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Ultrasound Obstet Gynecol 2016; 48: 504–510

Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/uog.15813

Prediction of morbidly adherent placenta using a scoring


system
J. TOVBIN*, Y. MELCER*, S. SHOR*, M. PEKAR-ZLOTIN*, S. MENDLOVIC†, R. SVIRSKY*
and R. MAYMON*
*Department of Obstetrics and Gynecology, Assaf Harofeh Medical Center, Zerifin, Israel; †Department of Pathology, Assaf Harofeh
Medical Center, Zerifin, Israel, affiliated with the Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel

K E Y W O R D S: Doppler; morbidly adherent placenta; prenatal diagnosis; scoring system; ultrasound

ABSTRACT Conclusions Our proposed scoring system is highly


predictive of MAP in patients at risk. This allows
Objective To evaluate the accuracy of an ultrasound-
an adequate multidisciplinary team approach for the
based scoring system for diagnosing morbidly adherent
planning and timing of delivery in such cases. Copyright
placenta (MAP).
© 2015 ISUOG. Published by John Wiley & Sons Ltd.
Methods This study included pregnant women referred
to our ultrasound unit during 2013–2015 because of
INTRODUCTION
suspected MAP on a previous ultrasound examination
or because they had at least one previous Cesarean Morbidly adherent placenta (MAP) defines a spectrum
delivery. All women were assessed using a scoring system of conditions, including placenta accreta, increta and
based on the following: number and size of placental percreta, which are associated with significant maternal
lacunae; obliteration of the demarcation between the and fetal morbidity and mortality1 . As a result of
uterus and placenta; placental location; color Doppler the notably increased rate of Cesarean deliveries, the
signals within placental lacunae; hypervascularity of the reported incidence of placenta accreta has increased from
placenta–bladder and/or uteroplacental interface zone; approximately 0.8 per 1000 deliveries in the 1980s to 3
and number of previous Cesarean deliveries. Each per 1000 deliveries in the past decade2 . Placenta previa
criterion was assigned 0, 1 or 2 points and the sum and previous uterine surgery represent the major risk
of points yielded the final score. Patients were classified factors for MAP1,3 – 12 .
into low, moderate or high probability for MAP based Antenatal diagnosis of MAP and a multidisciplinary
on the final score. The presence of MAP was determined team approach to care have the potential to reduce
by the surgeon at delivery and clinical descriptions were maternal and fetal intrapartum complications, including
documented in the electronic patient file. Pathological maternal blood loss, requirement for transfusion, hys-
diagnoses were available only in cases that underwent terectomy, intraoperative urological and gastrointestinal
hysterectomy. injuries, and even maternal death13 – 16 .
Results In total, 258 pregnant women were included Ultrasound evaluation, with grayscale and color
in the study, of whom 23 (8.9%) were diagnosed with Doppler imaging, is the recommended first-line modality
MAP. There was a statistically significant difference in for diagnosing MAP17,18 . Grayscale ultrasound features
the prevalence of MAP when women were grouped suggestive of placenta accreta include the loss of
according to the scoring system, with 0.9%, 29.4% and myometrial interface or retroplacental clear space,
84.2% in the low, moderate and high probability groups, reduced myometrial thickness and the presence of
respectively (P < 0.0001). All sonographic criteria of the intraplacental lacunae19 – 37 .
scoring system were significantly associated with MAP The next step in predicting placental invasion by
(P < 0.0001). Receiver–operating characteristics (ROC) ultrasound is to integrate some of the abovementioned
curves for prediction of MAP using the number of individual sonographic parameters associated with MAP
placental lacunae and obliteration of the uteroplacental into a well-defined scoring system. Previous investigators
demarcation yielded an area under the ROC curve of 0.94 have proposed a standardized evaluation of women at
(95% CI, 0.86–1.00). risk for MAP38,39 . However, these reports were based on

Correspondence to: Prof. R. Maymon, Department of Obstetrics and Gynecology, Assaf Harofeh Medical Center, Zerifin, 70300, Israel
(e-mail: maymonrb@bezeqint.net)
Accepted: 11 November 2015

Copyright © 2015 ISUOG. Published by John Wiley & Sons Ltd. ORIGINAL PAPER
Scoring system for prediction of morbidly adherent placenta 505

small retrospective studies and both groups recommended Table 1 Detailed scoring system for ultrasound evaluation of
further study to validate their scoring model. suspected morbidly adherent placenta according to six different
criteria
In the current study, our aim was to develop a scoring
system for predicting MAP based on an assessment of Parameter Score
ultrasound and clinical characteristics in a cohort of
women at risk of MAP. Based on the assessment outcome, Number of previous Cesarean deliveries
1 1
patients were offered specific antepartum and intrapartum
≥2 2
management. Lacuna maximum dimension
≤ 2 cm 1
> 2 cm 2
SUBJECTS AND METHODS Number of lacunae
≤2 1
We conducted a single-center study for predicting MAP in >2 2
high-risk pregnant women attending our ultrasound unit Obliteration of uteroplacental demarcation 2
between December 2013 and February 2015 for suspected Location of placenta
MAP on an ultrasound examination performed elsewhere Anterior 1
or at least one previous Cesarean delivery. All women Placenta previa 2
were recruited and scanned during either the second Doppler assessment
Blood flow in placental lacunae 1
or third trimester of pregnancy using two-dimensional Hypervascularity of placenta–bladder 2
(2D) grayscale imaging and color Doppler flow mapping. and/or uteroplacental interface
Inclusion criteria were one or more of the following:
previous Cesarean delivery, myomectomy, history of
adherent placenta, ultrasound suspicion of MAP. Patients
were excluded from the study if they did not deliver at this physician in consultation with another one (R.M.
our hospital. The study was approved by the Institutional and J.T.).
Review Board. The scoring system was used not only for stratifying
The examination was based on a scoring system, individual risk of MAP but also for counseling and
developed and used routinely in our department, that preoperative planning in each patient, by either raising
determines the probability for MAP. All ultrasound awareness of MAP or providing reassurance to women
images were reviewed and scored according to six different who desired a future pregnancy. As part of our protocol,
criteria (Table 1): number and size of placental lacunae all pregnant women with suspected MAP were followed
(an irregular area of low echogenicity larger than 1 × 1 cm up antenatally in a specialized clinic by a multidisciplinary
in the placental parenchyma40 ); obliteration of the medical team including an experienced sonographer, a
demarcation between the uterus and the placenta; number perinatologist, obstetricians and anesthesiologists, which
of previous Cesarean deliveries; placental location; and allows for multidisciplinary planning and delivery before
color Doppler assessment of flow in the placental lacunae the onset of labor and/or vaginal bleeding.
and placenta–bladder and/or uteroplacental interface The follow-up of patients with low probability of
hypervascularity27 – 35 . having MAP was based on obstetric indications other than
Each criterion was assigned 0, 1 or a maximum adherent placenta. If a woman categorized as medium or
of 2 points and the sum of the points obtained high probability was not hospitalized because of placenta
from each criterion yielded the final score. Based on previa or unrelated indications, we conducted follow-up
this suggested scoring system, patients were classified scans every 2–3 weeks. All women with a high probability
into one of three groups: low (≤ 5 points), moderate were seen at least once in a joint work-up meeting with a
(6–7 points) or high (8–12 points) probability for multidisciplinary team.
MAP (Figure 1 and Table 1). The images and Our antenatal care approach included supplemen-
measurements (obtained using electronic calipers) were tation with oral iron to maximize iron stores and
printed as a thermal hard copy for the patient oxygen-carrying capacity. In selected patients, concur-
record file. Only satisfactory ultrasound images were rent parenteral iron infusion was given preoperatively.
included for data processing. Ultrasound examinations Preoperative ultrasound mapping of the placental loca-
were performed with either a 2–5-MHz curvilinear tion was performed to assist in determining the optimal
transabdominal transducer or a 5–9-MHz transvaginal approach for abdominal wall and uterine incisions and to
probe. Ultrasound images and associated reports used avoid disturbance of the placenta before delivery of the
in the clinical management of each patient were stored fetus.
electronically in a picture-archiving and communication As part of our protocol, the results of the scoring system
system throughout the study period. Therefore each were reported to the patients and the surgical team. In
patient had both a hard copy and an archived electronic all cases of medium and high probability of MAP, a
file of the images. Each patient file was evaluated by preoperative checklist was completed to confirm that the
a single physician with expertise in imaging (R.M.) required preparations had been made and to identify
using the scoring system and all cases with high the name and contact information of the consultant in
probability of MAP were scanned and assessed by case they were needed for intraoperative or perioperative

Copyright © 2015 ISUOG. Published by John Wiley & Sons Ltd. Ultrasound Obstet Gynecol 2016; 48: 504–510.
506 Tovbin et al.

Figure 1 Scoring system for predicting morbidly adherent placenta in a case with two prior Cesarean deliveries (2 points). Obliteration of
demarcation ( ) between uterus and placenta (2 points). b, bladder. (b) Placental lacunar size ≥ 2 cm (arrow; 2 points). (c) Placenta previa
(note outline of cervix; 2 points). (d) Number of placental lacunae ≥ 2 cm (arrows; 2 points). (e) Hypervascularity between placenta and
bladder shown by color Doppler assessment (arrows; 2 points). The sum of points obtained from each criterion yields a maximum score of
12 points, indicating high probability of morbidly adherent placenta.

assistance18 . Thus patients who were classified as high a hysterectomy was decided at surgery dependent on
probability for MAP (8–12 points) underwent surgery the surgical findings. Pathological diagnoses were avail-
by a highly experienced senior obstetrician and a able only in cases that underwent wedge resection or
multidisciplinary team. Cesarean hysterectomy (Figure 2). The pathologist was
According to our protocol, in all cases of moderate not blinded to the suspected diagnosis but was blinded to
and high probability of MAP, preoperative consultation the sonographic score. All patients who underwent hys-
and notification of the blood bank was conducted and terectomy had massive placenta percreta diagnosed during
adequate access to replacement blood was secured. In surgery.
the high-risk group, an ultrasound examination was For the purpose of the current study, the medical
conducted by R.M. and J.T. just before surgery to map records of all cases were reviewed, and information
again the placenta and identify its location in the uterine regarding demographics, obstetric and gynecological
cavity in relation to the bladder and the array of various history, operative procedure and maternal postoperative
large blood vessels. complications was obtained for each probability group.
Patients with a low probability of MAP were scheduled Statistical analysis was conducted in the statistical labo-
for vaginal delivery if Cesarean section was not indicated ratory at Tel Aviv University using SPSS Statistics version
for other reasons. In these patients, the obstetric team 21 software (IBM Corp., Armonk, NY, USA). Continuous
waited for spontaneous placental separation and the variables are presented as mean ± SD or as median (range).
placenta was subsequently examined. MAP was defined Frequencies are presented as percentages. The accuracy of
in this group by failed attempts to remove the placenta the various criteria in discriminating MAP from non-MAP
during the third stage of labor. Patients with medium or was examined in terms of sensitivity, specificity, pos-
high probability of MAP were scheduled for Cesarean itive predictive value and negative predictive value. A
section at 36 weeks of gestation. two-tailed Fisher’s exact test or Pearson’s chi-square test
When gross placental invasion was evident at surgery was used to determine the association of various sono-
(Figure 2), massive bleeding occurred, the placenta was graphic criteria with the presence of MAP. A two-tailed
difficult to detach from the uterus or a part of the P-value < 0.05 was considered statistically significant.
placenta remained attached, the common practice in Logistic regression analysis was used to determine which
our institute was not to attempt to remove the pla- sonographic parameters of the scoring system were sig-
centa manually1 and a B-Lynch procedure or Cesarean nificantly associated with a clinical diagnosis of MAP by
hysterectomy was performed, where appropriate. The the surgeons. Odds ratios (OR) with 95% CIs are given.
presence and severity of placental adherence was deter- The receiver–operating characteristics (ROC) curves for
mined by the surgeons, and the clinical descriptions were the sonographic criteria and the composite score were
documented in the electronic patient file. The need for plotted.

Copyright © 2015 ISUOG. Published by John Wiley & Sons Ltd. Ultrasound Obstet Gynecol 2016; 48: 504–510.
Scoring system for prediction of morbidly adherent placenta 507

cv
d

cv

cv

Figure 2 Specimen showing morbidly adherent placenta diagnosed antenatally and managed by Cesarean hysterectomy. (a,b) Vasculari-
zation over uterine serosa was observed. (c) Hysterectomy specimen demonstrating morbidly adherent placenta. (d) The placenta had
invaded the myometrium and could not be separated from the uterus. (e) Chorionic villi (cv) had penetrated into necrotic decidua (d)
(hematoxylin and eosin stain, original magnification × 20). (f) Chorionic villus (cv) within necrotic decidua (hematoxylin and eosin stain,
original magnification × 40).

RESULTS 69.6% (16/23), 98.7% (232/235), 84.2% (16/19) and


97.1% (232/239), respectively. The positive and negative
In total, 268 patients were recruited during the study likelihood ratios were 54.5 and 0.31, respectively. The
period. Ten patients delivered elsewhere and were lost overall sensitivity (detection rate) of a high or moderate
to follow-up, and thus 258 women were included in the probability score diagnosing MAP was 91.3% (21/23)
study. Twenty-three (8.9%) women had a diagnosis of and the specificity was 93.6% (220/235).
MAP and 235 (91.1%) had no clinical evidence of an Logistic regression was used to examine the rela-
adherent placenta (Figure 3). The mean ± SD maternal tionship between sonographic variables found to be
age at ultrasound evaluation was 33.8 ± 4.5 years and significantly associated with MAP on univariable analysis
mean gestational age at diagnosis was 33.9 (range, and a clinical diagnosis of an invasive placenta, presented
16–41) weeks. Mean ± SD maternal gravidity and as OR (95% CI). The OR for MAP was 28.1 (95% CI,
parity were 4.0 ± 1.6 and 2.0 ± 1.2, respectively. Mean 5.34–147.67) for the presence of one placental lacuna
gestational age at delivery was 37.7 ± 1.7 (range, 24–41) and 220.7 (95% CI, 42.11–1156.84) when two lacunae
weeks. were present, which yielded the greatest prediction of
There was a statistically significant difference in the MAP. For obliteration of the uteroplacental demarcation,
prevalence of MAP when women were grouped according the OR was 87.24 (95% CI, 26.21–290.35). The OR for
to the probability category derived from the sonographic lacuna size ≤ 2 cm was 19.43 (95% CI, 4.86–77.57) and
score, with 0.9%, 29.4% and 84.2% in the low, moderate when lacuna size was > 2 cm, the OR was 203.23 (95%
and high probability groups, respectively (Figure 3) CI, 49.54–1493.26). The OR for Doppler flow in the pla-
(P < 0.0001). Two patients in the low-probability group cental lacunae was 29.73 (95% CI, 4.03–218.97) and for
had placental adherence (false negative), but this was placenta–bladder and/or uteroplacental interface hyper-
minimal and was not associated with significant blood vascularity was 79.28 (95% CI, 23.75–264.61). The OR
loss and postoperative outcome was normal in both cases. for anterior placenta was 2.7 (95% CI, 0.3–23.76) and
Nine (47.4%) of the 19 women in the high-probability for placenta previa was 83.7 (95% CI, 11.65–769.97).
group underwent Cesarean hysterectomy and in all cases The ROC curves for each sonographic parameter
the histopathological report confirmed the diagnosis of predicting MAP are shown in Figure 4. The ROC curve
MAP (Figure 2). Each individual sonographic parameter of the composite score of the number of placental
that we assessed in the scoring system was significantly lacunae and obliteration of the demarcation between
associated with MAP (P < 0.0001). The overall sensitivity, the uterus and placenta was plotted (Figure 5), yielding
specificity, and positive and negative predictive values an area under the ROC curve of 0.94 (95% CI,
of a high probability score diagnosing MAP were 0.86–1.00).

Copyright © 2015 ISUOG. Published by John Wiley & Sons Ltd. Ultrasound Obstet Gynecol 2016; 48: 504–510.
508 Tovbin et al.

Initial study
(n = 268)

Lost to follow-up
(n = 10)

Final study
(n = 258)

Low probability Moderate probability High probability


(n = 222; 86%) (n = 17; 6.6%) (n = 19; 7.4%)

+ – + – + –

(n = 2; 0.9%) (n = 220; 99.1%) (n = 5; 29.4%) (n = 12; 70.6%) (n = 16; 84.2%) (n = 3; 15.8%)

Figure 3 Flowchart summarizing detection rate of morbidly adherent placenta in low-, moderate- and high-probability groups. +, morbidly
adherent placenta; −, normal placentation. P < 0.0001, Pearson’s chi-square test.

1.0 1.0

0.8
0.8

0.6
Sensitivity

0.6
Sensitivity

0.4

0.4 0.2

0.2 0 0.2 0.4 0.6 0.8 1.0


1 – Specificity

Figure 5 Receiver–operating characteristics (ROC) curve for


0 0.2 0.4 0.6 0.8 1.0 prediction of morbidly adherent placenta using a combination of
1 – Specificity number of placental lacunae and obliteration of hypoechoic
uteroplacental demarcation (area under the ROC curve, 0.94 (95%
CI, 0.86–1.00)).
Figure 4 Receiver–operating characteristics (ROC) curves for
prediction of morbidly adherent placenta. Curves represent
prediction of probability of invasion using lacunar size ( ; Cesarean deliveries, the placental location and lacunae
area under the ROC curve (AUC), 0.89 (95% CI, 0.81–0.98)),
number of placental lacunae ( ; AUC, 0.92 (95% CI,
features, obliteration of the uteroplacental demarcation
0.85–0.99)), obliteration of demarcation between uterus and and color Doppler flow assessment was highly predictive
placenta ( ; AUC, 0.83 (95% CI, 0.72–0.95)), interface of MAP, allowing for antenatal and intrapartum
hypervascularity ( ; AUC, 0.87 (95% CI, 0.76–0.97)) and specific management. Although two (0.9%) of the 222
location of placenta ( ; AUC, 0.86 (95% CI, 0.77–0.95)). women in the low-probability group had MAP (false
negative), only minimal placental adherence was observed
DISCUSSION intraoperatively. They had both normal intrapartum
blood loss and postoperative outcome. In our series, the
Prenatal diagnosis of placenta accreta is paramount, most effective ultrasound criteria for detection of MAP
as most pregnant women with this condition are were a combination of two parameters, the number of
asymptomatic. Correct prenatal diagnosis allows time for placental lacunae and obliteration of the uteroplacental
a multidisciplinary team to make delivery plans, which demarcation, which yielded an area under the ROC
will help decrease surgical complications, maternal blood curve of 0.94 (95% CI, 0.86–1.00) (Figure 5). Previous
loss and prolonged intensive care unit admissions41 – 43 . reports showed similar results to ours19,29,31,44 – 46 ;
The main findings of the current study are that however, a prospective study that combines several
the sonographic score derived from the number of ultrasound parameters in one coherent scoring system

Copyright © 2015 ISUOG. Published by John Wiley & Sons Ltd. Ultrasound Obstet Gynecol 2016; 48: 504–510.
Scoring system for prediction of morbidly adherent placenta 509

Table 2 Summary of studies predicting placental invasion by a scoring system based on sonographic parameters associated with morbidly
adherent placenta (MAP)

Study Trimester Reference Women MAP


Reference design Inclusion criteria at scan standard Diagnostic criteria scanned (n) (%)

Rac Retro Previous CS and PP or 3 Pathology Location of placenta, loss of the 184 29
(2015)39 low-lying placenta retroplacental clear zone,
irregularity and thickness of the
uterus–bladder interface, the
smallest myometrial thickness,
presence of lacunar spaces and
bridging vessels
Gilboa Retro PP and previous CS or 3 Surgical findings, Presence and number of placental 109 69.7
(2015)38 placenta overlying pathology lacunae, interruption of the
any uterine scar or uterus–bladder interface,
ultrasound suspicion obliteration of demarcation
of MAP or findings between the uterus and the
of multiple lacunae placenta
Present Retro PP and/or previous CS 2–3 Surgical findings, Number and size of placental 258 8.9
study or ultrasound pathology lacunae, obliteration of
suspicion of MAP demarcation between uterus and
placenta

Only first author of each study is given. CS, Cesarean section; PP, placenta previa; Retro, retrospective.

to estimate the probability of MAP has not yet been the interface between the myometrium and the placenta
reported. may be difficult on conventional transabdominal ultra-
Two retrospective studies proposed a standardized sound during the late third trimester because the lower
evaluation of women at risk for MAP38,39 (Table 2). uterine segment appears as a thin line.
Gilboa et al.38 reported a series of 21 women with Assigning a score in clinical practice may be helpful
placenta percreta that was identified at surgery and in the antenatal diagnosis of MAP and seems to be
proposed a scoring system based on the sonographic a key factor in reducing maternal and fetal morbidity
findings. Their detection rate of placenta percreta was and mortality, by allowing multidisciplinary counseling,
63.6%. However, the main goal of their scoring system and planning and timing of delivery. During the
was to identify patients with Stage 3 MAP and offer antenatal period, care is taken to increase hemoglobin
a prophylactic pelvic artery catheterization. Rac et al.39 levels by administration of appropriate medication and
created a predictive equation for placental invasion to evaluate the patient for any potential obstetric
based on sonographic parameters that were studied in complications. Surgery is planned with an experienced
88 cases. surgeon, anesthetic and perinatal intensive care team.
The pathophysiology of placental lacunae is not In addition, an adequate number of blood units are
clear, although a strong relationship between lacu- made available in the operating room. This multitask
nar spaces and placental invasion has been described approach can only be achieved if early detection of
previously19,21,45,47,48 . Lacunae may be present even such a potentially life-threatening obstetric disorder is
in women with placenta previa without myometrial achieved.
invasion47 . Finberg and Williams19 found that the Some limitations of this study should be acknowledged.
number and abnormal appearance of lacunar spaces The main one was the fact that the surgical team
were directly correlated with certainty and severity of was not blinded to the ultrasound findings and the
MAP. In a recent systematic review, the overall pooled diagnosis of MAP during surgery was made by the
sensitivity and specificity from 13 studies of lacunar surgeons in all cases in which hysterectomy was avoided.
spaces diagnosing MAP was 77% and 95%, respec- Despite these limitations, the study presents a novel and
tively, with an overall diagnostic accuracy of 88.4%37 . effective method that enables preoperative preparation of
The rationale for including the presence or absence of women with MAP who are at risk of major maternal
the demarcation between the uterus and placenta in the complications.
suggested scoring system is based on the premise that inva- Factors such as maternal age, parity, mode of con-
sion of trophoblastic tissue into the myometrium and the ception and history of other uterine surgical procedures
absence of decidua basalis in invasive placentation pro- associated with MAP such as dilation and curettage, and
gressively lead to a reduction in myometrial thickness and endometrial ablation were not included in our model.
a loss of space between the myometrium and placenta31 . Additional studies are needed to validate our scoring
Cali et al.49 reported recently that the absence of the utero- system model, and to incorporate those parameters.
placental demarcation was the most effective sonographic In conclusion, the present simple ultrasound and
criterion for detection of an invasive placenta, with a neg- clinical scoring system may be highly predictive of MAP,
ative predictive value of 96.7%. However, evaluation of allowing for adequate antenatal risk assessment. It is

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510 Tovbin et al.

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