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Accuracy of ultrasound for the prediction of placenta accreta

Published:March 17, 2014DOI:https://doi.org/10.1016/j.ajog.2014.03.029

      Objective

      Ultrasound has been reported to be greater than 90% sensitive for the diagnosis of accreta. Prior studies may be subject to bias because of single expert observers, suspicion for accreta, and knowledge of risk factors. We aimed to assess the accuracy of ultrasound for the prediction of accreta.

      Study Design

      Patients with accreta at a single academic center were matched to patients with placenta previa, but no accreta, by year of delivery. Ultrasound studies with views of the placenta were collected, deidentified, blinded to clinical history, and placed in random sequence. Six investigators prospectively interpreted each study for the presence of accreta and findings reported to be associated with its diagnosis. Sensitivity, specificity, positive predictive, negative predictive value, and accuracy were calculated. Characteristics of accurate findings were compared using univariate and multivariate analyses.

      Results

      Six investigators examined 229 ultrasound studies from 55 patients with accreta and 56 controls for 1374 independent observations. 1205/1374 (87.7% overall, 90% controls, 84.9% cases) studies were given a diagnosis. There were 371 (27.0%) true positives; 81 (5.9%) false positives; 533 (38.8%) true negatives, 220 (16.0%) false negatives, and 169 (12.3%) with uncertain diagnosis. Sensitivity, specificity, positive predictive value, negative predictive value, and accuracy were 53.5%, 88.0%, 82.1%, 64.8%, and 64.8%, respectively. In multivariate analysis, true positives were more likely to have placental lacunae (odds ratio [OR], 1.5; 95% confidence interval [CI], 1.4–1.6), loss of retroplacental clear space (OR, 2.4; 95% CI, 1.1–4.9), or abnormalities on color Doppler (OR, 2.1; 95% CI, 1.8–2.4).

      Conclusion

      Ultrasound for the prediction of placenta accreta may not be as sensitive as previously described.

      Key words

      See related editorial, page 87
      Placenta accreta is defined as an abnormal adherence of placental villi to underlying myometrium with an absence of decidua basalis. Failure to anticipate placenta accreta and prepare for its appropriate management can lead to emergency hysterectomy with profuse, life-threatening hemorrhage,
      • Miller D.A.
      • Chollet J.A.
      • Goodwin T.M.
      Clinical risk factors for placenta previa-placenta accreta.
      • Belfort M.A.
      Publications Committee SfM-FM. Placenta accreta.
      disseminated coagulopathy, renal failure, acute respiratory distress, or even death.
      • Bauer S.T.
      • Bonanno C.
      Abnormal placentation.
      Additional surgical complications include cystotomy, ureteral injury, infection, venous thromboembolism or prolonged hospitalization.
      • Silver R.M.
      • Landon M.B.
      • Rouse D.J.
      • et al.
      Maternal morbidity associated with multiple repeat cesarean deliveries.
      • Eller A.G.
      • Porter T.F.
      • Soisson P.
      • Silver R.M.
      Optimal management strategies for placenta accreta.
      • Warshak C.R.
      • Ramos G.A.
      • Eskander R.
      • et al.
      Effect of predelivery diagnosis in 99 consecutive cases of placenta accreta.
      Accurate antenatal diagnosis of placenta accreta can allow arrangements to be made for a planned delivery at a tertiary care center utilizing a multidisciplinary approach, which has been shown to significantly reduce maternal morbidity.
      • Eller A.G.
      • Porter T.F.
      • Soisson P.
      • Silver R.M.
      Optimal management strategies for placenta accreta.
      • Warshak C.R.
      • Ramos G.A.
      • Eskander R.
      • et al.
      Effect of predelivery diagnosis in 99 consecutive cases of placenta accreta.
      • Eller A.G.
      • Bennett M.A.
      • Sharshiner M.
      • et al.
      Maternal morbidity in cases of placenta accreta managed by a multidisciplinary care team compared with standard obstetric care.
      As the incidence of placenta accreta increases concurrently with an increased incidence of cesarean delivery,
      • Miller D.A.
      • Chollet J.A.
      • Goodwin T.M.
      Clinical risk factors for placenta previa-placenta accreta.
      • Silver R.M.
      • Landon M.B.
      • Rouse D.J.
      • et al.
      Maternal morbidity associated with multiple repeat cesarean deliveries.
      • Clark S.L.
      • Koonings P.P.
      • Phelan J.P.
      Placenta previa/accreta and prior cesarean section.
      • MacDorman M.
      • Declercq E.
      • Menacker F.
      Recent trends and patterns in cesarean and vaginal birth after cesarean (VBAC) deliveries in the United States.
      patients and providers are more frequently confronted with difficult decisions such as whether to plan for a scheduled hysterectomy or to transfer care to a tertiary care center. With its implications for surgical morbidity and future fertility, this is not a decision taken lightly.
      Placenta previa and history of prior cesarean delivery remain the most important predictors of placenta accreta.
      • Silver R.M.
      • Landon M.B.
      • Rouse D.J.
      • et al.
      Maternal morbidity associated with multiple repeat cesarean deliveries.
      In addition to clinical risk factors, ultrasound is often used antenatally as an adjunct to clinical history to modify risk estimation for placenta accreta. The accuracy of ultrasound for the prediction of placenta accreta is generally reported to be good with sensitivities ranging from 77–97%.
      • Chou M.M.
      • Ho E.S.
      • Lee Y.H.
      Prenatal diagnosis of placenta previa accreta by transabdominal color Doppler ultrasound.
      • Warshak C.R.
      • Eskander R.
      • Hull A.D.
      • et al.
      Accuracy of ultrasonography and magnetic resonance imaging in the diagnosis of placenta accreta.
      • Dwyer B.K.
      • Belogolovkin V.
      • Tran L.
      • et al.
      Prenatal diagnosis of placenta accreta: sonography or magnetic resonance imaging?.
      • Wong H.S.
      • Cheung Y.K.
      • Zuccollo J.
      • Tait J.
      • Pringle K.C.
      Evaluation of sonographic diagnostic criteria for placenta accreta.
      • Shih J.C.
      • Palacios Jaraquemada J.M.
      • Su Y.N.
      • et al.
      Role of three-dimensional power Doppler in the antenatal diagnosis of placenta accreta: comparison with gray-scale and color Doppler techniques.
      • Esakoff T.F.
      • Sparks T.N.
      • Kaimal A.J.
      • et al.
      Diagnosis and morbidity of placenta accreta.
      However, prior studies on the accuracy of ultrasound for the prediction of accreta may be subject to bias because of single expert observers, suspicion for accreta, and knowledge of risk factors. Our objective was to assess the accuracy of ultrasound for the prediction of placenta accreta using multiple observers blinded to clinical status.

      Materials and Methods

      Patients who delivered at the University of Utah between 2000 and 2012 with documentation of a clinical or histopathologic diagnosis of placenta accreta
      • Eller A.G.
      • Porter T.F.
      • Soisson P.
      • Silver R.M.
      Optimal management strategies for placenta accreta.
      • Eller A.G.
      • Bennett M.A.
      • Sharshiner M.
      • et al.
      Maternal morbidity in cases of placenta accreta managed by a multidisciplinary care team compared with standard obstetric care.
      • Wu S.
      • Kocherginsky M.
      • Hibbard J.U.
      Abnormal placentation: twenty-year analysis.
      were identified and matched to patients with placenta previa but no accreta by year of delivery. Histopathalogic diagnosis of accreta was confirmed by documentation of placental invasion into the myometrium, and clinical diagnosis of accreta was confirmed by documentation of abnormal adherence of the placenta or evidence of gross placental invasion at the time of surgery. Patients were included if they had ultrasound images of the placenta available at a gestational age of greater than or equal to 16 weeks. For each patient, every image of the placenta was collected, de-identified, and blinded to clinical history. Images from each study were then placed in random sequence using the Microsoft Excel random number generator.
      Six investigators consisting of 3 experienced obstetric radiologists (A.M.K., T.C.W., and P.J.W.) and 3 maternal-fetal medicine physicians (A.J.E., D.S.R., and R.M.S.) prospectively reviewed and interpreted each ultrasound study. All 3 radiologists are fellowship trained in abdominal imaging and have more than 10 years' experience in obstetric ultrasound, including evaluation of accreta. Similarly, all 3 maternal-fetal medicine specialists are fellowship trained and have a minimum of 8 years of experience in diagnosing placenta accreta (>20 years for 2 of the 3 physicians). Investigators were asked to score each imaging study for the presence of accreta (“yes,” “no,” or “unable to determine”) and indicate the presence or absence of specific findings that have been reported to be associated with its diagnosis. These findings included the following: number of lacunae,
      • Comstock C.H.
      • Love Jr., J.J.
      • Bronsteen R.A.
      • et al.
      Sonographic detection of placenta accreta in the second and third trimesters of pregnancy.
      • Finberg H.J.
      • Williams J.W.
      Placenta accreta: prospective sonographic diagnosis in patients with placenta previa and prior cesarean section.
      • Twickler D.M.
      • Lucas M.J.
      • Balis A.B.
      • et al.
      Color flow mapping for myometrial invasion in women with a prior cesarean delivery.
      • Isaacs D.L.
      • Rouse G.A.
      • Lange Md
      • Goeser C.D.
      • Lyko E.
      The sonographic appearance of placenta accreta.
      loss of retroplacental clear space,
      • Wong H.S.
      • Cheung Y.K.
      • Zuccollo J.
      • Tait J.
      • Pringle K.C.
      Evaluation of sonographic diagnostic criteria for placenta accreta.
      • Comstock C.H.
      • Love Jr., J.J.
      • Bronsteen R.A.
      • et al.
      Sonographic detection of placenta accreta in the second and third trimesters of pregnancy.
      • Finberg H.J.
      • Williams J.W.
      Placenta accreta: prospective sonographic diagnosis in patients with placenta previa and prior cesarean section.
      • Isaacs D.L.
      • Rouse G.A.
      • Lange Md
      • Goeser C.D.
      • Lyko E.
      The sonographic appearance of placenta accreta.
      • Hudon L.
      • Belfort M.A.
      • Broome D.R.
      Diagnosis and management of placenta percreta: a review.
      loss of visualization of the myometrium,
      • Isaacs D.L.
      • Rouse G.A.
      • Lange Md
      • Goeser C.D.
      • Lyko E.
      The sonographic appearance of placenta accreta.
      and bladder wall irregularity.
      • Isaacs D.L.
      • Rouse G.A.
      • Lange Md
      • Goeser C.D.
      • Lyko E.
      The sonographic appearance of placenta accreta.
      If color Doppler was used, investigators further identified the presence or absence of the following: subplacental vascularity,
      • Chou M.M.
      • Ho E.S.
      • Lee Y.H.
      Prenatal diagnosis of placenta previa accreta by transabdominal color Doppler ultrasound.
      • Warshak C.R.
      • Eskander R.
      • Hull A.D.
      • et al.
      Accuracy of ultrasonography and magnetic resonance imaging in the diagnosis of placenta accreta.
      • Comstock C.H.
      Antenatal diagnosis of placenta accreta: a review.
      vessels bridging from the placenta to the uterine margin,
      • Chou M.M.
      • Ho E.S.
      • Lee Y.H.
      Prenatal diagnosis of placenta previa accreta by transabdominal color Doppler ultrasound.
      • Wong H.S.
      • Cheung Y.K.
      • Zuccollo J.
      • Tait J.
      • Pringle K.C.
      Evaluation of sonographic diagnostic criteria for placenta accreta.
      • Isaacs D.L.
      • Rouse G.A.
      • Lange Md
      • Goeser C.D.
      • Lyko E.
      The sonographic appearance of placenta accreta.
      gaps in myometrial blood flow,
      • Chou M.M.
      • Ho E.S.
      • Lee Y.H.
      Prenatal diagnosis of placenta previa accreta by transabdominal color Doppler ultrasound.
      • Isaacs D.L.
      • Rouse G.A.
      • Lange Md
      • Goeser C.D.
      • Lyko E.
      The sonographic appearance of placenta accreta.
      vessels crossing interface disruption sites,
      • Wong H.S.
      • Cheung Y.K.
      • Zuccollo J.
      • Tait J.
      • Pringle K.C.
      Evaluation of sonographic diagnostic criteria for placenta accreta.
      or turbulent lacunae.
      • Chou M.M.
      • Ho E.S.
      • Lee Y.H.
      Prenatal diagnosis of placenta previa accreta by transabdominal color Doppler ultrasound.
      • Moodley J.
      • Ngambu N.F.
      • Corr P.
      Imaging techniques to identify morbidly adherent placenta praevia: a prospective study.
      If a diagnosis was made, investigator confidence for each imaging study was scored on a scale of 0 (none) to 10 (certain), and image quality was scored on a scale from 1 (very poor) to 10 (best).
      Study data were collected and managed using REDCap electronic data capture tools hosted at the University of Utah.
      • Harris P.A.
      • Taylor R.
      • Thielke R.
      • Payne J.
      • Gonzalez N.
      • Conde J.G.
      Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support.
      REDCap (Research Electronic Data Capture) is a secure, web-based application designed to support data capture for research studies, providing: (1) an intuitive interface for validated data entry; (2) audit trails for tracking data manipulation and export procedures; (3) automated export procedures for seamless data downloads to common statistical packages; and (4) procedures for importing data from external sources.
      Continuous variables were analyzed with the Student t test. Categorical variables were analyzed by the Wilcoxon-Mann-Whitney, χ2 or Fisher exact test, where appropriate. Sensitivity, specificity, positive predictive value, negative predictive value, and accuracy were calculated according to standard definitions. For multivariate analyses, all variables of interest were included in a logistic regression model. Covariates were then removed in a stepwise fashion until all covariates in the final model for a particular outcome had a P value of < .2. Receiver operating characteristic curves were generated and the area under the curve computed to determine the discriminative ability of ultrasound to correctly identify placenta accreta.
      • Cantor S.B.
      • Kattan M.W.
      Determining the area under the ROC curve for a binary diagnostic test.
      A P value of < .05 was considered statistically significant. All statistical analyses were performed using Stata 12.1 (StataCorp, College Station, TX). The institutional review board of the University of Utah approved this study.

      Results

      After exclusions, we identified 55 women with placenta accreta with available imaging studies at the University of Utah between 2000 and 2012. Fifty-six women with placenta previa but no accreta and appropriate imaging studies and matched to cases by year of delivery were chosen as controls. Clinical data are summarized in Table 1. Compared with patients with placenta previa only (no accreta), those with placenta accreta had significantly higher parity, more prior cesarean deliveries and an earlier gestational age at delivery. Maternal age and body mass index at the time of delivery were similar.
      Table 1Patient characteristics
      CharacteristicAccreta (Cases)ControlsP value
      Maternal age, y (mean ± SD)32.4 ± 5.231.3 ± 6.9.36
      Students t test
      Body mass index, kg/m2 (mean ± SD)29.0 ± 9.431.9 ± 6.9.15
      Students t test
      Gravidity (median, range)5 (2–18)4 (1–14).0047
      Wilcoxon-Mann-Whitney test
      Parity (median, range)3 (1–7)2 (0–10).0090
      Wilcoxon-Mann-Whitney test
      Cesarean delivery (n, %)< .001
      Fisher exact test.
      01 (1.8)16 (28.6)
      117 (30.9)25 (44.6)
      216 (29.1)9 (16.1)
      3+21 (38.2)6 (10.7)
      Delivery gestational age, wk (mean ± SD)33.8 ± 3.034.9 ± 4.0.12
      Students t test
      Gestational age at study, wk (median, interquartile range)29.2 (25.1–32.4)29.3 (23.9–33.6).11
      Wilcoxon-Mann-Whitney test
      Bowman. Accuracy of ultrasound for the prediction of placenta accreta. Am J Obstet Gynecol 2014.
      a Students t test
      b Wilcoxon-Mann-Whitney test
      c Fisher exact test.
      The 55 women with placenta accreta had a total of 116 ultrasound studies and the 56 women with placenta previa but no accreta had 113 studies. Thus, a total of 229 ultrasound studies were available for review. All ultrasound images were collected, deidentified, and placed in a random order. Each of the 6 investigators reviewed all studies for a total of 1374 independent observations.
      A specific diagnosis regarding the presence or absence of placenta accreta was reported for 1205/1374 (87.7%) studies, including 614/678 (90.6%) of controls and 591/696 (84.9%) of cases (P = .001). Of studies receiving a diagnosis, diagnostic performance characteristics were as follows: 371 true positives (30.8%), 81 false positives (6.7%), 533 true negatives (44.2%), and 220 false negatives (18.3%). 165/1374 studies (12.0%) were designated “unable to determine” and 4/165 studies (2.4%) were not given a diagnosis. Results for sensitivity, specificity, positive predictive value, negative predictive value and overall accuracy are shown in Table 2. Two analyses are presented; one excluding studies that were interpreted as “uncertain” and one that assigned uncertain diagnoses as “no accreta.” Receiver operator characteristic curves, which accounted for ultrasound as a binary test (absence or presence of accreta), are shown in Figure 1. Overall, the diagnostic performance characteristics were improved when uncertain diagnoses were excluded.
      Table 2Diagnostic performance characteristics of ultrasound for the diagnosis of placenta accreta
      CharacteristicExcluding missing/uncertain diagnosesMissing/uncertain diagnoses assigned as no accreta
      Sensitivity62.8 (58.7–66.7)53.3 (49.5–57.1)
      Specificity86.8 (83.9–89.4)88.1 (85.4–90.4)
      PPV82.1 (78.7–85.0)82.1 (78.8–85.4)
      NPV70.8 (68.5–73.0)64.8 (62.9–66.7)
      Accuracy75.0 (72.5–77.4)65.8 (63.2–68.3)
      Data are % (95% confidence interval).
      NPV, negative predictive value; PPV, positive predictive value.
      Bowman. Accuracy of ultrasound for the prediction of placenta accreta. Am J Obstet Gynecol 2014.
      Figure thumbnail gr1
      Figure 1Receiver operating characteristic curve for ultrasound to accurately diagnose placenta accreta
      Areas under the curve are presented corresponding to inclusion or exclusion of uncertain or missing diagnoses.
      Bowman. Accuracy of ultrasound for the prediction of placenta accreta. Am J Obstet Gynecol 2014.
      Given that individual patients may have had more than one ultrasound study performed, we examined accuracy of diagnoses by patient. Diagnoses for the 56 women with previa only (ie, controls) were correct significantly more often than for the 55 cases (75% vs 60.4%, respectively, P < .0068). Similarly, concordant with higher overall specificity, incorrect results were lower for controls compared with cases (13.8% vs 27.0%, respectively, P = .0093). The ratio of unknown or missing diagnoses was not significantly different between cases and controls (13.3% vs 10.2%, respectively, P = .21).
      To determine which findings on ultrasound were associated with the presence of placenta accreta, an initial model was created with accreta as the outcome and included the following specific findings as covariates: number of lacunae, loss of the retroplacental clear space, loss of visualization of the myometrium, irregular bladder wall, or any color Doppler abnormalities. After stepwise removal of covariates from the model until remaining covariates had a P value of < .2, only loss of visualization of the myometrium was excluded in the final model. Placenta accreta was associated with more placental lacunae (odds ratio [OR], 1.4; 95% CI, 1.3–1.6), loss of the retroplacental clear space (OR, 2.2; 95% CI, 1.6–3.0), an irregular bladder wall (OR, 1.3; 95% CI, 1.0–1.6) and color Doppler abnormalities (OR, 1.3; 95% CI, 1.1–1.4). The receiver operating characteristic curve for this model is shown in Figure 2.
      Figure thumbnail gr2
      Figure 2Receiver operating characteristic curve for multivariable regression model to predict placenta accreta based on specific ultrasound findings.
      Bowman. Accuracy of ultrasound for the prediction of placenta accreta. Am J Obstet Gynecol 2014.
      Next, we examined whether specific ultrasound findings and/or patient demographic factors were associated with accurate and inaccurate diagnoses (ie, true positives, true negatives, false positives, false negatives, and uncertain diagnosis). The results of univariate analyses are shown in Table 3. True positives were significantly associated with lower maternal BMI (26.9 vs 29.1, P = .0034), better image quality (6.1 vs 5.7, P = .0026), more lacunae (5 vs 1.2, P < .001), loss of the retroplacental clear space (91.9% vs 19.0%, P < .001), an irregular bladder wall (39.4% vs 4.3%, P < .001) and color Doppler abnormalities (97.3% vs 65.7%, P < .001). False positives were associated with similar findings, but color Doppler abnormalities were not significantly different from other diagnoses (P = .45).
      Table 3Specific findings associated with accurate and inaccurate diagnoses
      VariableTrue positiveTrue negativeFalse positiveFalse negativeDiagnosis given
      YesNoP valueYesNoP valueYesNoP valueYesNoP valueYesNoP value
      Gestational age at study, wk28.9 ± 4.928.3 ± 5.5.04328.7 ± 5.628.3 ± 5.2.2828.0 ± 5.328.5 ± 5.4.4627.5 ± 5.228.7 ± 5.4.003428.5 ± 5.328.3 ± 5.6.59
      Maternal age at study, y33.0 ± 5.031.8 ± 6.7.001532.4 ± 5.531.6 ± 7.5.02131.4 ± 5.832.1 ± 6.4.2831.3 ± 5.832.2 ± 6.4.04232.0 ± 6.433.1 ± 5.6.029
      Maternal BMI at delivery26.9 ± 9.929.1 ± 10.3.003428.5 ± 10.128.5 ± 10.4.9423.6 ± 11.628.8 ± 10.1< .00131.8 ± 9.527.7 ± 10.3< .00128.4 ± 10.229.4 ± 10.6.37
      Number of placental lacunae5.0 ± 2.71.2 ± 2.7< .0010.74 ± 1.03.2 ± 2.8< .0012.9 ± 2.42.2 ± 2.6.0141.4 ± 1.42.4 ± 2.7< .0012.3 ± 2.61.7 ± 1.9.009
      Image quality
      Image quality was scored on a scale from 1 to 10 with 10 representing the best image quality
      6.1 ± 1.95.7 ± 2.2.00266.2 ± 2.05.6 ± 2.1< .0015.6 ± 2.15.8 ± 2.1.325.7 ± 2.05.9 ± 2.1.306.0 ± 2.04.0 ± 2.0< .001
      Confidence of interpretation
      Investigator confidence was scored on a scale from 0 to 100% with 100% representing the highest confidence.
      63.2 ± 22.369.5 ± 22.4< .00176.4 ± 19.561.6 ± 22.6< .00148.0 ± 25.869.0 ± 21.7< .00168.9 ± 21.567.4 ± 22.8.3969.0 ± 22.749.0 ± 9.4< .001
      Loss of retroplacental clear space341 (91.9)191 (19.0)< .00128 (5.3)504 (59.9)< .00170 (86.4)462 (35.7)< .00125 (11.4)507 (43.9)< .001464 (38.5)68 (40.2)< .001
      Loss of visualization of the myometrium338 (91.1)188 (18.7)< .00128 (5.3)498 (59.2)< .00167 (82.7)459 (35.5)< .00125 (11.4)501 (43.4)< .001458 (38.5)68 (40.2)< .001
      Irregular bladder wall146 (39.4)43 (4.3)< .00110 (1.9)179 (21.3)< .00118 (22.2)171 (13.2).01412 (5.45)177 (15.3).001186 (15.4)3 (1.8)< .001
      Any abnormal Doppler finding361 (97.3)659 (65.7)< .001322 (60.4)698 (83.0)< .00166 (81.5)954 (73.8).45149 (67.7)871 (75.5).022898 (74.5)122 (72.2)< .001
      Data are mean ± SD or n (%); P value determined by Student t test or χ2 test where appropriate.
      Bowman. Accuracy of ultrasound for the prediction of placenta accreta. Am J Obstet Gynecol 2014.
      a Image quality was scored on a scale from 1 to 10 with 10 representing the best image quality
      b Investigator confidence was scored on a scale from 0 to 100% with 100% representing the highest confidence.
      In contrast to the positive results (accreta thought to be present), true negatives had fewer lacunae (0.7 vs 3.2, P < .001), and fewer instances of loss of retroplacental clear space (5.3% vs 59.9%, P < .001), loss of visualization of the myometrium (5.3% vs 59.2%, P < .001), irregular bladder wall (1.9% vs 21.3%, P < .001) or abnormal color Doppler findings (60.4% vs 83.0%, P < .001). False negatives were similarly associated with these findings.
      Studies given an “uncertain” diagnosis were associated with relatively poorer image quality (4.0 vs 6.0, P < .001). Also, the magnitude of the differences between cases and controls with regard to placental lacunae, loss of the retroplacental clear space, loss of visualization of the myometrium, an irregular bladder wall, and color Doppler abnormalities was less pronounced than for studies given a “diagnosis.”
      For each diagnosis, an initial multivariate model was created that included specific ultrasound findings, perceived image quality, gestational age at which the study was performed, maternal age at delivery, and maternal BMI. Covariates were then removed in a stepwise fashion until all covariates in the final models had a P value of < .2. True positives were more likely to have placental lacunae (OR, 1.5; 95% CI, 1.4–1.6), loss of the retroplacental clear space (OR, 2.4; 95% CI, 1.1–4.9), or 1 or more abnormalities on color Doppler (OR, 2.1; 95% CI, 1.8–2.4), earlier study year (OR, 0.93; 95% CI, 0.88–0.99), and absence of an irregular bladder wall (OR, 0.66; 95% CI, 0.50–0.89). True negatives were more likely to have fewer lacunae (OR, 0.64; 95% CI, 0.57–0.73), better image quality (OR, 1.2; 95% CI, 1.12–1.29), and more advanced gestational age at the time of the study (OR, 1.05; 95% CI, 1.02–1.08). As might be expected, true negatives were less likely to have loss of the retroplacental clear space (OR, 0.34; 95% CI, 0.15–0.75) or 1 or more color Doppler abnormalities (OR, 0.50; 95% CI, 0.39–0.65).
      False positives were associated with loss of the retroplacental clear space (OR, 2.7; 95% CI, 1.9–3.8) or 1 or more color Doppler abnormalities (OR, 1.2; 95% CI, 1.1–1.4) and absence of an irregular bladder wall (OR, 0.47; 95% CI, 0.30–0.73). False negatives were associated with an earlier gestational age (OR, 0.96; 95% CI, 0.94–0.99), placental lacunae (OR, 1.2; 95% CI, 1.1–1.3), and inversely associated with loss of visualization of the myometrium (OR, 0.30; 95% CI, 0.19–0.46) and 1 or more color Doppler abnormalities (OR, 0.54; 95% CI, 0.43–0.68). Image studies for which a diagnosis was unable to be determined were inversely associated with image quality (OR, 0.68; 95% CI, 0.62–0.76) and 1 or more color Doppler abnormalities (OR, 0.62; 95% CI, 0.49–0.79), whereas loss of visualization of the myometrium (OR, 3.7; 95% CI, 2.7–5.1) and an irregular bladder wall (OR, 1.7; 95% CI, 1.3–2.1) showed positive associations.

      Comment

      Placenta previa and history of prior cesarean delivery are known risk factors for placenta accreta. The risk for placenta accreta with a previa and 1, 2, 3, or ≥4 prior cesarean deliveries is 11, 40, 61, and 67 percent, respectively.
      • Silver R.M.
      • Landon M.B.
      • Rouse D.J.
      • et al.
      Maternal morbidity associated with multiple repeat cesarean deliveries.
      Thus, with a previa and 2 prior cesarean deliveries, the pretest probability for placenta accreta is approximately 40%. Ultrasound is the mainstay for prenatal assessment of accreta, and the ability of ultrasound to accurately predict the presence of placenta accreta is reported to be excellent. One recent systematic review and metaanalysis examined the diagnostic value of ultrasound and noted a pooled sensitivity of 83% and a robust area under the summary receiver operating characteristic curve of 0.9485.
      • Meng X.
      • Xie L.
      • Song W.
      Comparing the diagnostic value of ultrasound and magnetic resonance imaging for placenta accreta: a systematic review and meta-analysis.
      However, the 13 studies included were limited by a low number of cases per study, a priori knowledge of risk factors, and single expert (or unspecified) observers. Our results show that when images are reviewed by a diverse group of providers, blinded to any clinical history, ultrasound for the prediction of placenta accreta may not be as sensitive or accurate as previously described.
      Chalubinski et al,
      • Chalubinski K.M.
      • Pils S.
      • Klein K.
      • et al.
      Prenatal sonography can predict degree of placental invasion.
      Esakoff et al,
      • Esakoff T.F.
      • Sparks T.N.
      • Kaimal A.J.
      • et al.
      Diagnosis and morbidity of placenta accreta.
      Warshak et al,
      • Warshak C.R.
      • Eskander R.
      • Hull A.D.
      • et al.
      Accuracy of ultrasonography and magnetic resonance imaging in the diagnosis of placenta accreta.
      and Chou et al
      • Chou M.M.
      • Ho E.S.
      • Lee Y.H.
      Prenatal diagnosis of placenta previa accreta by transabdominal color Doppler ultrasound.
      reported the largest studies (≥80 patients) of ultrasound for the prediction of accreta with 232, 108, 453, and 80 patients included, respectively. The total number of patients with confirmed accreta in these studies (ie, cases) was 35, 19, 46, and 16 with sensitivities of 91, 89, 77, and 82 percent, respectively. The corresponding accuracies (number of true positives and true negatives divided by total number of patients in the study) were 95, 91, 95, and 94 percent. For each study, patient history and risk for accreta were known. When only studies that were given a diagnosis were considered in our study, the sensitivity of 62.8% was lower than previously reported. If images with an uncertain diagnosis are treated as a negative result, our sensitivity of 53.5% and accuracy of 65.8% are even worse with over 1/3 of cases misidentified.
      Chalubinski et al,
      • Chalubinski K.M.
      • Pils S.
      • Klein K.
      • et al.
      Prenatal sonography can predict degree of placental invasion.
      Esakoff et al,
      • Esakoff T.F.
      • Sparks T.N.
      • Kaimal A.J.
      • et al.
      Diagnosis and morbidity of placenta accreta.
      Warshak et al,
      • Warshak C.R.
      • Eskander R.
      • Hull A.D.
      • et al.
      Accuracy of ultrasonography and magnetic resonance imaging in the diagnosis of placenta accreta.
      and Chou et al
      • Chou M.M.
      • Ho E.S.
      • Lee Y.H.
      Prenatal diagnosis of placenta previa accreta by transabdominal color Doppler ultrasound.
      reported specificities of 96, 91, 96, and 97 percent respectively. Our specificity was similar regardless of how uncertain diagnoses were treated, 86.8% if excluded and 88.1% if included. Although this suggests that a negative ultrasound is able to accurately identify those patients without accreta, the lower negative predictive value (64.8%) suggests that an important number of those with a negative ultrasound will be misdiagnosed (ie, have an accreta).
      When considering a diagnostic test, ultimately one needs to decide whether the results of that test will change the management of a given patient. Accordingly, one should consider likelihood ratios, the percentage of affected people with a positive test result divided by the percentage of unaffected individuals with a negative test result, along with pre- and posttest probabilities.
      • Grimes D.A.
      • Schulz K.F.
      Refining clinical diagnosis with likelihood ratios.
      Using the pooled sensitivity and specificity from the previously mentioned metaanalysis (83% and 95%, respectively), the likelihood ratio positive is calculated to be 16.6 with ratios greater than 10 generally thought to yield a large increase in posttest probability. Thus, in a patient with a previa and 1 or 2 prior cesarean deliveries, the pretest probabilities would be 11 and 40%, respectively, and the posttest probabilities would be approximately 65 and 90% for a positive ultrasound result. Conversely, the likelihood ratio negative would be 0.18 with posttest probabilities of approximately 2 and 10% respectively. Even with a relatively good test, we cannot completely eliminate the possibility of an accreta. In the case of a previa and 2 prior cesarean deliveries, the posttest probability is reduced from 40% to 10%, but for some providers this might not be a sufficient reduction in risk to avoid a planned cesarean hysterectomy. Consider then that these likelihood ratios and diagnostic performance characteristics have already taken into account pre-test probabilities and may be overly optimistic. If the blinded diagnostic performance characteristics are considered (sensitivity of 53.5% and specificity of 88%), the likelihood ratio positive is only 4.5 (associated with only a moderate increase in the post-test probability) and the likelihood ratio negative only 0.53. Thus for a patient with a previa and 2 prior cesarean deliveries, the posttest probability of a positive and negative ultrasound result would be approximately 65% and 20%, respectively. Regardless of the ultrasound result, these posttest probabilities are sufficiently imprecise so as to be useful as an adjunctive test but not as a definitive “gold standard.”
      Previous studies have shown that the number of placental lacunae,
      • Comstock C.H.
      • Love Jr., J.J.
      • Bronsteen R.A.
      • et al.
      Sonographic detection of placenta accreta in the second and third trimesters of pregnancy.
      • Finberg H.J.
      • Williams J.W.
      Placenta accreta: prospective sonographic diagnosis in patients with placenta previa and prior cesarean section.
      • Twickler D.M.
      • Lucas M.J.
      • Balis A.B.
      • et al.
      Color flow mapping for myometrial invasion in women with a prior cesarean delivery.
      • Isaacs D.L.
      • Rouse G.A.
      • Lange Md
      • Goeser C.D.
      • Lyko E.
      The sonographic appearance of placenta accreta.
      loss of retroplacental clear space,
      • Wong H.S.
      • Cheung Y.K.
      • Zuccollo J.
      • Tait J.
      • Pringle K.C.
      Evaluation of sonographic diagnostic criteria for placenta accreta.
      • Comstock C.H.
      • Love Jr., J.J.
      • Bronsteen R.A.
      • et al.
      Sonographic detection of placenta accreta in the second and third trimesters of pregnancy.
      • Finberg H.J.
      • Williams J.W.
      Placenta accreta: prospective sonographic diagnosis in patients with placenta previa and prior cesarean section.
      • Isaacs D.L.
      • Rouse G.A.
      • Lange Md
      • Goeser C.D.
      • Lyko E.
      The sonographic appearance of placenta accreta.
      • Hudon L.
      • Belfort M.A.
      • Broome D.R.
      Diagnosis and management of placenta percreta: a review.
      loss of visualization of the myometrium,
      • Isaacs D.L.
      • Rouse G.A.
      • Lange Md
      • Goeser C.D.
      • Lyko E.
      The sonographic appearance of placenta accreta.
      and bladder wall irregularity, and color Doppler abnormalities
      • Dwyer B.K.
      • Belogolovkin V.
      • Tran L.
      • et al.
      Prenatal diagnosis of placenta accreta: sonography or magnetic resonance imaging?.
      • Wong H.S.
      • Cheung Y.K.
      • Zuccollo J.
      • Tait J.
      • Pringle K.C.
      Evaluation of sonographic diagnostic criteria for placenta accreta.
      • Esakoff T.F.
      • Sparks T.N.
      • Kaimal A.J.
      • et al.
      Diagnosis and morbidity of placenta accreta.
      • Hudon L.
      • Belfort M.A.
      • Broome D.R.
      Diagnosis and management of placenta percreta: a review.
      • Moodley J.
      • Ngambu N.F.
      • Corr P.
      Imaging techniques to identify morbidly adherent placenta praevia: a prospective study.
      • Harris P.A.
      • Taylor R.
      • Thielke R.
      • Payne J.
      • Gonzalez N.
      • Conde J.G.
      Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support.
      are associated with placenta accreta. We found that each incremental increase in placental lacunae on a scale from 0 (none) to 10+ (many) was associated with a 1.4-fold increased risk for accreta as well as loss of the retroplacental clear space, an irregular bladder wall, and abnormalities using color Doppler, consistent with the observations of other studies. Furthermore, when the receiver operator characteristic curve was computed from this logistic regression model, the area under the curve was 0.82, suggesting that these factors may improve the diagnostic accuracy of ultrasound (Figure 2). Although the presence of these factors were associated with positive ultrasound result and the absence was associated with negative results, they do not appear to be useful for distinguishing accurate from inaccurate results (eg, true positives from false positives or true negatives from false negatives).
      Our study has several strengths. We were able to use a relatively large number of patients with accreta (55) that represents the largest number in the literature for which ultrasound was evaluated. Each patient had the potential for multiple studies (116 total) that were then evaluated independently by 6 investigators for 696 unique observations. Second, the images were evaluated by 3 radiologists and 3 maternal-fetal medicine physicians, which allowed for a diversity of evaluation that has not previously been reported and may be more applicable to general practice. Perhaps most importantly, the investigators evaluating ultrasound images were blinded to all clinical history and knowledge of risk factors. In this manner, the actual accuracy of ultrasound could be evaluated absent pretest bias based on history of prior cesarean delivery. Finally, all images were evaluated prospectively allowing for collection of the data points of interest.
      We acknowledge some weaknesses to our study as well. In practice, practitioners are aware of patient history and use this information to shape a diagnosis by performing the scan in real time and understanding certain practical measures, such as how much transducer pressure was used or sonographer experience. By blinding investigators, the environment is clearly an artificial one and in that respect may not be directly relevant to actual practice. In addition, although the images were prospectively evaluated by the investigators, the images themselves were collected retrospectively, which precluded the ability to use cine clips or real-time evaluation.
      In conclusion, the published accuracy of ultrasound for the diagnosis of placenta accreta is likely biased by knowledge of patient risk factors, which can significantly increase pretest probability. When evaluated by a diverse group of providers who blinded from patient history, the diagnostic performance characteristics of ultrasound may not be as high as previously reported.

      Acknowledgments

      University of Utah Center for Clinical and Translational Sciences grant support (CTSA 5UL1RR025764-02) enabled the use of REDCap (Research Electronic Data Capture) for this project.

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      Linked Article

      • Diagnosing placenta accreta
        American Journal of Obstetrics & GynecologyVol. 212Issue 2
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          While we wish to underscore a statement made in the editorial by Dr Nageotte,1 we wish to also add a relevant comment to the article by Bowman et al2 discussed in this same issue. In our own institution, we have seen a significant rise in the incidence of placenta accreta (doubling in the past dozen years), emphasizing the obvious contribution of the recently rising rate of cesarean. The concern that this should raise for the average practicing obstetrician is considerable, with regard to the results of this commonly unanticipated occurrence.
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