placenta percreta occurred
after 35 weeks gestation, emphasizing the greater risk of
severe spontaneous hemorrhage with increasing gestational
age. Adequate preparation for massive blood transfusion,
an experienced surgical and anesthetic team and intensive
hemodynamic monitoring will reduce the incidence of
maternal morbidity and mortality. However, for patients
with a focal lacunar flow pattern, an uneventful cesarean
hysterectomy can usually be performed at more advanced
gestation (3638 weeks). Further studies are necessary to
validate our suggestions.
In conclusion, we believe that any persistent placenta
previa, particularly in patients associated with prior
cesarean section, must benefit from elaborate prenatal
transabdominal color Doppler ultrasound studies to
identify abnormal uteroplacental vascular flow patterns.
In our studies, color Doppler findings further validated the
conventional gray-scale sonographic features. Furthermore, these findings clearly aided in the approach and
management of this most challenging obstetric disorder.
The extent and severity of hemodynamic changes of the
uteroplacental circulation in placenta previa accreta must
be taken into account, and each case must be managed
individually according to the variable vascular morphological patterns, which are detected and categorized by
transabdominal color Doppler ultrasound.

Ultrasound in Obstetrics and Gynecology

Placenta previa accreta

ACKN OW LE D G E M E NTS
This study was supported by the Medical Research Council
(Grant nos 876405A and 886406A) of the Taichung
Veterans General Hospital, Taiwan.

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