UROGENITAL

Suspected invasive placenta: evaluation with magneticresonance imaging

Laurence Bour & Vinciane Placé & Sandra Bendavid & Yann Fargeaudou &

Jean-Jacques Portal & Aude Ricbourg & Delphine Sebbag & Anthony Dohan &

Eric Vicaut & Philippe Soyer

Received: 26 February 2014 /Revised: 20 May 2014 /Accepted: 16 July 2014 /Published online: 29 July 2014# European Society of Radiology 2014

AbstractPurpose To determine the utility of magnetic resonance im-aging (MRI) in diagnosing invasive placenta (IP).Materials and methods MRI findings in 32 women withsuspected IP were evaluated independently by four readers.Interobserver agreement was calculated with kappa (κ) statis-tics. Associations between MRI findings and IP were assessedby univariate andmultivariate analyses. Sensitivity, specificityand accuracy of MRI for the diagnosis of IP were estimated.Results Sixteen women (16/32; 50 %) had confirmed IP.Interobserver correlation for the diagnosis of IP was fair (κ=0.40). Univariate analysis revealed that thinning or focal de-fect of the uteroplacental interface (P<0.0001) was the mostdiscriminating MRI variable in the differentiation betweennormal and IP. Overall sensitivity and specificity of MRI forthe diagnosis of IP were 84 % [95 % CI: 75–94 %] and 80 %

[95 % CI: 66–93 %], respectively. Thinning or focal defect ofthe uteroplacental interface was the most accurate finding(88 %) in the diagnosis of IP. Multivariate analysis revealedthat thinning or focal defect of the uteroplacental interface wasthe single independent predictor of IP (P=0.0006; OR=64.99).Conclusion MR imaging has 84 % sensitivity [95 % CI:75–94 %] and 80 % specificity [95 % CI: 66–93 %] forthe diagnosis of IP. Thinning or focal defect of theuteroplacental interface is the most discriminating inde-pendent MR variable in differentiating between normalplacenta and IP.Key points•MR imaging has acceptable degrees of accuracy to diagnoseinvasive placenta.

• Focal uteroplacental interface defect is the best finding todiagnose invasive placenta.

Electronic supplementary material The online version of this article(doi:10.1007/s00330-014-3354-z) contains supplementary material,which is available to authorized users.

L. Bour :V. Placé : S. Bendavid :Y. Fargeaudou :D. Sebbag :A. Dohan : P. SoyerDepartment of Abdominal and Interventional Imaging, HôpitalLariboisière-AP-HP, 2 rue Ambroise Paré, 75475 Paris cedex 10,France

L. Boure-mail: jlaurence.bour@gmail.com

V. Placée-mail: vinciane.place@lrb.aphp.fr

S. Bendavide-mail: sandra.bendavid@lrb.aphp.fr

Y. Fargeaudoue-mail: yann.fargeaudou@hotmail.fr

D. Sebbage-mail: delphinesebbag@gmail.com

A. Dohane-mail: anthony.dohan@lrb.aphp.fr

J.<J. Portal : E. VicautDepartment of Biostatistics and Clinical Research, HôpitalLariboisière-AP-HP, 2 rue Ambroise Paré, 75475 Paris cedex 10,France

J.<J. Portale-mail: jean-jacques.portal@lrb.aphp.fr

E. Vicaute-mail: eric.vicaut@lrb.aphp.fr

A. RicbourgDepartment of Obstetrics and Gynecology, HôpitalLariboisière-AP-HP, 2 rue Ambroise Paré, 75475 Paris cedex 10,Francee-mail: aude.ricbourg@lrb.aphp.fr

D. Sebbag :A. Dohan : E. Vicaut : P. Soyer (*)Diderot-Paris 7 University-Sorbonne Paris-Cité, 10 Avenue deVerdun, 75010 Paris, Francee-mail: philippe.soyer@lrb.aphp.fr

Eur Radiol (2014) 24:3150–3160DOI 10.1007/s00330-014-3354-z

• Focal uteroplacental interface defect is the single indepen-dent predictor of invasive placenta.

Keywords Abnormal placentation . Placenta accreta .

Placenta increta . Placenta percreta .Magnetic resonanceimaging

Introduction

Invasive placenta is a serious condition that is defined bymyometrial involvement by the fetal trophoblast and mayinvolve up to 1/500 pregnancies [1, 2]. It is due to a defectof the decidua and includes three types of abnormalities,depending on the degree of placental invasion through themyometrium. Placenta accreta is the least invasive presenta-tion that corresponds to an abnormal placental attachment tothe myometrium. Placenta increta partially invades themyometrium whereas placenta percreta corresponds to a fullpenetration of the trophoblast through the myometrium thatreaches the serosal surface and ultimately may involve adja-cent pelvic organs [3].

Placenta previa (i.e. a placenta abnormally located inthe lower uterine segment thus covering partially or total-ly the internal cervical os), prior caesarean section (C-section) and an advanced maternal age are three well-recognized major risk factors that are associated withinvasive placenta [4–6]. The spontaneous risk of invasiveplacenta is 0.4 ‰ in the general population. However, itrises up to 5 % in case of placenta previa, up to 24 % ifthere are both placenta previa and prior history of C-section and more than 67 % when placenta previa isassociated with more than four prior C-sections [7].

In general, the diagnosis of invasive placenta is madeclinically and using ultrasound before delivery. However, insome cases, the diagnosis of invasive placenta is made duringdelivery [8]. Detection before delivery is of major importanceto best plan the delivery mode because of an increased risk ofpostpartum haemorrhage in women with this condition [9,10]. Although encouraging results were found by severalgroups, the capabilities of magnetic resonance (MR) imagingfor the diagnosis of invasive placenta are not fully and clearlyestablished [11–21]. In addition, several MR imaging findingshave been found to be suggestive of the diagnosis of invasiveplacenta but no studies have attempted to determine the diag-nostic capabilities of independent MR criteria as well as thevariability in perception for the presence of invasive placentaamong different and independent readers.

Accordingly, the goal of this study was to determinethe utility of MR imaging in the diagnosis of invasiveplacenta.

Materials and methods

Patients

From August 2006 through February 2012, the database ofour institution was retrospectively queried to identify all wom-en with suspected invasive placenta on the basis of clinicaland ultrasound findings. This study was approved by ourinstitutional review board and informed consent was obtainedfrom all women. After this initial search, the electronic archiv-ing system of our institution was used to retrieve the subgroupof women who had MR imaging of the pelvis before delivery.The full medical records of this subgroup of women (includ-ing clinical, biological, surgical and imaging files, as well asdischarge summaries) were reviewed by the study coordinatorusing a standardized data collection form that included quan-titative (age at the time of MR imaging, parity, gravidity) andqualitative variables (prior history of C-section, mode of de-livery, placental status). Sixty consecutive women were ini-tially found; of these, 28 women were excluded because noMR imaging was performed or because they were referredfrom other institutions and MR imaging examination was notavailable for review.

The study population included 32 women (mean age,33.8 years±5.3 (standard deviation) [SD]; median, 34 years;first quartile [Q1], 31 years; third quartile [Q3], 38 yearsrange, 21–42 years).

MR imaging

All MR examinations were performed using a 1.5-T clinicalMR unit (Magnetom Avanto, Siemens Healthcare, Erlangen,Germany) with 21 receiver channels, using two anterior torsophased-array coils with six channels and three posterior spineclusters with three channels each, with the patient in a supineposition. The gradient strength of the magnet was 45 mT/mwith a slew rate of 200 mT/m/ms. All patients had T2-weighted (HASTE), steady state two-dimensional(TrueFISP) and fat-suppressed T1-weighted three-dimensional gradient echo (3D VIBE) sequence without in-travenous administration of gadolinium chelate. MR imagingparameters are listed in Table 1.

T2-weighted MR images (HASTE) were obtained with asingle shot fast spin echo sequence in the three planes of theuterus using parallel imaging (GRAPPA; acceleration factor,2). Fat suppression was obtained with a frequency-selectivefat saturation to reduce chemical shift artefacts. TrueFISP MRimaging was obtained in the sagittal plane using parallelimaging (GRAPPA; acceleration factor, 3). Fat-suppressed3D VIBE imaging was performed in the sagittal plane. Themean total imaging time was approximately 3 min and themean total examination time was approximately 15 min. In nocases was the fetus examined with separate sequences.

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Image analysis

MR images were analysed independently by four radiologistsblinded to all clinical information. Of them, three were staffradiologists with a special expertise in pelvicMR imaging andone was a junior radiologist. The four radiologists were un-aware of patients history, results of clinical and ultrasoundexaminations and final diagnosis.

MR imaging examinations were interpreted on a PACSviewing station (Directview, 13.1 sp1 version, Kodak-Carestream Health, Inc, Rochester, NY, USA).

Eleven MR imaging findings were evaluated by using astandardized data collection form. These findings includedpresence of placenta previa, visibility of prior uterotomy scar,thinning or focal defect of the uteroplacental interface [21],disruption of the inner layer of the uteroplacental interface onHASTE MR images [18], loss of the normal uterine pearshape, presence of intraplacental thick dark bands onHASTE images [17], normal bladder serosa on HASTE im-ages, vesical tenting, presence of increased intraplacental vas-cularity [17], presence of a placental infarction on 3D VIBEimages, and marked placental heterogeneity on HASTE MRimages [17]. A complete description of MR imaging findingsis given in the Electronic Supplementary Material.

At the end of the data collection, each observer was askedto give a final diagnosis for each patient. First, they had todecide whether or not the patient had an invasive placenta.Second, in case of invasive placenta, they had to decidewhether or not the patient had placenta percreta. For the

purpose of clarity and clinical relevance, placenta accretaand placenta increta were considered together and referred toas placenta accreta.

Standard of reference

The reference standard for determining the actual status ofthe placenta was established by the study coordinator. Thereference standard consisted of intraoperative findings inall women and the results of histopathological examina-tions of the removed uterus for the subset of women whohad hysterectomy. The final diagnosis regarding the statusof the placenta was based on well-established criteria [22,23]. Briefly, they included impossible total manual re-moval of the placenta because of the absence of cleavageplane between the placenta and the uterus; massive bleed-ing from the implantation site after difficult manual de-livery or histological confirmation of abnormal placenta-tion on hysterectomy specimens or on a fragment ofplacenta when placenta accreta was confirmed duringdelivery. Furthermore, a definite diagnosis of placentapercreta was confirmed during surgery when completeinvasion of the myometrium and uterine serosa wasobserved.

Statistical analysis

For the purpose of clarity, placenta accreta and placentaincreta were evaluated together for data analyses in the samegroup named “placenta accreta”. Women without invasiveplacenta as confirmed using the standard of reference werereferred to as the “normal placenta group” and women withinvasive placenta (placenta accreta, increta or percreta) werereferred to as the “abnormal placenta group”.

One medical statistician (with 27 years of experience inmedical statistics) performed all statistical analyses.Calculations were performed with SAS 9.2 software (SASInstitute, Cary, NC). Descriptive statistics were calculatedfor all of the categorical variables evaluated by MR imaging.Descriptive statistics included frequencies and proportions.Interobserver agreement regarding categorical data wasassessed using the Fleiss kappa (κ) statistics for multipleobservers. The Magree macro (SAS Institute) was used tocalculate κ values estimated frommultiple observers. κ valueswere further classified according to Landis and Koch [24].

To identify the MR imaging variables associated with adiagnosis of normal placenta and those associated withinvasive placenta, we compared the MR imaging findingsin the women who had normal placenta with those in thewomen who had invasive placenta (i.e. women with pla-centa accreta, increta or percreta). Similarly, to identifythe MR imaging variables associated with a diagnosis ofplacenta accreta and those associated with a diagnosis of

Table 1 Imaging parameters for MR imaging

Parameters Sequence

Sequence name HASTE TrueFISP 3D VIBE

TR (ms) 1,000 6.6 6.1

TE (ms) 81 3.3 2.75

Flip angle (°) 150 60 15

Number of signal averages 1 2 1

Reconstruction matrix size 340×448 336×448 174×192

Section thickness (mm) 4–8 5–6 1.8

Intersection gap (mm) 1.2 1.8 0.36

Voxel size (mm3) 1.9×1.4×6 1.1×0.9×6 1.5×1.5×1.8

Field of view (mm) 360 400 280

Echo train length 195 NA NA

Echo spacing (ms) 5.12–5.76 NA NA

Receiver bandwidth (Hz/pixel) 385–391 531–587 280

Number of sections acquired 20–30 16–24 80

Acquisition time (s) 20–30 38–53 24

NA not applicable, HASTE half-Fourier acquisition single-shot turbospin-echo, TrueFISP true fast imaging with steady-state free-precession(obtained with fat suppression), 3D VIBE three-dimensional volumeinterpolated breath-hold imaging (obtained with fat suppression)

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placenta percreta, we compared the findings in womenwho had placenta percreta with those in the women whohad placenta accreta. These comparisons were made usingthe results reported by the best of the four observers (i.e.the reviewer who achieved the greatest number of correctdiagnoses as defined by the standard of reference).Categorical variables were compared by using the chi-squared or Fisher’s exact test when any expected propor-tion of variables was less than 5. Statistically significantbinary variables found by univariate analysis (P<0.05)were then evaluated by a stepwise logistic regression test.A strict 5 % level of significance was selected because ofthe limited size of the patient population and the relativelyhigh number of variables. For the same reason, interactionterms were not considered in the logistic regression mod-el. The relationships between each MR imaging variableand the status of the placenta were tested by stepwisemultivariate logistic regression analysis. Odds ratios andcorresponding 95 % confidence intervals (CIs) for pro-portions were calculated. All statistical tests were twotailed, and P<0.05 was considered to indicate statisticalsignificance.

The sensitivities, specificities, accuracies, and positive andnegative predictive values—with corresponding 95 % CIs—of all MR imaging criteria for the diagnosis of abnormalplacenta, placenta accreta and placenta percreta were estimat-ed for each reviewer. Overall sensitivity and specificity werecalculated using the method developed byMcCarthy and Guo[25] that takes into account the fact that estimations made bythe four observers on the same patients were not independentfrom a statistical point of view. This calculation is based on theratio estimator of the variance of clustered binary data asproposed by Rao and Scott [26].

Results

Patients

The reference standard revealed that 16/32 (50 %) womenwith a mean age of 31.4 years±5 (SD) (median, 32.5 years;first quartile [Q1], 29.5 years; third quartile [Q3], 34.5 years;range, 21–38 years) had a normal placenta and 16/32 (50 %)women with a mean age of 36.1 years±4.5 (SD) (median,37.5 years; Q1, 33 years; Q3, 39.5 years; range, 25–42 years)had an invasive placenta. Obstetrical data of the patients arelisted in Table 2.

In the “abnormal placenta” group, all women (16/16;100 %) had a placenta previa and history of at least one priorC-section; of these, 10/16 (63 %) had a placenta percreta, 5/16(31 %) a placenta accreta and 1/16 (6 %) had a placentaincreta. Final diagnosis regarding the status of the placenta

was obtained intraoperatively during delivery in 12/16 (75 %)women and histopathologically after caesarean hysterectomyin 4/16 (25 %) women. Among the four women who hadhysterectomy, histopathological analyses revealed placentaaccreta in two women, placenta increta in one woman andplacenta percreta in one woman.

In the “normal placenta” group, 3/16 women (18.5 %) hadboth placenta previa and prior history of C-section (Fig. 1).Final diagnosis regarding the status of the placenta was ob-tained intraoperatively during delivery in 16/16 (100 %)women.

Interobserver agreement

Interobserver agreement was good for the diagnosis of pla-centa percreta (κ=0.61), moderate for the diagnosis of normalplacenta (κ=0.51) and poor for the diagnosis of placentaaccreta (κ=0.20).

Interobserver agreement was good for two of the 11 MRimaging variables (i.e. placenta previa, κ=0.78 and normalhypointense bladder serosa on T2-weighted MR images, κ=0.61). For the remaining nine variables, five had a moderateinterobserver agreement (i.e. presence of increasedintraplacental vascularity, κ=0.53; intraplacental thick darkbands, κ=0.49; thinning or focal defect of the uteroplacental

Table 2 Demographic and obstetrical data of two groups of patients withsuspected invasive placenta

Normalplacenta (n=16)

Invasiveplacenta (n=16)

Age (years)

Mean 31.4 36.1

SD 5 4.5

Median 32.5 37.5

Q1–Q3 29.5–34.5 33.0–39.5

Range 21–38 25–42

Parity

Mean 2.1 3.4

SD 1.5 2.7

Median 2.0 2.5

Q1–Q3 1.0–2.5 1.5–4.5

Range 1.0–5.0 1.0–10

Gravidity

Mean 2.8 4.25

SD 1.5 2.8

Median 3.0 3.0

Q1–Q3 1.5–4.0 2.0–6.0

Range 1–5 1–11

Prior C-section 10/16 (63 %) 16/16 (100 %)

SD standard deviation; Q1, Q3 first and third percentiles, respectively

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interface, κ=0.42). Detailed κ values for the MR imagingcriteria are given in Table 3.

Differentiation between normal and invasive placenta

Sensitivity, specificity and accuracy obtained by the fourindependent reviewers in the diagnosis of invasive placentawere 75–94%, 75–81 % and 78–88%, respectively (Table 4).The best results were obtained by reviewer 3 who was con-sidered as the best reviewer for further analysis. There were no

single cases of invasive placenta that were missed by the fourreviewers in the same woman. In 9/16 women (56 %), thediagnosis of invasive placenta was reached correctly by thefour reviewers. Overall sensitivity and specificity of MRimaging for the diagnosis of invasive placenta were 84 %[95 % CI 75–94 %] and 80 % [95 % CI 66–93 %],respectively.

The distribution of the various MR criteria among thedifferent groups of patients is given in Table 5. Among the11 MR imaging variables that were studied, the following fivewere significantly associated with the diagnosis of invasiveplacenta: thinning or focal defect of the uteroplacental inter-face, P<0.0001 (Fig. 2); disruption of the inner layer of theuteroplacental interface on HASTE images, P=0.0004(Fig. 3); loss of the normal uterine pear shape, P=0.0004;intraplacental thick dark bands on T2-weighted MR images,P=0.0023 (Fig. 4); and presence of placenta previa, P=0.0131 (Table 6).

The sensitivities and specificities of the 11 MR imagingvariables for the diagnosis of invasive placenta are shown inTable 7. Presence of a placenta previa, loss of the normaluterine pear shape, thinning or focal defect of theuteroplacental interface (Figs. 2 and 4) and disruption of theinternal layer of the uteroplacental interface were the mostsensitive criteria with 75 %, 75 %, 81 % and 81 % sensitivity,respectively, for the diagnosis of invasive placenta. Thinningor focal defect of the uteroplacental interface was the mostaccurate finding (88 %; 95%CI: 71–97%) in the diagnosis ofinvasive placenta.

Multivariate analysis with stepwise logistic regression re-vealed that thinning or focal defect of the uteroplacentalinterface was the single independent predictor of invasiveplacenta (P=0.0006).

Differentiation between placenta accreta and placenta percreta

Three MR imaging variables were more frequently observedin the patients with placenta percreta than in those with

Fig. 1 34-year-old woman with suspected invasive placenta who hadMR imaging of the pelvis at 39 weeks of pregnancy. T2-weightedHASTE MR image in the axial plane shows normal, homogeneoushyperintense placenta with uteroplacental interface made of three indi-vidual layers: an inner hypointense layer (black arrows), a mid hyperin-tense layer (white arrow) and an outer hypointense layer (arrowhead).Intraoperative findings confirmed normal placenta

Table 3 Interobserver agreement for 11 MR imaging variables in 32patients with suspected invasive placenta

MR imaging feature Kappavalue*

Placenta previa 0.78

Visibility of prior uterotomy scar 0.10

Thinning or focal defect of the UPI 0.42

Disruption of the inner layer of the UPI 0.31

Loss of the normal uterine pear shape 0.29

Intraplacental thick dark bands 0.49

Normal bladder serosa 0.61

Vesical tenting 0.27

Increased vascularity 0.53

Placental infarction 0.04

Marked placental heterogeneity 0.34

UPI uteroplacental interface

*0.00–0.20, poor agreement; 0.21–0.40, fair agreement; 0.41–0.60, mod-erate agreement; 0.61–0.80, good agreement; 0.81–0.99, excellent agree-ment; 1.00, perfect agreement

Table 4 Sensitivity, specificity and accuracy obtained by four inde-pendent readers in the diagnosis of invasive placenta

Sensitivity Specificity Accuracy

Reader 1 75 (12/16)[50–89]

81 (13/16)[57–93]

78 (25/32)[64–92]

Reader 2 88 (14/16)[64–96]

75 (12/16)[50–89]

81 (26/32)[68–95]

Reader 3 94 (15/16)[71–98]

81 (13/16)[57–93]

88 (28/32)[76–99]

Reader 4 81 (13/16)[57–93]

81 (13/16)[57–93]

81 (26/32)[68–95]

Data are percentages. Numbers in parentheses are proportions used tocalculate percentages. Numbers in brackets are 95 % CIs

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placenta accreta. They included increased placental vascular-ity (60 % vs. 0 %, P=0.026), intraplacental thick dark bands(80 % vs. 17 %, P=0.024) and marked placental heterogene-ity (80 % vs. 17 %, P=0.024). When considering the “abnor-mal placenta” group, the overall sensitivity and specificity ofMR imaging to differentiate between “placenta accreta” and“placenta percreta” were 46 % [95 % CI: 31–61 %] and 78 %[95 % CI: 62–92 %], respectively (Figs. 5 and 6).

Discussion

One important result of our study is that thinning or focaldefect of the uteroplacental interface was identified as thesingle, independent, discriminating MR variable in thedifferentiation between normal and invasive placenta. Inaddition, thinning or focal defect of the uteroplacentalinterface was the most accurate finding (88 %; 95 % CI:71–97 %) in the diagnosis of invasive placenta. Of inter-est, this MR criterion was not evaluated in the study byLax et al. [17]. These researchers considered that thisfeature is frequently observed, even in normal placenta,especially during the third trimester [17].

In our study, the overall sensitivity and specificity of MRimaging in the diagnosis of invasive placenta were consistentwith those already reported in the literature that ranged be-tween 38 % and 100 % for sensitivity [14, 27] and 65 % and100 % for specificity [14, 16]. By contrast, our results showedsome degree of discrepancies with prior studies with respect tointerobserver variability. In this regard, in the study by Laxet al., three MR imaging features, including uterine ab-normal bulging, intraplacental dark bands and placentalheterogeneity, were associated with invasive placenta witha κ value greater than 0.40, whereas in our study lower κvalues were found [17].

In our study, only two MR criteria showed both moderateinterobserver agreement and significant association with in-vasive placenta on univariate analysis. These two MR criteriawere intraplacental thick dark bands (κ=0.49, P=0.0023) andthinning or focal defect of the uteroplacental interface (κ=0.42, P<0.0001). The presence of a thinning or focal defect ofthe uteroplacental interface was found to be the single inde-pendent predictor of invasive placenta on stepwise multivar-iate logistic regression analysis.

We found that placental heterogeneity was not significantlyassociated with the diagnosis of invasive placenta. This is incontrast with the results of Lax et al. who reported that thisfinding was more frequently observed in case of invasiveplacenta [17]. It is currently admitted that normal placentashows some degree of physiological heterogeneity [28]. Inthis regard, Blaicher et al. described the spectrum of normalpresentation of the placenta [28]. They found placental

Table 5 Categorical MR criteriain three patient groups by the bestreader

Numbers in parentheses are per-centages. Data were extractedfrom results of reader 3 who wasthe best reader with the greatestnumber of correct diagnoses asdefined by the standard ofreference

UPI uteroplacental interface

Normalplacenta (n=16)

Placentaaccreta (n=6)

Placentapercreta (n=10)

All patients

(n=32)

Placenta previa 5 (31) 6 (100) 6 (60) 17 (53)

Visibility of prior uterotomy scar 1 (6) 0 (0) 0 (0) 1 (3)

Thinning or focal defect of UPI 1 (6) 4 (67) 9 (90) 14 (44)

Disruption of inner layer of UPI 3 (19) 4 (67) 9 (90) 16 (50)

Loss of normal uterine pear shape 2 (13) 4 (67) 8 (80) 14 (44)

Intraplacental thick dark bands 1 (6) 1 (17) 8 (80) 10 (31)

Normal bladder serosa 15 (94) 6 (100) 6 (60) 27 (84)

Vesical tenting 0 (0) 0 (0) 3 (30) 3 (9)

Increased placental vascularity 2 (13) 0 (0) 6 (60) 8 (25)

Placental infarction 0 (0) 0 (0) 1 (10) 1 (3)

Marked placental heterogeneity 5 (31) 1 (17) 8 (80) 14 (44)

Fig. 2 33-year-old woman with suspected invasive placenta who hadMR imaging of the pelvis at 42 weeks of pregnancy. T2-weightedHASTE MR image in the axial plane shows anterior and medial defectof the uteroplacental interface (arrows). Placenta accreta was confirmedintraoperatively

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heterogeneity in a number of cases with variations dependingon the gestational age [28]. We consider that the presence ofplacental heterogeneity is difficult to ascertain because thereare no studies to date that have clearly defined objective orquantitative criteria for placental heterogeneity. The diagnosisof placental heterogeneity is subjective and primarily dependson the presence or absence of abnormal dark bands on T2-weighted MR images [29].

On TrueFISP and HASTE MR images, the normaluteroplacental interface presents with three parallel layers: an

inner layer with low signal intensity, a middle layer withmoderate high signal intensity and an outer layer with lowsignal intensity, which is thought to correspond to the uterineserosa [18]. It has been demonstrated that focal non-visualization of the inner layer on TrueFISP and HASTEMR images is strongly associated with invasive placenta[18]. The inner layer represents both decidua and the innermyometrium [18]. In our study, this feature was statisticallyassociated with invasive placenta (P=0.0004) but with a fairinterobserver agreement (κ=0.31). This result could be ex-plained in part by observer experience, which may account forvariability in perception of this subtle MR imaging feature.

In our study, we evaluated several MR imaging criteria todetermine their association with the diagnosis of invasiveplacenta. We found that visibility of a prior uterotomy scar,placental infarction, increased intraplacental vascularity anddefect of the bladder serosa were not significantly associatedwith the diagnosis of invasive placenta.

Areas of placental infarctions are difficult to depict, espe-cially in the absence of T1-weighted MR images. Placentalinfarction contributes to placental heterogeneity but there is noclinical consequence if not depicted. Moreover, during thethird trimester, normal placenta may present with areas ofinfarction in about 25 % of the cases so that this MR findingcan be considered as part of the normal appearance [28]. Thisis further supported by the fact that areas of placental infarc-tions occupying less than 5 % of the placenta are frequentlyobserved on histopathological analysis of mature normal pla-centas [15]. This may explain why placental infarction is notassociated to a significant degree with the diagnosis of inva-sive placenta on MR imaging.

In our study, irregular and large vessels were observed in6/16women (38%)with invasive placenta and in 2/16women

Fig. 3 39-year-old woman with suspected invasive placenta who hadMR imaging of the pelvis at 37 weeks of pregnancy. a T2-weightedHASTE MR image in the coronal plane shows placenta previa withdisruption of low signal inner layer of uteroplacental interface (arrow).b T2-weighted HASTE MR image in the sagittal plane shows placenta

previa, abnormal uterine bulging (white arrow), uteroplacental inner layerdisruption (black arrowhead) and thick intraplacental dark bands (whitearrowheads). Placenta accreta was confirmed intraoperatively and afterhistopathological examination after total hysterectomy

Fig. 4 35-year-old woman with suspected invasive placenta who hadMR imaging of the pelvis at 34 weeks of pregnancy. T2-weightedHASTE MR image of the pelvis in the coronal plane shows placentaprevia, with internal heterogeneity, thick intraplacental dark band(arrowhead). There is a defect of the whole uteroplacental interface(white arrows) with placental protrusion. The uterovesical interface(black arrows) is normal. MR findings were consistent with placentaaccreta whereas intraoperative findings confirmed placenta percreta

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(13 %) with normal placenta. However the difference was notsignificant so that our results suggest that this finding may notbe helpful to discriminate between normal and invasive pla-centa. By contrast, in their study, Derman et al. reported that75 % of invasive placentas presented with disorganized andhypertrophied intraplacental blood vessels measuring morethan 6 mm [29]. These vessels presented with linear flowvoids on HASTE images and had an increased signal onTrueFISP images, indicating slow vascular flow. Because offibrin deposition, intraplacental thick dark bands werehypointense on HASTE images but with a non-modifiedsignal on TrueFISP images. This presentation on TrueFISPimages helped differentiate vessels from intraplacental darkbands. In the same study, irregular and large vessels wereobserved only in invasive placenta and this finding had a goodinterobserver agreement (κ=0.76) [29].

MR imaging is a useful tool before delivery to diagnoseinvasive placenta in order to plan the delivery and particularlyto anticipate severe postpartum haemorrhage [9]. MR imagingis performed during the third trimester of gestation and pref-erably before 30 weeks’ gestation [16]. Currently, three mainmanagement options are available for invasive placenta, in-cluding the “caesarean-hysterectomy”, the full conservative

management during which the invasive placenta is left-in-place inside the uterus with no attempt made to remove it afterdelivery [30, 31], and the extirpative approach with manualremoval of the placenta which is currently the least favouredoption [10, 30, 31]. Pelvic artery embolization is nowadays animportant complementary tool and can be associated withthese strategies, with encouraging results [9]. After conserva-tive treatment, MR imaging can be used during the post-partum period to assess placental resorption [10].

Ultrasound is generally used as the first-line examinationfor the detection of invasive placenta [32]. Ultrasound isusually performed during the third trimester of pregnancyand MR imaging is generally used to complement a doubtfulultrasound examination, and especially when there is a poste-rior placenta or in overweight women [15]. A recent meta-analysis found that ultrasound and MR imaging have equiva-lent overall sensitivities and specificities for the diagnosis ofinvasive placenta [33]. However, on a case-by-case analysis,researchers demonstrated that the two imaging tests may becomplementary in a substantial number of women, so thattheir association may heighten the level of confidence withwhich the diagnosis of invasive placenta can be ascertained orexcluded [15, 16]

Table 6 Association between independent MR imaging findings and placental status at χ2 and logistic regression analyses

Variable Normalplacenta (n=16)*

Invasiveplacenta (n=16)*

P value OR**

Placenta previa 5 (31) 12 (75) 0.0131 6.60(1.40–31.05)

Visibility of prior uterotomy scar 1 (6) 0 (0) >0.99† –

Thinning or focal defect of UPI 1 (6) 13 (81) <0.0001 64.99(6.00–703.47)

Disruption of inner layer of the UPI 3 (19) 13 (81) 0.0004 18.78(3.18–110.82)

Loss of normal uterine pear shape 2 (13) 12 (75) 0.0004 21.00(3.26–135.48)

Intraplacental thick dark bands 1 (6) 9 (56) 0.0023 19.29(2.03–183.41)

Normal bladder serosa 15 (94) 12 (75) 0.3326† 0.20(0.02–2.03)

Vesical tenting 0 (0) 3 (19) 0.2258† –

Increased placental vascularity 2 (13) 6 (38) 0.2200† 4.20(0.70–25.26)

Placental infarction 0 (0) 1 (6) >0.99† –

Marked placental heterogeneity 5 (31) 9 (56) 0.1540 2.83(0.67–12.02)

Invasive placenta indicates placenta accreta, increta or percreta

UPI indicates uteroplacental interface

*Data are numbers of patients. Numbers in parentheses are percentages

**Numbers in parentheses are 95 % CIs. Odds ratios (ORs) and corresponding 95 % CIs are not shown for some variables because the frequencies ofzero values in the corresponding cells led to unstable estimates of those variables or because variables were not entered into the logistic regressionanalysis

†Fisher exact test values. All other data in this column are standard χ2 values

Eur Radiol (2014) 24:3150–3160 3157

Our study has several limitations. One relates to its retro-spective nature. In this regard, there was a relatively highprevalence of placenta percreta among the “abnormal placen-ta” group, whereas placenta percreta usually represents lessthan 20 % of the cases of invasive placenta [1, 3–7]. Becauseplacenta percreta is more easily depicted on MR images, itcould affect the general conclusion of our study and mayresult in an overestimation of the actual capabilities of MRimaging in differentiating between normal and invasive pla-centa. Another limitation is that a new finding onMR imaging(i.e. placental protrusion into the internal os) was very recentlyreported as significantly associated with the diagnosis ofinvasive placenta [34] and this finding was not analysed inour evaluation. A third limitation is that MR imaging was notcompared to ultrasound.

In conclusion, MR imaging has 84 % sensitivity [95 % CI:75–94 %] and 80 % specificity [95 % CI: 66–93 %] for thediagnosis of invasive placenta, although it is associated with afair interobserver agreement. Placenta previa, thinning or focaldefect of the uteroplacental interface, disruption of the innerlow signal layer of the uteroplacental interface, intraplacentalthick dark bands and loss of the normal uterine pear shape areMR imaging features that are significantly associated with the

Table 7 Values for MRI variables in the diagnosis of invasive placenta

Variable TP* FP* FN* TN* Sensitivity† Specificity† PPV† NPV† Accuracy†

Placenta previa 12 5 4 11 75 (12/16)(54–96)

69 (11/16)(46–91)

71 (12/17)(49–92)

73 (11/15)(51–96)

72 (23/32)(56–87)

Visibility of prior uterotomy scar 0 1 16 15 0 (0/16)(0–21 )

94 (15/16)(71–98)

0 (0/1)(0–98 )

48 (15/31)(30–67)

47 (15/32)(29–65)

Thinning or focal defect of UPI 13 1 3 15 81 (13/16)(57–93)

94 (15/16)(71–98)

93 (13/14)(68–98)

83 (15/18)(60–94)

88 (28/32)(71–97)

Disruption of inner layer of UPI 13 3 3 13 81 (13/16)(57–93)

81 (13/16)(57–93)

81 (13/16)(57–93)

81 (13/16)(57–93)

81 (26/32)(64–93)

Loss of normal uterine pear shape 12 2 4 14 75 (12/16)(50–89)

88 (14/16)(64–96)

86 (12/14)(60–96)

78 (14/18)(54–91)

81 (26/32)(64–93)

Intraplacental thick dark bands 9 1 7 15 56 (9/16)(33–76)

94 (15/16)(71–98)

90 (9/10)(59–98)

68 (15/22)(47–83)

75 (24/32)(57–89)

Normal bladder serosa 4 1 12 15 25 (4/16)(10–49)

94 (15/16)(71–98)

80 (4/5)(37–96)

55 (15/27)(37–72)

59 (19/32)(41–76)

Vesical tenting 3 0 13 16 19 (3/16)(6–43)

100 (16/16)(79–100)

100 (3/3)(42–100)

55 (16/29)(37–71)

59 (19/32)(41–76)

Increased vascularity 6 2 10 14 38 (6/16)(18–61)

88 (14/16)(64–96)

75 (6/8)(40–92)

58 (14/24)(38–75)

63 (20/32)(44–79)

Placental infarction 1 0 15 16 6 (1/16)(1–28)

100 (16/16)(79–100)

100 (1/1)(20–100)

52 (16/31)(34–68)

53 (17/32)(35–71)

Marked placental heterogeneity 9 5 7 11 56 (9/16)(33–76)

69 (11/16)(44–85)

64 (9/14)(38–83)

61 (11/18)(38–79)

63 (20/32)(44–79)

UPI uteroplacental interface, PPV positive predictive value, NPV negative predictive value

*Data are numbers with true-positive (TP), false-positive (FP), false-negative (FN) and true-negative (TN) findings, out of a total of 32 patients withsuspected invasive placenta

†Data are percentages. Numbers in parentheses on the first line are the proportions used to calculate the percentages. Numbers in parentheses on thesecond line are 95 % CIs

Fig. 5 39-year-old woman with suspected invasive placenta who hadMR imaging of the pelvis at 36 weeks of pregnancy. T2-weightedHASTE MR image of the pelvis in the sagittal plane shows placentaprevia, abnormal anterior placental bulging with no visible uteroplacentalinterface (arrows) and placental protrusion through serosa (arrowhead).MR findings were consistent with placenta percreta. Intraoperative find-ings confirmed placenta percreta with bladder involvement

3158 Eur Radiol (2014) 24:3150–3160

diagnosis of invasive placenta. Of these, presence ofintraplacental thick dark bands and thinning or focal defectof the uteroplacental interface have a better interobserveragreement. Our results show that thinning or focal defect ofthe uteroplacental interface is the most discriminating inde-pendent MR variable in the differentiation between normaland invasive placenta.

Acknowledgements The scientific guarantor of this publication isPhilippe Soyer, MD, PhD. The authors of this manuscript declare norelationships with any companies whose products or services may berelated to the subject matter of the article. The authors state that this workhas not received any funding. One of the authors has significant statisticalexpertise. Institutional review board approval was obtained. Writteninformed consent was obtained from all patients in this study. No subjectsor cohorts have been previously reported. Methodology: retrospective,diagnostic study/observational, single centre study.

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Fig. 6 31-year-old woman with suspected invasive placenta who hadMR imaging of the pelvis at 37 weeks of pregnancy. T2-weightedHASTE MR image in the sagittal plane shows abnormal uterine bulging(arrowheads), large (>6 mm) and irregular vessels within an irregular andinterrupted uterovesical interface (white arrow), and thick intraplacentaldark bands (black arrow). MR findings were consistent with placentapercreta. Intraoperative findings confirmed placenta percreta with largeplacental mass eroding the posterior and lateral side of the lower uterinesegment, major adhesion between uterus and bladder, multiple subserousvessels, and left ureter involvement

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