Abstract
Objective
To estimate the level of interobserver agreement in the calculation of placenta accreta index (PAI) as well as to evaluate the accuracy of PAI in prediction of morbidly adherent placenta.
Materials and methods
This was a prospective study where 45 pregnant women (from 28 to 37 weeks of gestational age) with at least one previous Caesarean section and ultrasound-proven placenta previa were included. A known and previously published scoring system, the PAI, was evaluated independently by two radiologists and the cases were followed for the delivery and histopathology outcome. The accuracy of the PAI and the level of interrater agreement was analysed using cross-table analysis, intraclass correlation efficient and Cohen’s kappa as statistical variables.
Results
Adherent placenta was found in 15 patients accounting for 33% of cases. The PAI showed nearly 90% sensitivity, specificity and the predictive values. Interrater agreement in calculation of PAI by the two radiologists was perfect with an intraclass correlation efficient of 0.959. An easy-to-use morbid adherent placenta score was also predicted to simplify the results of PAI, which showed moderate agreement (κ = 0.746).
Conclusions
The PAI can be helpful in stratifying the individual risk of placental invasion above the baseline risk. The PAI-derived, simplified scoring system called morbid adherent placenta score can be used as a simple tool to interpret and convey the results of PAI.
Keywords: Morbidly adherent placenta, accreta, prospective reliability study
Introduction
Morbidly adherent placenta is a type of placental attachment disorder where the placenta is inseparable from the uterus due to variable degrees of invasion of trophoblastic tissue across the uterine wall.1 Increasing rates of Caesarean sections are causing more chances of placenta accreta, which now affects nearly 1 in 533 pregnancies according to US-based data collected from 1982 to 2002.2 Placenta previa with previous Caesarean delivery poses the greatest risk for placenta accreta and the risk increases substantially after repeated surgeries, ranging from 3% to 67% from first to fifth surgery onwards.3 Risk of placental invasion in cases of placenta previa without Caesarean section ranges from 1% to 5%.4 Due to a higher probability of severe obstetric haemorrhage, it is one of the most common cause of Caesarean hysterectomies.5 Hence, early detection and predelivery knowledge of adherent placenta is crucial in the prevention of maternal morbidity and may be useful for multidisciplinary management of suspected placental invasion.
Ultrasonography (US) with colour Doppler is the first line imaging modality for the diagnosis of placental invasion.4,6,7 The accuracy and reproducibility of previous studies investigating morbidly adherent placenta are still under debate because each study used different US criteria and none employed interobserver variation in predicting placental invasion.7–14 Multiparametric analysis using a combination of various sonographic and clinical features of women at increased risk of invasive placenta was done by Rac et al.8 and they proposed a probability index, termed the placenta accreta index (PAI). This combines the number of previous Caesarean sections, location and morphology of the placenta, retroplacental zone, utero-placental interface, smallest myometrial thickness and the presence of bridging vessels.
The number of previous surgeries and the sonographic location of the placenta remain constant. However, the placental morphology and other sonographic details useful for calculation of PAI may vary and lead to discrepancy in the estimation or probability of invasive placenta. Therefore, it is imperative to estimate the reliability and reproducibility in calculation of the index, which is the focus of our study.
Material and methods
The study group included 45 pregnant women selected from the Department of Obstetrics and Gynaecology, presenting in their third trimester with a previous history of at least one Caesarean section and with US-diagnosed placenta previa. Placenta previa was considered based on transabdominal US showing the lower margin of the placenta within 2 cm of the internal os. This was further classified into low lying, marginal and complete placenta previa. The study was approved by the institutional review board and was conducted over a two-year period. Patients presenting with multiple gestations, active vaginal bleeding and retroplacental hematoma were excluded.
All patients were sent for standard obstetric ultrasound, where the PAI was calculated by two radiologists (SC with 10 years and AA with 6 years of experience), separately (blinded to each other’s results). The scans were done using an Acuson S2000 diagnostic ultrasound system (Siemens Healthcare, Erlangen, Germany) with a curvilinear 3.5 MHz transducer and a HS70A Prime diagnostic ultrasound system (Samsung Medison, Seoul, South Korea) with curvilinear 1–7 MHz transducer.
Placenta accreta index calculation
Number of previous Caesarean sections, placental location, placental morphology (grading of lacunae), smallest sagittal myometrial thickness and presence of bridging vessels are combined to give the PAI value. Table 1 shows the scoring system and value assigned to each of the variables, following the recommendations of Rac et al.8 Grading of placental lacunae was done according to Finberg and Williams classification (Figure 1) which is Grade 0 for no lacunae, Grade 1 for small 1–3 lacunae; Grade 2 for larger 4–6 lacunae and Grade 3 for many, large and bizarre shaped lacunae.7,15 There were no objective criteria used for differentiating small and large lacunae. Colour Doppler was also used for assessment of the flow in placental lacunae and for visualisation of the bridging vessels.
Table 1.
Value of each parameter to generate placenta accreta index.
| Parameters | Score/ value |
|---|---|
| <2 Caesarean deliveries | 0 |
| ≥2 Caesarean deliveries | 3.0 |
| Placental lacunae | |
| Grade 3 | 3.5 |
| Grade 2 | 1.0 |
| Grade 1 | 0 |
| Smallest myometrial thickness | |
| ≤1mm | 1.0 |
| <1 and ≥3mm | 0.5 |
| >3 and ≤5mm | 0.25 |
| Anterior placenta previa | 1.0 |
| Bridging vessels (visible on colourDoppler at uterine–bladder interface) | 0.5 |
Source: Rac MW. Placenta Accreta Index. Am J Obstet Gynecol 2014.
Modified & Reproduced with permission from Elsevier.
Figure 1.
US images showing Finberg–Williams classification of placental lacunae (shown as solid yellow arrows); (a) grade 0 with no lacunae; (b) grade 1 with 1–3 small lacunar spaces; (c) grade 2 with 4–6 large lacunae and (d) grade 3 with multiple (more than six), bizarre shaped lacunar spaces.
PAI values were further classified into two broad categories with values <5 as unfavourable for invasion and ≥ 5 as favourable for invasion. This was termed the morbid adherent placenta (MAP) score with 0 as unfavourable and 1 as favourable. The MAP score was also given by the two radiologists according to the calculated PAI values for each patient.
Statistical analysis
The clinical and sonographic data for all cases were charted in Microsoft Excel 2010 (Microsoft Corp., Redmond, WA, USA). All statistical analysis was done using SPSS Statistics software for Macintosh, (Version 24.0. Armonk, NY: IBM Corp.) Sensitivity, specificity and predictive values were calculated using cross-table analysis. Reliability analysis was done by measuring interrater agreement. Cohen’s kappa was used for ordinal variables (placental lacunar grading and MAP score) while intraclass coefficient (ICC) was used for the scale variables (PAI value). The level of statistical significance was determined at p <0.05.
Results
The age range of the cohort was 22 to 33 years with mean age of 27 years. Mean gestational age at delivery (n = 45) was 35.2 weeks (Table 2). In total, 14 patients had placenta accreta and increta based on the operative and histopathological findings. One patient had percreta with invasion of urinary bladder, thus making a total of 15 cases of adherent placenta (Figure 2). Out of the 15 cases, 11 patients had a history of two or more previous Caesarean sections. The remaining four had a history of one previous Caesarean section. Two cases among those 15 also had history of other surgeries like curettage and myomectomy. Figure 3 illustrates a case of anterior placenta previa with low PAI and MAP score indicating low suspicion for placental invasion.
Table 2.
Distribution of demographic and sonographic variables among the cohort (N = 45) and in cases of proven placenta accreta (N = 15).
| Variables | Number of patients (N = 45) |
|---|---|
| Mean age of patients | 27 years |
| Mean gestational age at delivery | 35.2 weeks |
| Number of cases of placenta accreta/increta | 14 |
| Number of cases of placenta percreta | 1 |
| Other surgeries (myomectomy or curettage) | 2 |
| Previous history of one Caesarean section | 4 (N = 15) |
| Previous history of two Caesarean sections | 9 (N = 15) |
| Previous history of more than three Caesarean sections | 2 (N = 15) |
Figure 2.
(a) US image of the case of placenta percreta (MAP score >5) showing complete placenta previa with grade 3 placental lacunae (multiple and throughout the placental substance), severe myometrial thinning (yellow arrow) and loss of retroplacental zone. Multiple bridging vessels (small white arrows) showing loss of interface with urinary bladder. (b). Gross specimen of the uterus (fundus shown by black arrow) with placental tissue (white solid arrow) completely invading the anterior lower uterine wall confirming placenta accreta.
Figure 3.
(a) US image of the case of anterior marginal placenta previa with maintained utero-placental interface, with no placental lacunae. Myometrial thickness was uniform (yellow arrow). (b) Colour Doppler image at the same level showing retroplacental flow and a few bridging vessels. MAP score was <5.
Hysterectomy was performed in 10 out of 15 cases and there was no maternal mortality. Bladder injury was seen in the single case of percreta. Table 3 shows the breakdown of scoring results of the two radiologists in all 15 cases of adherent placenta.
Radiologist 1 suggested probability of placenta accreta in 17 out of 45 patients resulting in sensitivity of 93.3%, specificity of 90% and higher negative predictive value of 96.4%. Accreta in 14 out of 45 cases was predicted by Radiologist 2 with resultant sensitivity of 86.6%, specificity of 96.6% and higher positive predictive value of 92.8% (Table 4).
Table 3.
Tabulated form of the scoring results of both radiologists in proven cases of morbidly adherent placenta (N = 15).
| Radiologist 1 |
Radiologist 2 |
|||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| S. no | CDS | PLS | MTS | PP | BV | PAI | MAP | CDS | PLS | MTS | PP | BV | PAI | MAP |
| 1 | 3.0 | 3.5 | 1.0 | 1.0 | 1 | 9.5 | 1 | 3.0 | 3.5 | 1.0 | 1.0 | 1.0 | 9.5 | 1 |
| 2 | 3.0 | 3.5 | 0.5 | 1.0 | 1 | 9.0 | 1 | 3.0 | 3.5 | 0.25 | 1.0 | 1.0 | 8.75 | 1 |
| 3 | 0 | 1.0 | 1.0 | 1.0 | 0 | 3 | 0 | 0 | 3.5 | 1.0 | 1.0 | 0 | 5.5 | 1 |
| 4 | 3.0 | 1.0 | 0 | 1.0 | 0 | 5 | 1 | 3.0 | 3.5 | 0 | 1.0 | 0 | 7.5 | 1 |
| 5 | 3.0 | 1.0 | 1.0 | 1.0 | 1 | 7 | 1 | 3.0 | 1.0 | 0.5 | 1.0 | 1.0 | 7.5 | 1 |
| 6 | 3.0 | 1.0 | 0.5 | 1.0 | 0 | 5.5 | 1 | 3.0 | 1.0 | 1.0 | 1.0 | 1.0 | 7 | 1 |
| 7 | 3.0 | 3.5 | 1.0 | 1.0 | 1 | 9.5 | 1 | 3.0 | 3.5 | 1.0 | 1.0 | 1.0 | 9.5 | 1 |
| 8 | 0 | 3.5 | 1.0 | 1.0 | 1 | 6.5 | 1 | 0 | 3.5 | 1.0 | 1.0 | 1.0 | 6.5 | 1 |
| 9 | 3.0 | 0 | 1.0 | 1.0 | 0 | 5 | 1 | 3.0 | 0 | 0.25 | 1.0 | 0 | 4.25 | 0 |
| 10 | 0 | 3.5 | 0.5 | 1.0 | 1 | 6 | 1 | 0 | 3.5 | 0.5 | 1.0 | 1.0 | 6 | 1 |
| 11 | 3.0 | 1.0 | 1.0 | 1.0 | 1 | 7 | 1 | 3.0 | 1.0 | 1.0 | 1.0 | 1.0 | 7 | 1 |
| 12 | 3.0 | 1.0 | 0.5 | 1.0 | 0 | 5.5 | 1 | 3.0 | 1.0 | 0.5 | 1.0 | 0 | 5.5 | 1 |
| 13 | 3.0 | 3.5 | 0.5 | 1.0 | 1 | 9 | 1 | 3.0 | 3.5 | 0.5 | 1.0 | 1.0 | 9 | 1 |
| 14 | 0 | 3.5 | 0.5 | 1.0 | 1 | 6 | 1 | 0 | 1.0 | 0.5 | 1.0 | 1.0 | 3.5 | 0 |
| 15 | 3.0 | 0 | 1.0 | 1.0 | 1 | 6 | 1 | 3.0 | 0 | 1.0 | 1.0 | 1.0 | 6 | 1 |
CDS: Caesarean delivery scoring; PLS: placental lacunae scoring; MTS: myometrial thickness scoring; PP: anterior placenta previa; BV: bridging vessels; PAI: placenta accreta index; MAP: morbid adherent placenta score.
Interrater agreement in the form of reliability indices (κ-value and ICC) is shown in Table 5, which highlights that MAP had a moderate (κ = 0.746) degree of agreement and PAI had perfect (ICC= 0.959) agreement among both radiologists. Lower levels of agreement are noted in assessment of placental lacunar grade and scoring.
Table 4.
Measures of accuracy by two radiologists among delivery and histologically proven cases of placenta accreta (N = 15) and normal placenta.30
| Placenta accreta | Sensitivity (%) | Specificity (%) | PPV (%) | NPV (%) | |
|---|---|---|---|---|---|
| Radiologist 1 | 17 | 93.3 | 90 | 82.3 | 96.4 |
| Radiologist 2 | 14 | 86.6 | 96.6 | 92.8 | 93.5 |
PPV: positive predictive value; NPV: negative predictive value.
Discussion
Risk assessment of morbidly adherent placenta is a major challenge in modern day obstetrics with a progressive increase in the number of Caesarean sections being performed. Advancements in diagnostic modalities like application of colour Doppler, improved resolution, improved transducer technology and 3D imaging have enhanced the capability of practitioners to detect adherent placenta. A detailed knowledge of the US features of morbidly adherent placenta and its associated risk factors is critically important for the imaging specialists to avoid life-threatening haemorrhage and maternal mortality. An easy and reproducible diagnostic tool is required, which may be used as a standard criterion to stratify the probability of placental invasion.
The primary findings of this study are, firstly, that the PAI can be used as a sensitive and specific marker for prediction of probability of invasive placenta. Secondly, this criterion shows a high degree of reliability and consistency in its calculation. Thirdly, a crude estimate of probability of placental invasion (high or low) can be derived from the PAI value, better termed the MAP score. This may be useful to convey the US results to the referring obstetrician for decision making and appropriate treatment planning.
The criteria used in calculation of PAI shows that two of the variables i.e. previous two Caesarean sections and anterior placenta previa shows no disparity in assigning the score. However, the other variables like placental lacunae grade, myometrial thickness and bridging vessels are subjective and may vary. Out of these three variables, the grade of placental lacunae shows maximum weightage and scoring, which may change the final scoring. Therefore, interobserver agreement in placental lacunae analysis was also done, which showed a moderate level of agreement. This can be attributed to less disparity in identification of grade 3 placental lacunae, which had the highest invasion score.
Rac et al. found that a PAI score above 5 shows high specificity in the range of 92 to 100% with high positive predictive value (PPV) between 75 and 100. This was similar to the present study, which applied this criterion and found the specificity ranging from 90% to 97% and PPV from 82% to 93%. Similarly, the lower PAI values showed sensitivity in the range of 86% to 93%, which was 72% to 100% in the reference study.
US-based studies for the prediction of placental attachment disorders are summarised in Table 6 with their corresponding assessment methods. These studies have offered different markers for the prediction of invasive placenta, and weighted each of the markers for importance separately and in combination. Systematic review and meta-analysis of 23 different studies was done by D’Antonio et al., which proposed that colour Doppler detection of bridging vessels showed highest sensitivity and specificity in detecting invasive placenta.16 However, the study by Rac et al. had given least weightage to the bridging vessels and maximum to the placental lacunae. A study by Comstock et al.10 also proposed the highest predictive value of placental lacunae in diagnosing placenta accreta. However, they also added the value of turbulent flow velocity of >15 cm/s, which was not included by Rac et al. Smallest myometrial thickness of <1 mm had shown 100% sensitivity by Twickler et al.17 in 2000, which is also given a relatively lower score than grade 3 placental lacunae in calculation of PAI. Hence, we can ascertain that no single parameter is sufficient enough to accurately predict the adherent placenta and therefore a multiparametric index or score is advantageous. The PAI shows a clear-cut gradient in the relative importance of the markers starting from myometrial thickness (lowest score) to the number of Caesarean sections and grading of placental lacunae (highest score). A previous study involving 314 cases of placenta previa suggested that the presence of any of two US features of placental adhesion are diagnostic for placental attachment disorders (two-criteria system).18
Table 5.
Interrater agreement among two radiologists for the defined parameters.
| Parameters | Reliability index (95% CI) | Level of agreement |
|---|---|---|
| Grade of placental lacunae (0–3) | κ-value = 0.341 | Slight |
| Score of placental lacunae (0, 1, 3.5) | ICC = 0.763 (0.558–0.872) | Moderate |
| MAP score (0, 1) | κ-value = 0.746 | Moderate |
| Placenta accreta index (0–9) | ICC = 0.959 (0.924–0.978) | Perfect |
κ-value: Cohen’s kappa; ICC: intraclass correlation coefficient; CI: confidence interval.
Table 6.
Previous studies on placental attachment disorders with methods employed and their applications.
| Previous studies | Sample size | Assessment method | Study purpose |
|---|---|---|---|
| Twickler et al.17 | 215 | Colour flow mapping and smallest myometrial thickness (<1) | Colour Doppler in placental myometrial invasion |
| D’Antonio et al.16 | Meta-analysis of 23 studies | Colour Doppler showing bridging vessels | Role of US in invasive placentation. |
| Shih et al.14 | 170 | 3D power Doppler | Placenta accreta |
| Comstock et al.10 | 2002 | Lacunae with turbulent flow (velocity >15 cm/s) | Placental attachment disorders |
| Cali et al.7 | 187 | Hypervascularity of uterine–bladder interface | Placenta accreta versus percreta |
| Rac et al.8 | 184 | Placenta accreta index (PAI) | Morbid adherent placenta |
| Pilloni et al.18 | 314 | Two-criteria system | Placental attachment disorders |
Our study also recommends the use of a simplified MAP score, which is derived from the proven PAI. It gives scores of 0 or 1 for unfavourable (<5) and favourable (≥5) PAI values, respectively. The reference study by Rac et al. gives a large probability table of placental invasion with sensitivity and specificity for each of the PAI value, which may range from 5% to 96% and, in practical terms, it is cumbersome to follow since both the radiologist and the obstetrician needs an answer in terms of yes or no. Therefore, the MAP score may be applied as a simple binary variable for indicating the chances of morbidly adherent placenta.
The main limitation of this study is its small sample size, which leads to fewer cases of morbidly adherent placenta. We have included only the high-risk cases and therefore our results may not be generalisable to a low risk population. A primigravida with US and MRI features of morbidly adherent placenta was found during the study period; however, she was excluded according to the study criteria. Another limitation is the use of only a transabdominal transducer, which is inferior to a transvaginal one because of the proximity of the low-lying placenta in the third trimester. However, transabdominal assessment may sometimes be beneficial over the endocavitary approach, which could be unacceptable to a number of women and could lead to bleeding or infection.19,20 Magnetic resonance imaging (MRI) was not included in the study as it was not available for all the patients due to cost constraints. A few recent studies have compared the role of US and MRI in placental attachment disorders.21–23 Future studies with a larger sample size and use of multimodality imaging like US and MRI should be done to enhance the probability and highlight any new markers of placental invasion.
This is a stand-alone study where we have tested the accuracy as well as the reliability of PAI and also recommended a PAI-derived binary marker (MAP score) for the ease of communication of results.
Conclusion
The PAI can be employed as a standard US-based method for assessing the probability of morbidly adherent placenta due to its easy, cost effective and objective methodology. The probability of placental invasion should be evaluated in all high-risk cases and scoring should be given to stratify the risk. Widespread awareness and uniform application of this index will be helpful to convey the risk of abnormal placentation to the referring obstetrician and for planning appropriate multidisciplinary management.
Footnotes
Contributors: SA, AA and SC researched literature and conceived the study. AA and SA designed the audit. AA, SC and SA were involved in protocol development. SA and AA helped in patient recruitment and data analysis. AA wrote the first draft of the article. SA and AA wrote the final version of the article. All authors reviewed and approved the final version of the article.
Declaration of patient consent: The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
Declaration of Conflicting Interests: The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.
Ethics approval: The Institute Ethical Committee (IEC) of Teerthanker Mahaveer Medical College & Research Centre (TMMC&RC), Moradabad, India and institutional review board approved this study.
Guarantor: AA.
ORCID iD: Arjit Agarwal https://orcid.org/0000-0002-2518-6767
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