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Ultrasound in Med. & Biol., Vol. -, No. -, pp.

1–8, 2013
Copyright Ó 2013 World Federation for Ultrasound in Medicine & Biology
Printed in the USA. All rights reserved
0301-5629/$ - see front matter

http://dx.doi.org/10.1016/j.ultrasmedbio.2013.05.017

d Original Contribution

COMPARING THE DIAGNOSTIC VALUE OF ULTRASOUND AND MAGNETIC


RESONANCE IMAGING FOR PLACENTA ACCRETA: A SYSTEMATIC REVIEW
AND META-ANALYSIS

XINYUE MENG,* LIMEI XIE,* and WEIWEI SONGy


* Department of Ultrasound, Shengjing Hospital of China Medical University, Shenyang, China; and y Department of
Gynecology and Obstetrics, Shengjing Hospital of China Medical University, Shenyang, China

(Received 9 January 2013; revised 15 April 2013; in final form 24 May 2013)

Abstract—The aim of this study was to evaluate the diagnostic value of ultrasound (US) as compared with
magnetic resonance imaging (MRI) in the detection of placenta accreta. Sensitivity, specificity, summary receiver
operating characteristic curves and areas under the curve (AUCs) were described and calculated using Meta-Disc
Statistical Software, Version 1.4 (Unit of Clinical Biostatistics, Ram on y Cajal Hospital, Madrid, Spain). In the 13
studies included, US sensitivity was 83% (95% confidence interval [CI] 77%–88%), US specificity was 95% (95%
CI: 93%–96%) and the diagnostic odds ratio (DOR) was 63.41 (95% CI: 29.04–138.48). In the MRI studies, sensi-
tivity was 82% (95% CI: 72%–90%), specificity was 88% (95% CI: 81%–94%) and the DOR was 22.95 (95% CI:
3.19–165.11). Summary receiver operating characteristic analysis indicated that the diagnostic value of US in
detection of placenta accreta is not significantly different from that of MRI. Both US and MRI were highly sensitive
and specific in the detection of placenta accreta to support effective diagnostic methods. (E-mail: xielm72@yahoo.
cn) Ó 2013 World Federation for Ultrasound in Medicine & Biology.
Key Words: Ultrasound, Magnetic resonance imaging, Placenta accreta, Meta-analysis.

INTRODUCTION The risk of placenta accreta increases from 0.3% after


one prior cesarean section to 0.6%, 2.1%, 2.3% and
Placental invasion is characterized by abnormally firm
6.7% after two, three, four and more than four prior
attachment of the placenta to the uterine wall, collectively
cesarean sections, respectively (Silver et al. 2006).
termed placenta accreta (Sofiah and Fung 2009). This
Once placenta accreta occurs, it may threaten the life of
invasion occurs when the decidua is invaded by the cho-
the mother and fetus. Massive hemorrhage at the time
rionic villi or when the placenta abnormally implants in
of attempted placenta removal is the immediate clinical
the myometrium and serosa (Teo et al. 2009). Based on
consequence of placenta accreta, and it is the most
the degree of penetration of the chorionic villi, placental
common indication for emergent intrapartum or post-
invasion is graded into placenta accreta, increta and per-
partum hysterectomy (Zelop et al. 1993). The reported
creta. In this article, all of these varieties are referred to as
maternal mortality risk of placenta accreta may reach
placenta accreta.
7% (O’Brien et al. 1996). Given the dangers associated
Since the early 1900s, the incidence of placenta
with the condition, accurate prenatal diagnosis of
accreta has increased 13-fold, or approximately 1 in
placental accreta is paramount.
588 women, largely because of the rising rate of cesarean
Ultrasound (US) imaging and magnetic resonance
delivery. Cesarean delivery increased dramatically from
imaging (MRI) have been widely used as diagnostic tools
5.8% in 1970 to 32.9% in 2009 in the United States
in placenta accreta. The diagnostic criteria derived from
(Balayla and Bondarenko 2013; Blanchette 2011;
US that suggest placenta accreta, increta and percreta
Solheim et al. 2011; Wortman and Alexander 2013).
include one or more of the following: (i) loss of the
normal hypoechoic retroplacental myometrial zone; (ii)
thinning or disruption of the hyperechoic uterine
Address correspondence to: Limei Xie, Department of Ultra- serosa-bladder interface; (iii) presence of focal exophytic
sound, Shengjing Hospital of China Medical University, 36 Sanhao
Street, Heping District, Shenyang, Liaoning, 110004, China. E-mail: masses; (iv) myometrium thickness ,1 mm; (v) placental
xielm72@yahoo.cn lacunae with high-velocity turbulent venous-type flow;

1
2 Ultrasound in Medicine and Biology Volume -, Number -, 2013

and (vi) increased vascularity proximal to the bladder (c) case reports or case series; (d) insufficient data to re-
wall on color Doppler (Chou et al. 2000; Finberg and assess sensitivity and specificity from an individual
Williams 1992; Thia et al. 2007). In contrast, the study; and (f) duplicate data.
diagnostic criteria extracted with MRI include (i) Studies using US with or without Doppler imaging
abnormal uterine bulging; (ii) heterogeneous signal of were included; similarly, studies using MRI with or
the placenta on T2-weighted (T2 W) images; (iii) dark in- without gadolinium contrast were included. All retrieved
traplacental bands on T2 W images; (iv) focal interrup- articles were reviewed by two observers who applied the
tions in the myometrial wall; (v) tenting of the bladder; inclusion and exclusion criteria described above.
and (vi) direct visualization of the invasion of pelvic Disagreements were resolved by consensus.
structures by placental tissue (Baughman et al. 2008;
Lax et al. 2007). Data extraction
The reported diagnostic accuracy of US and MRI Data were extracted independently from all studies
varies widely for placenta accreta. Meta-analysis is that fit the inclusion criteria by the same observer of study
a statistical method that allows the results of individual selection. When observer disagreements occurred, a third
studies to be evaluated systematically (Irwig et al. reader reviewed the article, and the disagreement was
1994). Therefore, the purpose of this article was to resolved by discussion. For each study included, certain
summarize the available publications and to compare data were extracted: first author, year of publication,
the diagnostic value of US and MRI in detection of study design (prospective or retrospective), patient char-
placenta accreta. acteristics (average gestational age), technical aspects
(e.g., probe type and probe frequency used in the US
METHODS studies, magnetic field strength and contrast agent used
in the MRI studies), image interpretation (blinded or
Search strategy not). For each study, the numbers of TPs, FPs, FNs and
A computerized literature search (Deville et al. TNs for US and MRI were recorded.
2000) of PubMed, EMBASE and the Cochrane Central
Register of Controlled Trials Database was conducted Quality assessment
to identify relevant published articles on the diagnostic The methodological quality of the articles was as-
accuracy of US or MRI in detection placenta accreta. sessed using the updated quality assessment tool
We used a combination of the following terms: (i) QUADAS-2 (Quality Assessment of Diagnostic Accu-
‘‘US’’ OR ‘‘ultrasound’’ OR ‘‘MRI’’ OR ‘‘magnetic reso- racy Studies) guidelines (Whiting et al. 2011) to evaluate
nance imaging’’; (ii) ‘‘placenta accreta’’ OR ‘‘placenta in- the risk of bias and applicability. Each item was rated as
creta’’ OR ‘‘placenta percreta’’; and (iii) ‘‘sensitivity’’ OR ‘‘low,’’ ‘‘high,’’ or ‘‘unclear.’’ The ‘‘unclear’’ category was
’’specificity’’ OR ‘‘accuracy’’ OR ‘‘diagnosis’’ OR used only when insufficient data were reported. In the
‘‘detection.’’ No date limits were specified, and the search publication that included two index tests (US and MRI),
was current as of March 20, 2013. To expand our search, it was necessary to assess each index test in QUADAS
the reference lists from all retrieved articles were DOMAIN 2 (index test). Certain items were omitted
screened to identify additional studies. because they were not relevant to this topic.

Study selection Meta-analysis


Only the studies that satisfied all of the following A random effect model was used for primary statis-
criteria were included: (i) use of US or MRI in patients tical pooling of the data to obtain a summary estimate of
with a history of previous cesarean section or a diagnosis sensitivity and specificity with 95% confidence intervals
of placenta previa; (ii) sample size of at least eight (CIs) for US and MRI. The summary receiver operating
patients; (iii) English publications that could assess the characteristic (SROC) curve, the area under the curve
number of true positives (TPs), false positives (FPs), false (AUC) and the Q* index (the points on the SROC curve
negatives (FNs) and true negatives (TN), either directly or where sensitivity and specificity are equal) were also
indirectly; (iv) confirmation of the diagnosis with the gold calculated. Each study included provides an estimate of
standard of histopathologic analysis and/or intra- true-positive rates (TPRs) and false-positive rates
operative finding; and (v) in cases in which data were pre- (FPRs) in the meta-analysis, and a graph is made from
sented more than once, the article with the most details or the TPRs and FPRs. The SROC curve can be created
the most recent publication date. using a regression model (Moses et al. 1993). Z-Value
The exclusion criteria were: (a) articles not within tests were performed to determine whether the sensitivity,
the field of interest of this review; (b) review articles, specificity and AUC for US were significantly different
editorials, letters, comments or conference proceedings; from those for MRI (p , 0.05 was considered statistically
US vs. MRI in diagnosis of placenta accreta d X. MENG et al. 3

Table 1. TP, FP, FN, TN and other features of ultrasound (13 studies)
Average gestational Number Probe Probe Color andpower Image
Study age (wk) of patients TP FP FN TN type frequency (MHz) Doppler imaging interpretation

Finberg and Williams (1992)* — 4 14 4 1 15 TA/TV — Not used Blind


Lerner et al. (1995)y 34.2 (30–37) 21 5 1 0 15 TV 5.0–6.5 Used Blind
Levine et al. (1997)y 31.2 (26–37) 19 6 1 1 11 TA/TV 3.5–7.0 Used Blind
Chou et al. (2000)y 30.5 (16–36) 80 14 2 3 61 TA 3.5 Used Blind
Lam et al. (2002)y — 13 4 0 8 1 TA 5.0–7.0 Not used Blind
Warshak et al. (2006)y 25 (11–37) 453 30 16 9 398 TA/TV 3.5–5.0 Used Blind
Japaraj et al. (2007)y Third trimester 21 7 0 0 14 TA/TV 3.5–5.0 Used Blind
Dwyer et al. (2008)y — 32 14 5 1 12 TA 4.0–6.0 Used Blind
Masselli et al. (2008)y 30 (22–37) 50 11 0 1 38 TA — Used Blind
Lim et al. (2011)y Second trimester 13 6 2 3 2 TA 4.0–6.0 Used Not blind
Esakoff et al. (2011)y Third trimester 108 17 8 2 81 TA 4.0–6.0 Used Blind
Elhawary et al. (2013)z 29.3 (26–32) 39 8 3 2 26 TA 3.5–7.5 Used Blind
Chalubinski et al. (2013)y — 232 32 8 3 189 TA/TV 3.75–7.5 Used Blind

TP 5 true positive; FP 5 false positive; FN 5 false negative; TN 5 true negative; TA 5 transabdominal probe; TV 5 transvaginal probe.
* Prospective study design.
y
Retrospective study design.
z
Unknown study design.

significant). All statistics (sensitivity, specificity, diag- the field of interest of this review (n 5 338); (ii) articles
nostic odds ratio [DOR], SROC, AUC and Q*) refer to were published as reviews, letters, case reports or case
the diagnostic value of each index test. series (n 5 19); (iii) the data from the articles could not
Heterogeneity was assessed by calculating the I2 be used to construct or calculate TPRs, FPRs, FNRs or
statistic, which is a quantitative measure of the amount TNRs (n 5 13); (d) publications were not written in
of heterogeneity with an upper limit of 100%. I2 values English (n 5 3); and (e) the articles were published
of 25%, 50% and 75% were considered indicative of more than once (n 5 3). A total of 13 studies
low, moderate and high heterogeneity, respectively (Chalubinski et al. 2013; Chou et al. 2000; Dwyer et al.
(Higgins et al. 2003). When I2 exceeded 50%, a random 2008; Elhawary et al. 2013; Esakoff et al. 2011;
effect model was used in the meta-analysis. In all other Finberg and Williams 1992; Japaraj et al. 2007; Lam
cases, a fixed effect model was used. et al. 2002; Lerner et al. 1995; Levine et al. 1997; Lim
Statistical analyses were performed using Meta- et al. 2011; Masselli et al. 2008; Warshak et al. 2006)
Disc Statistical Software Version 1.4 (Unit of Clinical met all inclusion criteria and were selected for data
Biostatistics, Ram on y Cajal Hospital, Madrid, Spain) extraction and meta-analysis.
(Zamora et al. 2006).
Details on examination
The TP, FP, FN and TN results and other details
RESULTS
related to the 13 studies are summarized in Tables 1
Literature search and 2. Eleven of the 13 studies were retrospective, one
A comprehensive literature search revealed 389 study was prospective and the one was not defined. Gesta-
primary studies. After review of the titles, abstracts and tional ages of the patients included in the studies ranged
full texts, 376 articles were excluded. The reasons for from 11 to 37 wk. The diagnostic accuracy of US was
exclusion were as follows: (i) the articles were not in assessed in 13 papers, whereas six papers assessed the

Table 2. TP, FP, FN, TN and other features of magnetic resonance imaging (6 studies)
Average gestational Number Gadolinium Field Image
Study age (wk) of patients TP FP FN TN contrast material strength (T) interpretation

Lam et al. (2002)* — 9 3 1 5 0 Used 1.5 Blind


Warshak et al. (2006)* 28 (18–37) 40 23 0 3 14 Used 1.5 Blind
Dwyer et al. (2008)* — 32 12 6 3 11 Not used 1.5 Blind
Masselli et al. (2008)* 30 (22–37) 50 12 0 0 38 — 1.5 Blind
Lim et al. (2011)* Second trimester 13 7 1 2 3 Not used 1.5 Not blind
Elhawary et al. (2013)y 29.3 (26–32) 39 8 4 1 26 Not used 1.5 Blind

TP 5 true-positive; FP 5 false-positive; FN 5 false-negative; TN 5 true-negative.


* Retrospective study design.
y
Unknown study design.
4 Ultrasound in Medicine and Biology Volume -, Number -, 2013

Table 3. QUADAS-2 results for included studies performed with ultrasound (US) or magnetic resonance imaging (MRI)
Risk of bias Applicability concerns

Patient Reference Flow and Patient Reference


Study Modality selection Index test standard timing selection Index test standard

Finberg and Williams US [ [[ [ [[ [ [[ [


(1992)
Lerner et al. (1995) US [ [ [ [[ [[ [ [[
Levine et al. (1997) US [ [ [ [[ [ [[ [
Chou et al. (2000) US [ [ [ ? [ [ [
Lam et al. (2002) US [ [ [ [ [ [ [
Warshak et al. (2006) US [ [ [ [[ [ [[ [
Japaraj et al. (2007) US [ [ [[ [[ [ [[ [
Dwyer et al. (2008) US [ [ [ [[ [ [ [[
Masselli et al. (2008) US [ [ [ [[ [ [ [
Lim et al. (2011) US [ [ [ [ [ [ [
Esakoff et al. (2011) US [ [ [ ? [ [ [
Elhawary et al. (2013) US [ [ [ ? [ [[ [
Chalubinski et al. (2013) US [ [ [ [[ [ [[ [
Lam et al. (2002) MRI [[ [ [ [ [[ [[ [
Warshak et al. (2006) MRI [[ [ [ [[ [[ [[ [
Dwyer et al. (2008) MRI [ [[ [ [[ [ [ [[
Masselli et al. (2008) MRI [ [ [ [[ [ [ [
Lim et al. (2011) MRI [ [ [ [ [ [ [
Elhawary et al. (2013) MRI [ [ [ ? [ [ [

[ 5 Low risk; [[ 5 high risk; ? 5 unclear risk.

accuracy of MRI. In the six trials comparing US with combined the methods. Color Doppler imaging and
MRI, the relative accuracies of US and MRI were directly power Doppler imaging were used in 11 studies. The
compared within the same group of patients in four transducer frequency in US varied from 3.5 to
studies (Dwyer et al. 2008; Elhawary et al. 2013; Lim 7.5 MHz. In the MRI studies, the six papers included
et al. 2011; Masselli et al. 2008). In two studies, 183 patients who were available for the analysis.
patients underwent MRI evaluation because of Gadolinium contrast materials were used in two studies
suspicious findings on US or because US provided (Lam et al. 2002; Warshak et al. 2006).
inconclusive evidence of placenta accreta (Lam et al.
2002; Warshak et al. 2006). In the US studies, the 13 Quality assessment
papers included 1115 patients who were available for A quality assessment of the included studies based
the analysis. Several studies used transabdominal or on the updated QUADAS-2 is outlined in Table 3. Over-
transvaginal probes alone, whereas other studies all, the quality of the studies was satisfactory.

Fig. 1. Sensitivity of diagnosis of placenta accreta with ultrasound. CI 5 confidence interval.


US vs. MRI in diagnosis of placenta accreta d X. MENG et al. 5

Fig. 2. Specificity of diagnosis of placenta accreta with ultrasound. CI 5 confidence interval.

Meta-analysis DISCUSSION
The pooled sensitivity, pooled specificity and DOR
Ultrasound is the most commonly used imaging
of the two diagnostic methods obtained on the basis of
modality for the diagnosis of placental accreta because
a random effect model, are illustrated in Figures 1–4.
it is an inexpensive, non-invasive and time-saving
The pooled sensitivities of US and MRI were 0.83 and
method. Color Doppler and power Doppler, as well as
0.82, respectively, and there was no statistically
the use of a transvaginal transducer, appeared to improve
significant difference in sensitivity between US and
the performance of conventional ultrasound in the assess-
MRI (p . 0.05). The pooled specificities were 0.95 and
ment of placenta accreta. Color and power Doppler high-
0.88 for US and MRI, respectively; there were no
lighted areas of increased vascularity caused by dilated
statistically significant differences in specificity
blood vessels crossing the placenta and uterine wall
between US and MRI (p . 0.05). The DORs of US and
(Chou et al. 2002), which further validated the conven-
MRI were 63.41 and 22.95, respectively.
tional gray-scale sonographic features. A transvaginal
To compare US and MR, we used SROC analysis
transducer can improve the near-field resolution of the
(Figs. 5, 6). The AUCs for US and MRI were 0.9485
interface between the placenta and the lower uterine
and 0.8963, respectively, and the Q* indices were
segment, especially in cases of placenta previa or poste-
0.8884 and 0.8273, respectively. Whether the AUC of
rior placenta (Lerner et al. 1995). Higher-frequency
SROC curves statistically differed between the two diag-
probes have been reported to improve spatial resolution
nostic tests can be determined by Z-value statistics anal-
for superficial structures, thereby affecting the accuracy
ysis (Hanley and McNeil 1982). The Z-value for US and
of US (Benacerraf et al. 2000). Given that it is more
MRI was 0.8193, and the corresponding p-value was
accessible to patients and physicians, US will continue
0.4126.
to be the mainstay for prenatal diagnosis of placenta

Fig. 3. Sensitivity of diagnosis of placenta accreta with magnetic resonance imaging. CI 5 confidence interval.
6 Ultrasound in Medicine and Biology Volume -, Number -, 2013

Fig. 4. Specificity of diagnosis of placenta accreta with magnetic resonance imaging. CI 5 confidence interval.

accreta (Teo et al. 2009). However, US may be unreliable All but one of the studies found that US and MRI are
when imaging a posterior placenta; in such a case, MRI effective tools in the diagnosis of placenta accreta. Lam
can achieve superior diagnostic accuracy (Bakri et al. et al. (2002) reported the sensitivity of US and MRI as
1993; Thorp et al. 1992). 33% and 38%, respectively. However, the findings of an
More recently, MRI with and without gadolinium individual study have limited generalizability because
has been explored as an adjuvant modality for further of the relatively small number of patients. To derive
improving prenatal diagnosis of placenta accreta. It is more rigorous estimates of the diagnostic performance
believed that the gadolinium delineates the outer of US and MRI, we pooled published studies.
placental surface proximal to the myometrium more To the best of our knowledge, this systematic review
clearly; as a consequence, the confusion between hetero- with meta-analysis is the first attempt to compare the
geneous signals originating in the placenta from those diagnostic value of US and MRI in the detection of
caused by maternal blood vessels is eliminated, thereby placenta accreta. Considering the fact that diagnostic
enhancing the specificity of MRI. However, the use of ga- performance is determined by sensitivity as well as spec-
dolinium in pregnancy is controversial given the potential ificity, a meta-analysis that considers the two factors is
for negative effects (Dwyer et al. 2008; Warshak et al. necessary. The relationship between sensitivity and spec-
2006). ificity is non-linear, and SROC analysis is thus helpful in
transforming the information linearly to compare the
diagnostic methods subsequently. Analysis of the SROC
curves revealed that the AUC of US was 0.9485 with
a Q* index of 0.8884, whereas the AUC of MRI was
0.8963 with a Q* index of 0.8273. The above results indi-
cate that both US and MRI have a high degree of sensi-
tivity and specificity in diagnosing placenta accreta.
Significant difference analysis of the two diagnostic
methods was performed using the Z-value test from the
AUCs of the SROC curves. In this study, the Z-value
was 0.8193 with a corresponding p-value of 0.4126, indi-
cating the absence of a significant difference in diagnostic
value between US and MRI.
Massive hemorrhage and associated morbidities,
including cystotomy, ureteral injury, pulmonary embolus,
admission to the intensive care unit and re-operation, are
common with placenta accreta. When placenta accreta is
suspected on US or MRI, the attending obstetricians
should prepare and counsel the patients and assemble
a multidisciplinary team (including obstetricians, anes-
Fig. 5. Summary receiver operating characteristic (SROC) thetists, interventional radiologists, urologists, visceral
curve for ultrasound. The size of the circle is proportional to
the weight of the individual study. AUC 5 0.9485; surgeons and neonatologists) to handle a potentially
SE(AUC) 5 0.0148; Q* 5 0.8884; SE(Q*) 5 0.0198. life-threatening situation in the operation room (Japaraj
AUC 5 area under the curve; SE 5 standard error. et al. 2007). It is reported that approximately 90% of
US vs. MRI in diagnosis of placenta accreta d X. MENG et al. 7

was not used), type and frequency of probe, contrast


agent and experience of the physician may bring potential
bias. However, these biases were unavoidable because of
the retrospective nature of this study.

CONCLUSIONS
There is no significant difference in diagnostic value
between US and MRI in placenta accreta. Both US and
MRI are highly specific and sensitive in diagnosing or
excluding the presence of placenta accreta, and US
should be the first choice for patients with limited time
and financial support.

Acknowledgments—This study was supported by a grant from the Scien-


tific Research Programs of Higher Education Institutions of Liaoning
Education Department, China (No. 2012225019).

Fig. 6. Summary receiver operating characteristic (SROC) REFERENCES


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