Ultrasound predictors of placental invasion: the Placenta ... · OBSTETRICS Ultrasound predictors...

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Ultrasound predictors of placental invasion:the Placenta Accreta IndexMartha W. F. Rac, MD; Jodi S. Dashe, MD; C. Edward Wells, MD; Elysia Moschos, MD;Donald D. McIntire, PhD; Diane M. Twickler, MD

OBJECTIVE: We sought to apply a standardized evaluation of ultra- RESULTS: Of 184 gravidas who met inclusion criteria, 54 (29%) had
sound parameters for the prediction of placental invasion in a high-riskpopulation.
STUDY DESIGN: This was a retrospective review of gravidas with �1prior cesarean delivery who received an ultrasound diagnosis ofplacenta previa or low-lying placenta in the third trimester at ourinstitution from 1997 through 2011. Sonographic images werereviewed by an investigator blinded to pregnancy outcome and so-nography reports. Parameters assessed included loss of retroplacentalclear zone, irregularity and width of uterine-bladder interface, smallestmyometrial thickness, presence of lacunar spaces, and bridgingvessels. Diagnosis of placental invasion was based on histologicconfirmation. Statistical analyses were performed using linear logisticregression and multiparametric analyses to generate a predictiveequation evaluated using a receiver operating characteristic curve.

From the Departments of Obstetrics and Gynecology (all authors) and RadioUniversity of Texas Southwestern Medical Center, Dallas, TX.

Received May 20, 2014; revised July 28, 2014; accepted Oct. 15, 2014.

The authors report no conflict of interest.

Presented at the 34th annual meeting of the Society for Maternal-Fetal MedicFeb. 3-8, 2014.

Corresponding author: Martha W. F. Rac, MD. Martha.Rac@utsouthwestern

0002-9378/$36.00 � ª 2015 Elsevier Inc. All rights reserved. � http://dx.doi.org/10.1

invasion confirmed on hysterectomy specimen. All sonographic pa-rameters were associated with placental invasion (P < .001). Con-structing a receiver operating characteristic curve, the combination ofsmallest sagittal myometrial thickness, lacunae, and bridging vessels,in addition to number of cesarean deliveries and placental location,yielded an area under the curve of 0.87 (95% confidence interval,0.80e0.95). Using logistic regression, a predictive equation wasgenerated, termed the “Placenta Accreta Index.” Each parameter wasweighted to create a 9-point scale in which a score of 0-9 provided aprobability of invasion that ranged from 2e96%, respectively.

CONCLUSION: Assignment of the Placenta Accreta Index may be helpfulin predicting individual patient risk for morbidly adherent placenta.

Key words: accreta, invasion, ultrasound

Cite this article as: Rac MWF, Dashe JS, Wells CE, et al. Ultrasound predictors of placental invasion: the Placenta Accreta Index. Am J Obstet Gynecol 2015;212:343.e1-7.

he morbidly adherent placenta
T (accreta, increta, and percreta) hasemerged as a significant obstetric challengeover the last decade. Once a rare diag-nosis,1 morbidly adherent placenta nowcomplicates as many as 1 per 500 preg-nancies.2 Antenatal diagnosis of placentalinvasion has the potential to improvematernal and fetal outcomes.3,4 Predeliv-ery knowledge of morbidly adherentplacenta allows for multidisciplinaryplanning and delivery before the onset oflabor and/or vaginal bleeding.5 Thisapproach has lowered overall maternalmorbidity rates, including less blood loss,as well as fewer transfusion requirementsand intraoperative urologic injuries.3,6
Sonography with grayscale and colorDoppler imaging is the recommendedfirst-line modality for diagnosing mor-bidly adherent placenta.5,7,8 Althoughmore elaborate forms of imaging arepromising in defining the topography ofthe placenta, such as 3-dimensionalDoppler and volume contrast ultra-sound, validation studies are lacking aswell as generalized applicability of tech-nique.9,10 The diagnosis of morbidlyadherent placenta involves a number ofdifferent ultrasound variables, somequalitative and others that have beenquantified. These markers include aninability to visualize the normal retro-placental clear zone, irregularity and

logy (Dr Twickler),

ine, New Orleans, LA,

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attenuation of the uterine-bladder inter-face, retroplacentalmyometrial thickness,presence of intraplacental lacunar spaces,and bridging vessels between the placentaand bladder wall when using colorDoppler.11-16 A recent metaanalysis of 23studies explored the contribution of theseultrasound parameters to the overallprediction of morbidly adherent placentaand found a promising sensitivity of 91%and specificity of 97%.17

A logical next step in predictingmorbidly adherent placenta by ultra-sound would be to determine the sig-nificance of each ultrasound finding, toestimate the probability of invasionbased on a multiparametric analysis.Our objective was to develop a predictiveequation for probability of invasionbased on a combination of ultrasoundparameters and clinical characteristics ina cohort of women at increased risk forplacental invasion.

MATERIALS AND METHODS

This was a retrospective review of grav-idas with �1 prior cesarean deliveries

can Journal of Obstetrics & Gynecology 343.e1

mailto:[email protected]

http://dx.doi.org/10.1016/j.ajog.2014.10.022

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FIGURE 1Loss of retroplacental clearspace

Echolucent line that sonographically represents

vascular decidua basalis and extends entire

length of placenta. The middle arrow points to

area of obliteration from invading placenta and

smaller 2 arrows show normal retroplacental

clear space.

Rac. Placenta Accreta Index. Am J Obstet Gynecol 2015.

FIGURE 3Thinning of uterine-bladderinterface

Normally thick and echogenic interface is

replaced by ingrowth of morbidly adherent

placenta (arrows).


FIGURE 2Irregularity of uterine-bladderinterface

Arrows point to dot-and-dash appearance of

echogenic uterine-bladder interface. This

irregularity is caused by abnormal bridging

vasculature that is easily seen with Doppler

velocimetry.


FIGURE 4Smallest myometrial thickness

Retroplacental myometrium is thin as result of

abnormal ingrowth of placenta. Smallest myo-

metrial thickness in sagittal plane is measured.

Measurement of smallest thickness is <1 mm.


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who had sonographic confirmation ofplacenta previa or low-lying placenta inthe third trimester at our ultrasound unitfromDecember 1997 through December2011 and were subsequently delivered atour hospital. This was a single-centerstudy of a nonreferred population.Sonographic images and associated re-ports used in the clinical management ofeach patient were stored electronically ina picture archiving and communicationsystem throughout the study period. Theterms “prior cesarean delivery” and“placenta previa/low-lying placenta”were queried from our sonographicdatabase, to identify women who metinclusion criteria. The diagnosis ofplacenta previa was based on the pres-ence of placental tissue covering the in-ternal cervical os. Low-lying placentawas diagnosed when the placenta waswithin 2 cm from the internal cervical osbut did not cover it.

All transvaginal and transabdominalultrasound images were individuallyreviewed by study investigators whowere blinded to sonography reportfindings and pregnancy outcomes. Ifimages were unable to be retrieved, thepatient was excluded from analysis.Sonographic parameters evaluated fromarchived images included location ofplacenta, loss of the retroplacental clearzone, irregularity and thickness of theuterine-bladder interface, the smallestmyometrial thickness in sagittal andtransverse planes, presence of lacunarspaces, and bridging vessels. The tech-nique and findings for each parameterare depicted in Figures 1-6. In additionto grayscale imaging, color Doppler wasused in assessment of abnormal vascu-lature. If any portion of the placentacovered the anterior lower uterinesegment, the placenta was considered tobe anterior. Lacunar spaces were gradedaccording to Finberg and Williams11 asfollows: grade 0, none seen; grade 1, 1-3present and generally small; grade 2, 4-6present and tending to be larger andmore irregular; grade 3, manythroughout the placenta and appearinglarge and bizarre. Confirmation ofmorbidly adherent placenta was basedon histologic evidence of placental in-vasion from the hysterectomy specimen.

343.e2 American Journal of Obstetrics & Gynecol

Pregnancies that met study inclusioncriteria but did not require a cesareanhysterectomy or have histologic evidenceof placental invasion on hysterectomyspecimen served as the comparisongroup.Statistical analyses included linear lo-

gistic regression and multiparametricanalyses. Only those parameters withcomplete data were used in the

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prediction model. The nonlinearity ofthe continuous measures was examinedusing cubic smoothing splines comparedto the direct linear contribution. Mea-sures found to offer significantimprovement in prediction undernonlinear forms were used for the pre-diction equation. A receiver operatingcharacteristic curve was derived for eachcombination of parameters (all subsetsregression) to select the combinationwith the greatest area under the receiveroperating characteristic curve. Thecombination of parameters that gave thelargest area under the curve was used togenerate a predictive equation, which we

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FIGURE 5Placenta lacunar spaces

Sonolucent areas throughout placenta that vary

in size and shape and give placenta “Swiss

cheese” appearance. This patient had >6

lacuna (arrows). They were large and very

bizarre-appearing throughout, consistent with

grade-3þ lacunae. Additionally, no myome-

trium is present between placenta and uterine-

bladder interface.


TABLE 1Demographic characteristics according to histologic evidence ofplacental invasion

CharacteristicPlacentalinvasion, n [ 54

No placentalinvasion, n [ 130 P value

Age, y 31.6 � 5.28 31.1 � 5.82 .59

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termed the “Placenta Accreta Index(PAI).” Each parameter was then given aweighted value based on the coefficientsfrom the estimated regression equationto provide the PAI score from 0-9, withmorbidly adherent placenta more likelyat higher index scores. The sensitivity,specificity, positive predictive value(PPV), and negative predictive value(NPV) were calculated for each indexscore, with 95% confidence intervals(CIs), using standard methods for rates

FIGURE 6Bridging vessels

Doppler color mapping demonstrates abnormal

vasculature that bridges from placental mass to

uterine-bladder interface and sometimes

beyond (arrows).


and proportions. Univariate analysisincluded Pearson c2 test for frequencymeasures and Student t test and Wil-coxon rank sum test for continuousmeasures. For presentation purposes,the receiver operating characteristiccurves were smoothed using binormalestimation technique. P values < .05were judged statistically significant. Thisstudy was approved by the institutionalreview board of the University of TexasSouthwestern Medical Center.

RESULTS

During the study period, 190 womenwith at least 1 prior cesarean deliverywere diagnosed with either placentaprevia or low-lying placenta duringthird-trimester sonography and weredelivered at our institution. Images from6 women were not able to be retrievedand thus excluded from the final anal-ysis. Of 184 women in the final analysis,54 (29%) had histologic confirmationof morbidly adherent placenta, andthe remaining 130 women served asthe comparison group. Maternal de-mographic characteristics are shown in

Race/ethnicity, n (%)

Black 5 (9)

White 3 (6)

Hispanic 45 (83)

Other 1 (2)

Gestational age atsonography, wk

33.0 � 2.7

Prior cesarean deliveries,n (%)

1 13 (24)

2 24 (44)

�3 17 (31)

Prior uterine curettage,n (%)

8 (15)

P < .05 significant. Values given as n (%) and � (SD).


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Table 1. There were no differences in age,race/ethnicity, or gestational age at ul-trasound between pregnancies with andwithout histologic evidence of placentalinvasion. As expected, the number ofprior cesarean deliveries was signifi-cantly associated with risk for placentalinvasion.

Sonographic findings are presented inTable 2. Anterior placentation wassignificantly associated with placentalinvasion, P < .05, as was each of thesonographic parameters we assessed, allP < .001. Using both the categoricalmeasures of our evaluation (loss of ret-roplacental clear zone, lacunae, bridgingvessels, irregularity of uterine-bladderinterface) and continuous parameters(myometrial thickness and uterine-bladder interface width), in addition tonumber of prior cesarean deliveries andplacental location, receiver operatorcurves were constructed using differentmultiparametric combinations. Of the184 pregnancies studied, 88 had each ofthese ultrasound variables assessed andwere included in the final model, ofwhich 29 had invasion proven on

4 (3) .30

10 (8)

110 (85)

5 (4)

33.7 � 2.3 .08

< .001

87 (67)

31 (24)

12 (9)

21 (16) .82


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TABLE 2Ultrasound parameters of entire cohort

Variable

Placentalinvasion,n [ 54

No placentalinvasion,n [ 130 P value

Anterior placentation 38 (70) 36 (28) < .001

Lacunae < .001

Grade 0 11 (20) 62 (48)

Grade 1 15 (28) 52 (40)

Grade 2 10 (19) 12 (9)

Grade 3 18 (33) 4 (3)

Bridging vessels 35 (65) 24 (18) < .001

Sagittal smallest myometrialthickness, mm

0.9 [0.0,2.2] 2.4 [0.0,4.0] < .001

Uterine-bladder interfacethickness, mm

2.4 [0.0,4.0] 3.3 [2.4,4.0] .003

Values given as n (%) or median [Quartile 1, Quartile 2].



histologic exam. As shown in Figure 7,the combination of placental location,smallest sagittal myometrial thickness,lacunae, bridging vessels, and number ofcesarean deliveries yielded the greatestarea under the receiver operating char-acteristic curve: 0.87 (95% CI,0.80e0.95). When compared with the

FIGURE 7Receiver operator curve forprediction of placental invasionusing ultrasound variables andnumber of prior cesareandeliveries

AUC, area under curve; CI, confidence interval.



variables of placental location andnumber of prior cesarean deliveriesalone, findings that would not generallyrequire specialized sonography, theaddition of smallest myometrial thick-ness, lacuna, and bridging vesselssignificantly improved the prediction ofthe model: P ¼ .03. This is shown inFigure 8. Through logistic regressionmodeling, a predictive equation, whichwe termed the “PAI,” was generated us-ing these 5 parameters, based on theaddition or weighting of each parameter.The estimated regression equation isdefined as: PAI¼ ef/(1þ ef), where f is alinear function of the selected parame-ters and e is the base associated with thenatural logarithm.Incorporating the parameters yields

the following equation:

f ¼ �0:1935� 0:0404 ðgrayscale sagittal myometrial thickness ½mm�Þ� 0:0911 ðif lacuna ¼ 2Þ þ 1:234 ðif lacuna ¼ 4Þ þ 0:4195 ðif bridging vesselsÞþ 1:1332 ðif >1 prior cesarean deliveryÞ þ 0:6772 ðif anterior placentationÞ:

Using variable selection by stepwiseanalysis, parameters most highly associ-ated with placental invasion in ourmodel are presented in descending orderin Table 3. Of the 54 women with his-tologic confirmation of placental

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invasion, 49 (91%) had at least one ofthese sonographic parameters.

We next assigned a weighted value toeach sonographic parameter used in ourindex (Table 4). The probability of in-vasion corresponding to these values aswell as the sensitivity, specificity, PPV,and NPV for each index score is pre-sented in Table 5. As shown in the table,the probability of invasion increases withincreasing PAI score, such that a score of9 confers a 96% chance of histologicplacental invasion. The PPV describesthe predictive value of the index scorecompared to the probability of invasion,which is based on individual patientcharacteristics derived from our popu-lation. By adding ultrasound variables topatient characteristics weighted to ob-servations derived from a high-riskpopulation, the PAI can assign a gradedprobability of invasion unique to eachindividual patient evaluated.

COMMENT

We found that a score derived from theultrasound parameters of smallestmyometrial thickness, lacunar spaces,and presence of bridging vessels, inaddition to the number of prior cesar-ean deliveries and placental location,was highly predictive of placental in-vasion among pregnancies at increasedrisk. The application of the PAI can behelpful in stratifying individual risk ofinvasion above the a priori risk basedon number of prior cesarean deliveriesand placental location.18 It may be usedfor counseling and preoperative plan-ning, by either heightening awarenessfor morbidly adherent placenta orproviding reassurance to a woman who

desires future fertility. It may also play arole in identifying women who maybenefit from referral to a tertiary centerthat has sufficient blood bank capacityand multidisciplinary services. Also,instead of using each ultrasound

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FIGURE 8Receiver operator curves for prediction of placental invasion

Dashed curve represents prediction of invasion using number of cesarean deliveries and anterior

placental location only. Solid curve represents prediction of invasion using Placenta Accreta Index

(addition of lacunar spaces, smallest myometrial thickness and bridging vessels). Comparison of 2

curves yield P ¼ .03.

AUC, area under curve; CI, confidence interval.


TABLE 4Value of each parameter isadded together to generatePlacenta Accreta Index scoreParametera Value

�2 cesarean deliveries 3.0

Lacunae

Grade 3 3.5

Grade 2 1.0

Sagittal smallest myometrialthicknessb

�1 mm 1.0

<1 but �3 mm 0.5

>3 but �5 mm 0.25

Anterior placenta previac 1.0

Bridging vessels 0.5a If parameter is not present, then value is 0; b Meas-ured in sagittal plane; c If any portion of placenta isanterior.

Rac. Placenta Accreta Index. Am J Obstet Gynecol2015.


variable individually, our model es-tablishes a scoring system for a stan-dardized ultrasound evaluation of allpatients at risk for morbidly adherent

TABLE 3OR estimates and CIs of each parameParameter

Grade-3 lacunae

No. of cesarean deliveries

Placental location

Grade-2 lacunae

Bridging vessels

Sagittal smallest myometrial thickness

CI, confidence interval; OR, odds ratio.


placenta that can be universallyadopted.Previous investigators have also pro-

posed a standardized evaluation of

ter used in Placenta Accreta IndexOR 95% CI

10.8 1.4e83

9.6 2.5e37.1

3.9 1.1e14.1

2.9 0.6e12.7

2.3 0.6e8.7

1.0 0.8e1.2

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women at risk for placental invasion.19

Weiniger et al20 recently reported a se-ries of 92 womenwith placental invasionand developed a predictive equationfrom mathematical modeling of clinicaland sonographic variables. In that series,ultrasound suspicion of invasion wasconsidered a single variable, rather thanbased on a scoring system. Weinigeret al20 found that the combination ofplacenta previa, number of prior cesar-ean deliveries, and ultrasound suspicionof invasion was more predictive thanultrasound variables alone, with an areaunder the receiver operator character-istic curve of 0.85. Our study confirmsthe predictive value of combining patientcharacteristics with ultrasound variablesassociated with placental invasion, and italso acknowledges the interaction be-tween the different variables as theycontribute to individual risk.

Our study also provides insight intothe individual predictive value of eachultrasound parameter of morbidlyadherent placenta. Grade-3 lacunae and>1 prior cesarean delivery wereweighted the highest in our estimatedregression equation. A strong relation-ship between lacunar spaces and


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TABLE 5Sensitivity, specificity, and positive and negative predictive values at each PAI score

PAI nProbability ofinvasion, % (95% CI)

Sensitivity(95% CI)

Specificity(95% CI)

PPV(95% CI)

NPV(95% CI)

>0 1 5 (1e15) 100 (88e100) 19 (10e31) 38 (27e49) 100 (72e100)

>1 1 10 (4e22) 97 (82e100) 47 (34e61) 47 (34e61) 97 (82e100)

>2 2 19 (10e32) 93 (77e99) 58 (44e70) 52 (38e66) 94 (81e99)

>3 4 33 (22e47) 86 (68e96) 68 (54e79) 57 (41e72) 91 (78e97)

>4 6 51 (36e66) 72 (53e87) 85 (73e93) 70 (51e85) 86 (75e94)

>5 6 69 (50e83) 52 (33e71) 92 (81e97) 75 (51e91) 79 (68e88)

>6 2 83 (63e93) 31 (15e51) 100 (94e100) 100 (66e100) 75 (64e84)

>7 2 91 (73e97) 24 (10e44) 100 (94e100) 100 (59e100) 73 (62e82)

>8 5 96 (81e99) 17 (6e36) 100 (94e100) 100 (48e100) 71 (60e81)

CI, confidence interval; NPV, negative predictive value; PAI, Placenta Accreta Index; PPV, positive predictive value.



placental invasion has previously beendescribed.6,11,12,21,22 Finberg and Wil-liams11 found that number and bizarreappearance of lacunar spaces wasdirectly correlated with certainty andseverity of morbidly adherent placenta.In a recent systematic review, overallpooled sensitivity and specificity oflacunar spaces from 13 studies was 77%and 95% with an overall diagnostic ac-curacy of 0.884.17 A similar relationshiphas been shown for number of priorcesarean deliveries.2,18,23 In one of thelargest prospective series to date, Silveret al18 found that in the setting ofplacenta previa, the risk of accreta was11%, 40%, and >60% in women with 1,2, and �3 prior cesarean deliveries,respectively.

Other characteristics found to bepositively associated with morbidlyadherent placenta in our model,although to a lesser degree, includeplacental location, grade-2 lacunarspaces, smallest myometrial thickness,and bridging vessels. Both retrospectiveand prospective studies,9,11,12,14,16,24 aswell as metaanalyses and systematic re-views,17 have shown high sensitivities foreach of the above parameters. In 2000,Twickler et al12 found that a smallestmyometrial thickness <1 mm identifiedin third-trimester pregnancies at risk forplacental invasion was 100% sensitiveand 72% specific with a PPVand NPVof72% and 100%, respectively.12


Hypervascularity of the uterine-bladderinterface using both 2- and 3-dimen-sional Doppler ultrasound had the bestdiagnostic performance in a recent pro-spective series of women with a priorcesarean delivery and placenta previa.9

Similarly, D’Antonio et al17 reportedthat the presence of bridging vesselsidentified with color Doppler imagingwas the most predictive ultrasoundparameter of morbidly adherentplacenta, with an overall diagnostic ac-curacy of 0.95.Assigning the PAI in clinical practice

may be helpful in interpreting thesevarious sonographic variables in light ofthe patient’s history. As an example, if awoman who has had 2 prior cesareandeliveries is found to have an anteriorplacenta previa with grade-3 lacunae,smallest myometrial thickness of 1 mm,and no bridging vessels, she wouldreceive 3 points for the prior cesareandeliveries, 1 point for anterior previa, 3.5points for grade-2 lacunae, and 0.5points for the smallest myometrialthickness of 1 mm. This would result in aPAI score of 8. Her probability of inva-sion would be 91% (95% CI 73e97%),with a sensitivity of 24%, specificity of100%, and PPV and NPV of 100% and73%, respectively. This is much higherthan her risk of invasion based onnumber of cesarean deliveries andplacental location alone, which would beonly 40%.18 Conversely, a woman with 1

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prior cesarean delivery (0 points), ante-rior placenta previa (1 point), grade-1lacunae (0 points), smallest myometrialthickness of 1 mm (1 point), and nobridging vessels (0 points) would have aPAI of only 2, conferring a 10% proba-bility of invasion (95% CI, 4e22%).Depending on availability of local re-sources and multidisciplinary care, re-sults from our index could thus be usedfor counseling and assist with referraldecisions.

Limitations of our study include theretrospective design. We were unable tocontrol for suspicion of invasion or im-ages recorded, which leads to certainultrasound parameters not being recor-ded. As a result, we limited the logisticregression to those patients with all pa-rameters measured (n ¼ 88) to avoidoverfitting our model. Not all women inour cohort underwent transvaginal im-aging. Although no studies have beenperformed that directly compare thediagnostic accuracy of transabdominalvs transvaginal ultrasound in the settingof suspected placental invasion, trans-vaginal ultrasound allows for a morecomplete evaluation of the lower uterinesegment and is the current recom-mended standard of care.8,25-27 There-fore, inclusion of transabdominalimaging could theoretically affect thepredictive value of our model. Addi-tionally, our model was developed onlyfor pregnancies in the third trimester

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with prior cesarean delivery and placentaprevia or low-lying placenta, those atgreatest risk for placental invasion, andwould not apply in lower-risk pregnan-cies. Factors such as maternal age, parity,and history of other uterine surgicalprocedures that have been associatedwith morbidly adherent placenta, suchas dilation and curettage, myomectomy,and endometrial ablation,7 were notincluded in our model. It is not knownwhether ultrasound parameters used toidentify morbidly adherent placenta aresimilarly predictive for cases outside ofthe lower uterine segment or in lower-risk populations. Further studies areneeded in these populations to optimizeantenatal diagnosis of morbidlyadherent placenta. Finally, despitemethodological flaws inherent to retro-spective studies, our model provides thegroundwork for which parametersshould be prospectively evaluated.

Despite these limitations, strengths ofour study include the size of the cohort, ablinded review process, and use of his-tologic confirmation of invasion. As aresult, our model is designed to identifypatients with clinically significantplacental invasion requiring cesareanhysterectomy. Additionally, we reportprobability of invasion, which is a moreclinically relevant method of riskgradation compared to an absolute cut-off value of invasion vs no invasion. Inconclusion, our study shows that astandardized risk assessment based onnumber of previous cesarean deliveriesand ultrasound findings can identifythose women at highest risk formorbidly adherent placenta. If verifiedprospectively, assignment of the PAI maybe helpful for patient counseling anddelivery planning, all of which may ul-timately improve pregnancy outcomes

in women with morbidly adherentplacenta. -

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