Warshak, Carri R. MD; Eskander, Ramez MD; Hull, Andrew D. MD; Scioscia, Angela L. MD; Mattrey, Robert F. MD; Benirschke, Kurt MD; Resnik, Robert MD
Placenta accreta occurs as a result of a defect in the decidua basalis, allowing the anchoring villi to penetrate into the myometrium. When the trophoblastic tissue is found deeper within, or through the serosal surface of the uterus, the terms placenta increta and percreta are used, respectively. Although extremely rare 30 years ago, the frequency of abnormal placentation has increased 10-fold and is now observed in 9.3% of women with placenta previa or in 1 of 533 deliveries.1 Prior uterine surgery, most commonly cesarean delivery, is thought to cause the decidual defect, and the increase in placenta accreta may be attributed primarily to the rising cesarean delivery rate, which reached an all-time high of 29.1% in the United States in 2004.2 Other risk factors, such as maternal age greater than 35 years, smoking, subserosal uterine myomas, previous myomectomy, and Asherman’s syndrome, have also been reported.3 However, the central contributory role of previous cesarean delivery is illustrated by the fact that nulliparous women with a placenta previa have a risk for placenta accreta of 1–3%. In contrast, among those with two or more previous cesarean deliveries who have a placenta previa or low-lying anterior placenta, the risk increases to 30–50%.3,4
The immediate clinical consequence of placenta accreta is massive hemorrhage at the time of attempted placental removal, and it is the most common indication for emergency intra- or postpartum hysterectomy.5 The maternal mortality risk may reach 7%, and the extensive surgically related morbidities include massive transfusion, infection, urologic injury, and fistula formation.6
Optimal management of women with placenta accreta requires recognition of clinical risk factors, accurate preoperative diagnosis, detailed maternal counseling, and meticulous planning to ensure safety at the time of delivery. The purpose of this study was to evaluate and report our experience with using both pelvic ultrasonography and magnetic resonance imaging (MRI) for the diagnosis of placenta accreta.
MATERIALS AND METHODS
We conducted a historical cohort study of pregnant women from our obstetric and radiologic databases between January 2000 and June 2005 at the University of California, San Diego Medical Center. The women studied had a diagnosis of placenta previa, low-lying placenta with a previous cesarean delivery, or myomectomy, and they were evaluated for the possibility of placenta accreta by ultrasonography. The records of those referred for pelvic MRI because of suspicious or inconclusive findings for placenta accreta on previous ultrasound examination were also analyzed. The study protocol was approved by our Institutional Review Board. Inclusion was limited to those for whom complete information was available regarding clinical and pathologic diagnosis. Clinical information included gestational age at the time of diagnosis, previous uterine surgery, parity, clinical findings at the time of surgery, and pathologic diagnosis. Cesarean hysterectomy was recommended as the primary treatment for most women thought to have placenta accreta. The suspected depth of myometrial involvement did not effect counseling or clinical management, and for the purposes of this report, the diagnosis of placenta accreta refers to placenta increta and percreta as well as accreta.
Pelvic ultrasonography scans were performed by registered sonographers using both grayscale and color Doppler ultrasonography, and perinatal or radiological faculty interpreted all studies. The equipment included Siemens Sonoline Elegra (Siemens, Issaqua, WA) and GE Voluson 730 (GE Electric Medical Systems, Milwaukee, WI) with 3.5- or 5-MHz curvilinear, sector, and endovaginal transducers. The ultrasound findings considered to be consistent with placenta accreta included the following: 1) obliteration of the bladder wall–uterine interface with loss of the hypoechoic retroplacental myometrial zone; 2) adjacent placental sonolucent spaces; and 3) increased vascularity proximate to the bladder wall by color Doppler. Examples of a normal placental implantation, as well as typical findings in placenta accreta, are demonstrated in Figure 1. An ultrasound study was considered to be positive if the final interpretation included findings suggestive of, or conclusive for, placenta accreta. All studies considered to be suggestive but not conclusive underwent MRI evaluation.
Magnetic resonance imaging scans were performed on a Siemens Magnetom Symphony 1.5 Tesla scanner (Siemens Medical Solutions, Malvern, PA) equipped with high-performance gradients and phase-array coils. After informed consent was obtained, patients were placed on the scan table headfirst in whatever position they found most comfortable or turned toward a left lateral decubitus position. A radiologist with MR expertise monitored the entire study and guided the imaging work-up as is done with real-time ultrasound imaging.
Following a localizer scan, true patient sagittal and coronal scan series were acquired using the Half-fourier Acquisition with Single shot Turbo spin Echo (HASTE) with an effective echo-time of 90 ms in continuous 8-mm thickness slices covering the entire abdomen and pelvis. Additional HASTE sequences were then acquired to cover the entire placenta in three orthogonal planes, followed by selected oblique planes that are perpendicular to the placenta-uterine interface that is suspected. The HASTE sequence acquires sequential single slices rather than the full volume, where each image is acquired in a subsecond to freeze fetal motion. Additionally, two T1-weighted gradient echo turbo–flash sequences were then acquired orthogonal to each other and perpendicular to the suspect placenta-uterine interface to assess the outer uterine margin and acquire T1 and T2 signal characteristics of uterine, placenta, and parametrial tissues. The HASTE and T1-weighted scans are rapid and required intermittent breath-holding to minimize patient motion artifacts. This portion of the examination requires 15–20 minutes.
If the appearance of the placenta was suspect for placenta accreta (see criteria below), a dynamic gadolinium-enhanced MR series was then acquired perpendicular to the plane of the placenta-uterine interface suspected of being abnormal. The dynamic series is a Volume Interpolated Breathhold Examination (VIBE) acquired in the arterial phase and then again in the venous and equilibrium phases over the identical slices. This sequence is a 3D acquisition that used interpolated echoes and rapid fat-suppression where each series is acquired during a single breath-hold. When the dynamic series was needed, it added approximately 15 minutes to the study. The dose of gadolinium used was up to 0.1 mM/kg.
The appearance of the placenta on the precontrast examination was used to assess for the presence of placenta accreta. The characteristics used were the following: 1) thickened dark nodular contour of the placenta-uterine interface with extensions of the dark bands within the placenta; 2) mass effect of the placenta on the uterus causing an outer bulge; 3) heterogeneous placental signal on the T2-weighted HASTE sequences with large placental lakes or vessels. Assessment of the integrity of cervix, myometrium, bladder, and parametrial structures was also evaluated. All studies followed the above protocol and were interpreted by the same radiologist (R.F.M.).
The gadolinium-enhanced images acquired in the arterial phase defined the location of the outer placental surface relative to the myometrium, which was enhanced on the later sequences, and were used in all cases suspected to have placenta accreta. This confirmed the presence of deep invasion. Examples of the MRI appearance of normal and abnormal placentation are depicted in Figs. 2 and 3.
Pathology databases were then searched to verify the presence or absence of placenta accreta A clinical diagnosis of placenta accreta was made when the placenta was found to be adherent to the myometrium and difficult to remove and when hemorrhage ensued after attempts at placental delivery. All pathological specimens were reviewed by one of the authors (K.B.). The diagnosis of placenta accreta required that the anchoring villi directly abut the myometrium, without any intervening decidua basalis. The absence of decidual cells confirmed the diagnosis. The histologic appearance of placenta accreta in a term pregnancy is shown in Figure 4. The Gomori silver technique was employed to verify the nature of the basal cells by identifying decidual stromal cells possessing a distinctly silver-positive cell membrane, which is absent from the invasive extracellular trophoblastic cells. All true positive, as well as false positive and negative diagnoses were confirmed by pathologic examination (hysterectomy, curettings, or fragments of myometrium adherent to the placenta). A true negative was defined as an uncomplicated placental removal without excessive bleeding after vaginal or cesarean delivery.
Statistical analysis was performed using NCSS 2004 (NCSS, Kaysville, UT) statistical software. For both analyses we calculated sensitivity and specificity by using binary diagnostic test tables. Measures of test accuracy (eg, sensitivity, specificity, likelihood ratios, odds ratios) were computed with confidence intervals derived from Bayesian expansion.
During the study period, 453 women were found to have a diagnosis of placenta previa, low-lying placenta with previous cesarean delivery, or previous myomectomy, of whom 39 (8.6%) ultimately had clinical and pathologic confirmation of placenta accreta. Pelvic ultrasonography was accurate in predicting 30 of 39 placenta accretas (77%). The mean gestational age at diagnosis was 25.0 weeks (±standard error of the mean [SEM] 0.84) with a range of 11–37 weeks. Of the nine women with placenta accreta and a normal ultrasound study, five required hysterectomy because of hemorrhage at the time of delivery; the other four women did not have excessive bleeding and had tissue confirmation from curettings or placental tissue containing fragments of myometrium. Of the remaining 414 women without placenta accreta, ultrasonography correctly ruled out the diagnosis in 398 (96%) but was inaccurate in 16 instances (sensitivity 0.77, specificity 0.96, positive predictive value 0.65, negative predictive value 0.98). Of the 16 false positive diagnoses by ultrasound examination, MRI correctly predicted the absence of placenta accreta in 14 cases. Five women with placenta accreta were felt to have a definitive diagnosis of placenta accreta by ultrasonography and hence were not referred for MRI. The clinical characteristics and outcomes of the false positive and negative ultrasound studies are summarized in Table 1.
Thirty-nine women were ultimately found to have placenta accreta. Five women were nulliparous (12%), 33 women (85%) had a history of a prior cesarean delivery and 11 women had only one prior cesarean delivery (28%). One woman had only a history of a prior myomectomy. Thirty-five women had either planned or emergent cesarean hysterectomies.
Between January 2000 and June 2005, 42 women were referred for MRI studies to further evaluate a positive ultrasound study or because of ultrasound findings suggestive of, but not conclusive for, placenta accreta. Two women were unable to tolerate the procedure because of claustrophobia. Of the 40 women completing the study, 26 were subsequently confirmed by pathologic diagnosis to have placenta accreta. Magnetic resonance imaging was accurate in predicting 23 of 26 placenta accretas (88%) and ruled out the diagnosis correctly in all 14 women without placenta accreta (sensitivity 0.88, specificity 1.00, positive predictive value 1.0, negative predictive value 0.82). The mean gestational age at diagnosis with MRI was 28 weeks, with a range of 18–37 weeks (±SEM 0.71). The clinical characteristics and outcomes of the three women with false negative MRI studies are summarized in Table 2.
The accuracy of ultrasonography and MRI in predicting presence or absence of placenta accreta is summarized in Table 3, which presents test accuracy measures with confidence intervals. In general, MRI performed better than ultrasonography in identifying patients with placenta accreta (sensitivity 88%) and excluding those without (specificity 100%).
However, the 95% confidence intervals overlap, suggesting that the superiority of MRI over ultrasonography is not statistically significant.
Pelvic ultrasonography has been the most commonly used imaging modality for the diagnosis of placenta accreta. Finberg and Williams7 described its use in 34 women with a placenta previa and a previous cesarean delivery. They made a positive diagnosis in 18 women, of whom 14 had tissue confirmation. Sixteen were interpreted as negative, and one (6%) had placenta accreta at delivery. Subsequently, Levine and co-workers8 reported their experience with 19 women at risk, of whom seven had placenta accreta. Ultrasonography accurately identified six of the seven women and correctly identified normal placentation in 11 of 12 cases. In a larger series, Chou et al9 followed 80 women prospectively, and of 16 considered to have ultrasound findings consistent with placenta accreta, 14 had tissue evidence confirming the diagnosis. Of the remaining 64 studies interpreted as negative, placenta accreta was found in three, and the remainder was accurately diagnosed, resulting in a sensitivity of 82% and specificity of 96.8%. The findings of these three studies are similar to those presented in this paper, and taken together, suggest that ultrasonography has a primary role in screening women at risk of placenta accreta.
In contrast, a more recent report by Comstock et al10 suggested that the ultrasound diagnosis of placenta accreta by their criteria was accurate in 12 of 14 cases, but also noted 18 false positives. The differences in diagnostic accuracy of their findings compared with the three earlier reports, as well as the new findings presented above, may be explained by their use of only one characteristic to make the diagnosis, whereas the other studies took all the findings into consideration before coming to a diagnostic conclusion.
Until recently, MRI has received less attention than pelvic ultrasonography for the diagnosis of placenta accreta and with conflicting results. One of the above noted studies8 used MRI as an adjunctive modality to ultrasonography, but concluded that it added little to the diagnostic accuracy. Lam et al11 retrospectively evaluated 13 women with a diagnosis of placenta accreta, of whom nine had undergone MRI evaluation, and only four were confirmed by pathologic criteria to have placenta accreta. In a large series of 300 women suspected to have placenta accreta by ultrasonography, Palacios et al12 used MRI with gadolinium enhancement to delineate the topographic extent of abnormal placentation. However, these authors focused primarily on the depth of involvement and used only clinical correlation rather than pathologic examination to corroborate the accuracy of diagnosis. Consequently, it is difficult to determine with precision whether their MRI diagnoses were correct.
We believe that the use of gadolinium-based contrast enhancement adds to the specificity of MRI in the diagnosis of placenta accreta because it more clearly delineates the outer placental surface relative to the myometrium and eliminates the confusion between heterogeneous signals thought to be within the placenta from those caused by maternal blood vessels. There has been understandable reluctance to use gadolinium because of uncertainty regarding possible fetal effects. It readily crosses the placenta and enters into the fetal circulation and can be found in fetal tissues. However, there are no reports of deleterious effects in human fetuses. Moreover, gadolinium-based contrast agents are used commonly in radiologic studies of neonates and children. A recent statement by the American College of Radiology13 recommends that gadolinium-based MR contrast agents be given to pregnant women only after “a documented, in-depth analysis of the potential risks and benefits to that patient and her fetus.” A corresponding guideline statement by the European Society of Urogenital Radiology14 simply states that “when MR examination is necessary, gadolinium media may be given to the pregnant female,” and that no neonatal follow-up tests are necessary. Our clinical view is that placenta accreta is a potentially life-threatening obstetric complication, and that the benefits of early diagnosis, counseling, and surgical planning justify the theoretical risk of fetal gadolinium exposure.
In the United States, given that there are more than four million births per year, placenta accreta may complicate several thousand deliveries annually. As the cesarean delivery rate climbs, the risk of placenta accreta will increase proportionately. Given the extraordinary morbidity, as well as the risk of mortality in women with placenta accreta, appropriate counseling and management requires early and accurate prenatal diagnosis. Management may dictate hospitalization during pregnancy because of the risk of hemorrhage and will always require the availability of blood products, skilled anesthesia, special surgical expertise, and intensive care capability. A multidisciplinary approach including interventional radiology and urology may be needed as well.15–17
In conclusion, these data suggest that pelvic ultrasonography is highly reliable in ruling out the diagnosis of placenta accreta in women at risk. Among cases with suspicious but inconclusive findings on ultrasonography, MRI may be used to optimize diagnostic accuracy.
1. Wu S, Kocherginsky M, Hibbard JU. Abnormal Placentation: twenty-year analysis. Am J Obstet Gynecol 2005;192:1458–61.
2. Hamilton BE, Martin JA, Ventura SJ, Sutton PD, Menacker F. Births: preliminary data for 2004. Natl Vital Stat Rep 2005;54:1–17.
3. Clark SL, Koonings PP, Phelan JP. Placenta previa—accreta and prior cesarean section. Obstet Gynecol 1985;66:89–92.
4. Miller DA, Chollet JA, Goodwin TM. Clinical risk factors for placenta previa–placenta accreta. Am J Obstet Gynecol 1997;177:210–4.
5. Zelop CM, Harlow BL, Frigoletto FD Jr, Safon LE, Saltzman DH. Emergency peripartum hysterectomy. Am J Obstet Gynecol 1993;168:1443–8.
6. O’Brien JM, Barton JR, Donaldson ES. The management of placenta percreta: conservative and operative strategies. Am J Obstet Gynecol 1996;175:1632–8.
7. Finberg HJ, Williams JW. Placenta accreta: prospective sonographic diagnosis in patients with placenta previa and prior cesarean section. J Ultrasound Medicine 1992;11:333–9.
8. Levine D, Hulka CA, Ludmir J, Li W, Edelman RR. Placenta accreta: evaluation with color Doppler US, power Doppler US and MR imaging. Radiology 1997;205:773–6.
9. Chou MM, Ho ES, Lee YH. Prenatal diagnosis of placenta previa accreta with power amplitude ultrasonic angiography. Am J Obstet Gynecol 1997;177:1523–5.
10. Comstock CH, Love JJ, Bronsteen RA, Lee W, Vettraino IM, Huang RR, et al. Sonographic detection of placenta accreta in the second and third trimesters of pregnancy. Am J Obstet Gynecol 2004;190:1135–40.
11. Lam G, Kuller J, McMahon M. Use of magnetic resonance imaging and ultrasound in the antenatal diagnosis of placenta accreta. J Soc Gynecol Investig 2002;9:37–40.
12. Palacios Jaraquemada JM, Bruno CH. Magnetic resonance imaging in 300 cases of placenta accreta: surgical correlation of new findings. Acta Obstet Gynecol Scand 2005;84:716–24.
13. Kanal E, Borgstede JP, Barkovich AJ, Bell C, Bradley WG, Etheridge S, et al. American College of Radiology White Paper on MR Safety. AJR Am J Roentgenol 2004;182:1111–4.
14. Webb JA, Thomsen HS, Morcos SK. The use of iodinated and gadolinium contrast media during pregnancy and lactation. Eur Radiol 2005;15:1234–40.
15. American College of Obstetricians and Gynecologists. Placenta accreta. ACOG Committee Opinion 266. Washington, DC: ACOG; 2002.