Ultrasonographic Prediction of Placental Invasion in Placenta Previa by Placenta Accreta Index
Ultrasonographic Prediction of Placental Invasion in Placenta Previa by Placenta Accreta Index
Ultrasonographic Prediction of Placental Invasion in Placenta Previa by Placenta Accreta Index
Clinical Medicine
Article
Ultrasonographic Prediction of Placental Invasion in Placenta
Previa by Placenta Accreta Index
Keita Hasegawa 1 , Satoru Ikenoue 1, * , Yuya Tanaka 1 , Maki Oishi 1 , Toyohide Endo 1 , Yu Sato 1 , Ryota Ishii 2 ,
Yoshifumi Kasuga 1 , Daigo Ochiai 3 and Mamoru Tanaka 1
1 Department of Obstetrics and Gynecology, Keio University School of Medicine, 35 Shinanomachi, Sinjuku,
Tokyo 1608582, Japan
2 Department of Clinical Trial and Clinical Epidemiology, University of Tsukuba Faculty of Medicine,
1-1-1 Tennodai, Tsukuba 305-8577, Japan
3 Department of Obstetrics and Gynecology, Kitasato University School of Medicine, 1-15-1 Kitazato,
Minami, Sagamihara 252-0375, Japan
* Correspondence: sikenoue.a3@keio.jp; Tel.: +81-3-3353-1211; Fax: +81-3-3226-1667
Abstract: This study aimed to investigate the diagnostic accuracy of the placenta accreta index
(PAI) for predicting placenta accreta spectrum (PAS) in women with placenta previa. We analyzed
33 pregnancies with placenta previa at Keio University Hospital. The PAI was assessed in the early
third trimester, and PAS was diagnosed histologically or clinically defined as retained placenta after
manual removal attempts. The PAI and incidence of PAS were analyzed. Ten women (30%) were
diagnosed with PAS and had higher volumes of perioperative bleeding (p = 0.016), higher rate of
requiring uterine artery embolization (p = 0.005), and peripartum hysterectomy (p = 0.0002) than
women without PAS. A PAI > 2 was the most useful cut-off point for predicting PAS and was more
sensitive than prediction values using traditional evaluation (history of cesarean section and placental
location). Post-hoc analysis revealed a higher rate of previous history of cesarean delivery (30% vs.
4.4%, p = 0.038), severe placental lacunae (≥grade2) (70% vs. 8.7%, p = 0.0003), thin myometrial
thickness (90% vs. 22%, p = 0.0003), anterior placenta (100% vs. 30%, p = 0.0002), and presence of
Citation: Hasegawa, K.; Ikenoue, S.;
bridging vessels (30% vs. 0%, p = 0.0059) in PAS women. PAI could help predict the outcomes of
Tanaka, Y.; Oishi, M.; Endo, T.; Sato,
Y.; Ishii, R.; Kasuga, Y.; Ochiai, D.;
women with placenta previa with and without a history of cesarean delivery to reduce PAS-induced
Tanaka, M. Ultrasonographic perinatal complications.
Prediction of Placental Invasion in
Placenta Previa by Placenta Accreta Keywords: placenta accreta spectrum; placenta previa; ultrasonography; placenta accreta index
Index. J. Clin. Med. 2023, 12, 1090.
https://doi.org/10.3390/
jcm12031090
1. Introduction
Academic Editor: Rinat
Gabbay-Benziv Placenta accreta spectrum (PAS) is first suspected when placenta previa is identified
because 9.3% of placenta previa cases are associated with PAS [1]. Although the mortality
Received: 12 December 2022
rate of women with PAS has improved from 6–7% [2] to 0.05% recently [3], PAS is related
Revised: 27 January 2023
to an increased risk of perinatal complications and interventions, such as excessive peri-
Accepted: 29 January 2023
partum bleeding requiring blood transfusion, uterine artery embolization, and peripartum
Published: 31 January 2023
hysterectomy. Therefore, predicting PAS in the antepartum period is crucial because it is a
means to decrease maternal morbidity/mortality.
Ultrasonography is the mainstay of prenatal diagnosis and monitoring, as well as
Copyright: © 2023 by the authors. preoperative prediction of PAS, and has a high accuracy for prenatal diagnosis of invasive
Licensee MDPI, Basel, Switzerland. placentation in high-risk pregnancies [4]. Rac et al. [5] recently reported using the placenta
This article is an open access article accreta index (PAI) scored by ultrasonography for predicting PAS; however, validation and
distributed under the terms and replication studies for PAI are limited. Additionally, a previous study on the use of PAI
conditions of the Creative Commons only recruited women with a history of cesarean delivery [5]. It is well known that women
Attribution (CC BY) license (https:// without a history of cesarean delivery also have an increased risk of the adherent placenta
creativecommons.org/licenses/by/ in case of placenta previa [1].
4.0/).
Therefore, we aimed to investigate and validate the clinical utility of the PAI to predict
PAS in women with placenta previa both with and without a history of cesarean delivery.
Table 1. Clinical values of obstetric parameters for evaluating the placenta accreta index.
3. Results
Maternal characteristics and perinatal outcomes are summarized in Table 2. Of the
33 women with placenta previa, 10 (30%) were diagnosed with PAS, and 23 did not
have PAS. The PAS group showed a significantly larger volume of perioperative bleeding
and higher rates of uterine artery embolization and peripartum hysterectomy than the
non-PAS group.
PAS Non-PAS
p-Value
n = 10 n = 23
Maternal age, years 39 ± 3.3 38 ± 5.2 0.59
BMI, kg/m2 20 ± 3.0 22 ± 3.6 0.12
Nulliparas 4 (40%) 15 (65%) 0.17
Gestational age at delivery, weeks 35.2 ± 1.5 35.5 ± 2.4 0.51
Perioperative blood loss, g 2913 ± 1314 1650 ± 841 0.01
Uterine artery embolization 6 (60%) 3 (13%) <0.01
Blood transfusion 9 (90%) 14 (61%) 0.09
Peripartum hysterectomy 5 (50%) 0 (0%) <0.01
Birth weight, g 2372 ± 427 2333 ± 505 0.83
Apgar score at 1 min < 7 2 (20%) 7 (30%) 0.54
Apgar score at 5 min < 7 0 (0%) 3 (13%) 0.23
Continuous variables are presented as means ± standard deviations. Categorical variables are presented as n (%).
Statistically significant p-values are shown in bold text. Abbreviations: BMI, body mass index, PAS, placental
accreta spectrum.
The ROC curve predicting PAS using the PAI showed an AUC of 0.974 (95% confidence
interval [CI], 0.925–1.00). A PAI > 2 was indicated as the most useful cut-off point for PAS
prediction, with a sensitivity of 0.900 (95% CI, 0.555–0.997); specificity, 0.957 (95% CI,
0.781–0.999); positive predictive value, 0.900 (95% CI, 0.555–0.997); negative predictive
value, 0.957 (95% CI, 0.781–0.999) (Table 3). These values were higher than the prediction
rate of PAS based on the traditionally evaluated information (history of cesarean delivery
and anterior placental location: sensitivity, 0.300; specificity, 0.957; positive predictive value,
0.750; negative predictive value; 0.759). Seven (70%) out of 10 women with PAS had no
previous cesarean delivery, all of whom had a PAI > 2. Of the seven women with PAS
without a history of cesarean delivery, five (71%) were aged above 35, three (43%) received
infertility treatments, and only one (14%) had a history of uterine artery embolization.
Table 3. Sensitivity, specificity, and positive and negative predictive values corresponding to each
PAI score.
PAI Non-PAS PAS Sensitivity (95% CI) Specificity (95% CI) PPV (95% CI) NPV (95% CI)
>0 9 10 100.0 [69.2–100.0] 60.9 [38.5–80.3] 52.6 [28.9–75.6] 100.0 [76.8–100.0]
≤0 14 0
>1 5 10 100.0 [69.2–100.0] 78.3 [56.3–92.5] 66.7 [38.4–88.2] 100.0 [81.5–100.0]
≤1 18 0
>2 1 9 90.0 [55.5–99.7] 95.7 [78.1–99.9] 90.0 [55.5–99.7] 95.7 [78.1–99.9]
≤2 22 1
>3 1 5 50.0 [18.7–81.3] 95.7 [78.1–99.9] 83.3 [35.9–99.6] 81.5 [61.9–93.7]
≤3 22 5
>4 1 5 50.0 [18.7–81.3] 95.7 [78.1–99.9] 83.3 [35.9–99.6] 81.5 [61.9–93.7]
≤4 22 5
>5 0 2 20.0 [2.5–55.6] 100.0 [85.2–100.0] 100.0 [15.8–100.0] 74.2 [55.4–88.1]
≤5 23 8
Values are presented as median (Interquartile range). Abbreviations: PAI, placenta accreta index, PAS, placental
accreta spectrum, PPV, positive predictive value, NPV, negative predictive value, CI, confidence interval.
J. Clin. Med. 2023, 12, 1090 4 of 7
The post-hoc analysis of the five parameters of the PAI score revealed significantly
higher rates of previous cesarean deliveries ≥ 2 (30% vs. 4.4%, p = 0.038), placental lacunae
≥ Grade 2 (70% vs. 8.7%, p = 0.0003), myometrial thickness ≤ 5 mm (90% vs. 22%,
p = 0.0003), placenta adhering to the anterior wall of the uterus (100% vs. 30%, p = 0.0002),
and presence of bridging vessels to the bladder (30% vs. 0%, p = 0.0059) in the PAS group
than in the non-PAS group.
4. Discussion
As previously reported, our study replicated the finding that PAS is associated with
an increased risk of perinatal complications and requiring uterine artery embolization.
Moreover, the present study indicated the clinical utility and significance of the PAI to pre-
dict PAS preoperatively in women with placenta previa both with and without a previous
history of cesarean delivery, whereas previous study applied PAI only for women with a
history of cesarean delivery [5]. In particular, a PAI > 2 indicated a practical cut-off point to
predict PAS in women with placenta previa.
As expected, in the present study, the PAS group showed a significantly increased
number of perioperative complications, including a larger amount of perioperative bleed-
ing, a higher rate of uterine artery embolization, and peripartum hysterectomy than the
non-PAS group. Per previous reports, PAS is associated with a significantly higher risk of
blood transfusion (46.9%) and peripartum hysterectomy (52.2%) [3,8,9] which is consistent
with this study’s findings. The PAI assessment may be clinically important for women
with suspected placental invasion to reduce perinatal complications and maternal mortality
associated with PAS.
The present study revealed that the PAI has high diagnostic accuracy for PAS. In
particular, a PAI > 2 could be a useful cut-off point to predict PAS. Rac et al. [5] did not
present a cut-off point for the PAI, but used it to help with risk stratification and coun-
seling. Meanwhile, the present study suggests that PAI > 2 is useful for predicting PAS
in women with and without a previous history of cesarean delivery. Of the five param-
eters comprising the PAI evaluated in this study (history of cesarean delivery, presence
of placental lacunae, smallest myometrial thickness, placental location, and presence of
bridging vessels to the bladder), significant differences were identified in all parameters
between the PAS and non-PAS groups. We also reported on several ultrasonographic
parameters that are associated with PAS. The sensitivity of placental lacunae for iden-
tifying placenta accreta was reported as 75% [10]. The sensitivity and specificity of the
loss of the clear zone for identifying placenta accreta were reported as 74.9% and 76.9%,
respectively [10]. Another study showed that the sensitivity, specificity, and positive and
negative predictive values of placenta accreta using ultrasound findings were 53.3%, 88.1%,
82.1%, and 64.8%, respectively [11]. The prediction parameters calculated in the present
study using the PAI were greater than those calculated in previous reports. On this basis,
the diagnostic accuracy of PAI for PAS could be superior to the single ultrasonographic
parameter-based method.
Happe et al. validated the predictability of the PAI for PAS by using 79 PAS cases, but
only for women who had a history of previous cesarean delivery [12]. In fact, prior cesarean
delivery has a large influence on PAI scoring [5], and the higher prevalence of cesarean
deliveries has led to an increased incidence of PAS [13]. However, it is well known that
women diagnosed with placenta previa even without previous cesarean delivery have an
increased risk of PAS [1]. Indeed, the present study included seven (70%) women with PAS
without a history of cesarean delivery, all of whom presented with PAI >2 and increased
risk of PAS. The present findings potentially expand the utility of PAI for PAS prediction in
patients even without a previous history of cesarean delivery.
Magnetic resonance imaging (MRI) is another modality used to predict PAS and MRI
findings have been reported to be useful to define the topography and area of placental
invasion [14,15]. Berkley et al. [16] reported that the sensitivity of MRI is 80–85% and the
specificity is 65–100%. Fiocchi et al. [17] reported that MRI has 100% sensitivity and 92.3%
J. Clin. Med. 2023, 12, 1090 5 of 7
specificity for the prediction of PAS. However, MRI may also mislead the diagnosis of PAS
using ultrasonography [18], and it is not cost-effective as a screening tool for PAS. In this
study, we revealed similar sensitivity and specificity of the PAI as for MRI for predicting
PAS, indicating that the PAI has a high rate of diagnostic accuracy and exclusive diagnosis.
Given these results, predicting PAS using ultrasonography may be preferable to using MRI.
Our study and a previous study have demonstrated the diagnostic accuracy of PAS
using the PAI. However, Rac et al. [12] reported that the PAI could not help predict the
depth of placental invasion. Recently, machine learning models have been used to predict
the clinical outcomes in women with placenta accreta spectrum [19]. Because the severity of
PAS (e.g., depth of placental invasion) is associated with increased maternal morbidity [20],
further investigations including machine learning method and serum biomarkers are
warranted to predict the severity of perioperative complications (blood loss, uterine artery
embolization, and hysterectomy).
In our study, there were several strengths and limitations. The first strength was
that the PAI was scored preoperatively and reviewed by a single observer, which could
avoid observation bias and interobserver differences. The second strength was that the
effectiveness of other prediction methods had not been demonstrated. Maternal serum
alpha-fetoprotein, free beta-human chorionic gonadotropin [21,22], antithrombin III, PAI-1,
soluble Tie2, and soluble vascular endothelial growth factor receptor 2 have been shown
as biomarkers to predict PAS [23]. In addition, the maternal serum VEGF and Serum
Cripto-1 levels have been reported as novel biomarkers to predict abnormally invasive
placenta [24,25]. These biomarkers might aid clinicians additionally to ultrasonography
in detecting PAS cases in the early weeks of gestation. Meanwhile, the first limitation
was a small sample size, which might affect the statistical power of the present results.
In addition, women with PAS in the present study had risk factors besides a history of
cesarean delivery. The second limitation of our study was that patients with PAS accounted
for approximately 30% of all the placenta previa cases, which is higher than the general
frequency [1]. This may be related to the fact that our institution is a tertiary center and
that many of our patients are elderly or post-IVF pregnant women. The fact that our
institution is a tertiary center also resulted in high rates of blood loss, blood transfusion
and embolization in the non-PAS group despite 65% being nulliparas without PAS. The
third limitation was that systematic bias may have occurred because the observer could
not be blinded to the patients’ risk factors completely. The last limitation was that we
performed uterine artery embolization to preserve the uterus on maternal request for PAS
cases where the placenta was found to be invading the uterine wall at cesarean delivery,
where the placenta was retained after attempts at manual removal. Hence, these PAS cases
were diagnosed clinically, and there was a lack of pathological evaluation.
In conclusion, the present study confirmed the clinical significance of the PAI in
predicting PAS preoperatively in women with placenta previa, regardless of prior history
of cesarean delivery. In particular, a PAI >2 was found to be a valid cut-off point to
predict PAS in women who had placenta previa with and without a previous history of
cesarean delivery. Assigning a PAI score could be clinically important to avoid perinatal
complications and reduce maternal mortality associated with PAS.
Author Contributions: All authors accept responsibility for the paper as published. K.H. and
S.I. researched data, wrote the manuscript, contributed to discussion, and reviewed/edited the
manuscript. Y.T., M.O., T.E., Y.S., Y.K., D.O. and M.T. contributed to the discussion and reviewed the
manuscript. R.I. contributed to data analyses and reviewed the manuscript. All authors have read
and agreed to the published version of the manuscript.
Funding: This work was supported in the writing of the report by the Japan Society for the Promotion
of Science (JSPS) KAKENHI, Grant Number 22K16864.
Institutional Review Board Statement: The study was conducted according to the guidelines of
the Declaration of Helsinki, and approved by the Ethics Committee of Keio University School of
Medicine (No. 20030107).
J. Clin. Med. 2023, 12, 1090 6 of 7
Informed Consent Statement: As all information was anonymous in the institutional database,
informed consent from each included woman patient was not needed.
Data Availability Statement: The data presented in this study are available on reasonable request
from the corresponding author.
Acknowledgments: The authors thank all the medical staff at the Keio University Hospital who
contributed to the excellent patient care for patients included in this study.
Conflicts of Interest: The authors declare no conflict of interest.
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