Research
HJOG 2025, 24 (1), 31-41| doi: 10.33574/hjog.0582
Amr Helmy Yehia, Safaa Elhoussiny Mahmoud Mansour, Nashwa Elsaeed Hassan, Nermeen Ahmed Mostafa El Ghareeb
Department Obstetrics & Gynecology Department, Faculty of Medicine, Ain Shams University, Cairo, Egypt
Correspondence: Safaa Elhoussiny Mahmoud Mansour, Abbassia street, E-mail: safaamansour111990@gmail.com, Phone: 00201117008042, Cairo, Egypt
Abstract
Background: The term morbidly adherent placenta denotes an abnormal implantation of the placenta within the uterine wall and has been implemented to describe placenta accreta, increta, and percreta.
Aim of the Work: To evaluate the accuracy of ultrasound imaging in the prenatal diagnosis of placenta accreta.
Patients and Methods: After ethical committee approval and informed consent from the patients, this cross-sectional study was conducted at Ain Shams University Maternity Hospital from March 2022 to January 2023 and performed on 40 women who underwent cesarean section for placenta previa.
Results: As regards the intraoperative findings, our study results revealed that difficulty in placental separation was detected in (80.0%), Placental bed sutures were performed in (62.5%)-partial removal of the placental bed (20.0%). Tubal ligation was performed in 15.0%, Uterine artery ligation in 100.0%, Internal iliac ligation in 5.0%, Bladder injury in 10.0%; Emergency hysterectomy was performed in 27.5%, and Blood transfusion (57.5%).
Conclusion: Prenatal ultrasound is the best screening tool for a morbidly adherent placenta, and the present simple ultrasound parameters may be highly predictive of such a placenta, allowing for adequate antenatal risk assessment. It is helpful for patient counseling and delivery planning with a multidisciplinary team approach, all of which may ultimately improve pregnancy outcomes in women at risk of a morbidly adherent placenta.
Keywords: Ultrasound, placenta accrete, adherent placenta
Introduction
Placenta accreta occurs when the placental villi attach directly to the myometrium. Different types of placenta accreta include total placenta accreta, partial placenta accrete, or focal placenta accreta, and they are categorized based on the extent of placental tissue involved in their attachment to the myometrium. Approximately 75% of morbidly adherent placentas are placenta accreta, 18% are placenta increta, and 7% are placenta percreta1.
The morbidly adherent placenta has become more common in recent years. In 1977, the average occurrence was estimated to be 1 in 7000 pregnancies, but there was a wide range from 1 in 540 to none in 70,000 deliveries observed by different researchers. In 2004, the occurrence in France was 1.03 in 1000 over 10 years; in the United States, it was 8.3 in 10,000 deliveries over 12 years. The occurrence increased from 5.4 in 10,000 deliveries in the first six years to 11.9 in 10,000 deliveries in the most recent six years2.
The increase in the incidence of placenta accreta is anticipated to be due to the rising cesarean delivery rates, as a previous cesarean section is a major contributor to the morbidly adherent placenta. History of previous uterine surgery such as myomectomy, curettage, and cesarean section has been associated with abnormal processes of placentation. Even more concerning is the high likelihood of placenta previa being associated with placenta accreta 3.
Ultrasound tools and indicators used to diagnose placenta accreta may be noticeable as early as the first trimester of pregnancy. These characteristics include low-site uterine implantation of the gestational sac, multiple vascular spaces within the placental tissue, lack of the usual hypoechoic retroplacental region, and irregularities of the uterine serosal-bladder interface, among others4-5.
Sonograms are highly sensitive and specific for identifying placenta accreta, and MRI is typically used only in uncommon instances when sonograms do not provide a definitive diagnosis. The best time for scheduled delivery for a patient with placenta accreta is around 34–35 weeks into the pregnancy after receiving corticosteroid injections to improve fetal lung development6-7.
Managing placenta accrete effectively requires a multidisciplinary care approach. Effective management relies on prenatal diagnosis, particularly for this group of patients, and coordinating the appropriate surgical intervention interdisciplinary by ensuring that the most experienced team is available for these cases8-9.
Patients and methods
After ethical committee approval and informed consent from the patients, this cross-sectional study was conducted at Ain Shams University Maternity Hospital from March 2022 to January 2023 and performed on 40 women who underwent cesarean section for placenta previa.
Inclusion criteria: Pregnant women from 34 gestational weeks with placenta previa anterior with previous cesarean section or myomectomy, with at least one sign of invasion.
Exclusion criteria: Primagravida and non-scared uterus.
Study procedure:
A detailed history focusing on present and past & obstetrics history was obtained.
Routine general and abdominal examinations
All cases were subjected to sonographic (abdominal and transvaginal Doppler) studies on a placenta bed. All research study subjects followed up at the perinatology unit, and the delivery timing was individualized for each case. Diagnosis of placenta accreta was confirmed at the time of surgery by documentation of abnormal adherence of placenta or evidence of gross placental invasion and then again on pathology if a hysterectomy was conducted.
The sonographic examination involved standard fetal biometry, anomaly scan, placental localization, and morphology. The sonographic findings considered as criteria of placenta accreta (according to RCOG guidelines) were:
- Ultrasound imaging signs:
2D Greyscale signs, Loss of the ‘clear zone,’ Abnormal placental lacunae, Bladder wall interruption, Myometrial thinning, Placental bulge, and Focal exophytic mass
- 2D color Doppler signs:
Uterovesical hypervascularity, Sub-placental hypervascularity, Bridging vessels, and Placental lacunae feeder vessels
- 3D color Doppler signs:
Intra-placental hypervascularity (power Doppler).
Ultrasound was done by ultrasound machines (Samsung UGEO H60) using the curvilinear transducer (at frequency 2-6MHz) or transvaginal transducer (at frequency 2-6MHz). The lower uterine segment was evaluated using the highest–frequency transducer that can produce an adequate image, often the 5-MHz transducer. Transabdominal imaging was performed with the patient’s bladder full. The transvaginal US was always performed when the placenta was low-lying, or previa was present.
A lecturer or assistant lecturer on duty conducted a cesarean section.
All the cases correlated to intraoperative findings, and the morbidly adherent placenta was diagnosed intraoperatively by FIGO classification for the clinical diagnosis of placenta accreta spectrum disorders:
Grade 1: Abnormally adherent placenta (placenta adherent or accreta) – attached directly to the surface of the middle layer of the uterine wall (myometrium) without invading it
Grade 2: Abnormally invasive placenta (increta) – invasion into the myometrium
Grade 3: Abnormally invasive placenta (percreta) invasion may reach surrounding pelvic tissues, vessels, and organs.
Outcomes:
Primary Outcomes: Detect the accuracy of different ultrasound criteria in predicting placenta accrete and the sensitivity and specificity of each.
Secondary outcomes: The intraoperative findings of operative procedures, including difficulty in placental separation, placental bed sutures, partial removal of placental bed, uterine artery ligation
Internal iliac ligation, Bladder injury, Emergency hysterectomy, and Blood transfusion
Statistical analysis:
The collected data was coded, tabulated, and statistically analyzed using IBM SPSS statistics (Statistical Package for Social Sciences) software version 22.0, IBM Corp., Chicago, USA, 2013, and Microsoft Office Excel 2007. Descriptive statistics were done as minimum and maximum of the range and mean ± SD (standard deviation) for quantitative normally distributed data. In contrast, they were done for qualitative data as numbers and percentages.
Inferential analyses were done for quantitative variables using the Shapiro-Wilk test for normality testing and independent t-test in cases of two independent groups with normally distributed data. In qualitative data, inferential analyses for independent variables were done using the Chi-square test for differences between proportions, Fisher’s Exact test, and the Mann-Whitney test for variables with small expected numbers. The significance level taken at P value < 0.050 is significant; it is non-significant.
Diagnostic characteristics were calculated as follows:
– Sensitivity = (True positive test / Total positive golden) x 100
– Specificity = (True negative test / Total negative golden) x 100
– Diagnostic accuracy = ([True positive test + True negative test] / Total cases) x 100
– Youden’s index = sensitivity + specificity – 1
– Predictive positive value = (True positive test / Total positive test) x 100
– Predictive negative value = (True negative test / Total negative test) x 100
– LR+ = (sensitivity/ 1-specificity)
– LR- = (1- sensitivity/specificity)
– LR= LR+/ LR-
Kappa=Observed agreement–chance agreement / 1–chance agreement.
Results
The average age was 30.5 years with a standard deviation of 6.9, and the gestational age was 35.6 weeks with a standard deviation of 1.1. The median (1st−3rd interquartile range) for parity was 6.0 (1.0–7.0), and for previous cesarean sections, it was 5.0 (1.0–6.0) [Data not tabulated]
Table 1 demonstrates the ultrasound findings among the study participants. The final suggestions were invasion (77.5%), focal invasion (7.5%), and no invasion (15.0%).
In our study, we tried placental separation, which was difficult in 32 patients (80.0%). Placental bed sutures were performed in 25 patients (62.5%).
We partially removed the placental bed in patients with adherent placenta and then sutured the uterine wall in 20.0% of cases (8 patients).
In our protocol of uterine preservation, we perform uterine artery ligation in all patients. Unlike other protocols, we do not perform prophylactic Internal iliac artery ligation (in our study, we performed it in only 2 cases (5.0%).
Regarding the complications, bladder injury occurred in only 4 cases (10.0%), reflecting our surgeons’ higher surgical talent. Hysterectomy was performed in only 11 patients (27.5% of the cases), and 57.5% of cases received blood transfusion. (23 cases).
The histopathology findings of the cases that underwent hysterectomy. Of these, 72.7% were diagnosed with increta (8 cases) and 27.3% with accreta (3 cases).
The conservative management of placenta accreta begins with the trial of placental separation, which was difficult in 32 cases. Table 2 indicates that in cases with difficulty in placental separation, the following were statistically more common: Previous section number, Loss of clear zone, Abnormal placental lacunae, Bladder wall interruption-Myometrial thinning, Placental bulge, Uterovesical hypervascularity, bridging vessels-Placental lacunae feeder vessels, Intra-placental hypervascularity, and final suggestion Invasion.To predict cases with difficult lacental separation, our analysis showed that Bladder wall interruption, Uterovesical hypervascularity, and Bridging vessels had high diagnostic characteristics in predicting Difficulty in placental separation. The final diagnostic suggestion demonstrated higher accuracy Table 3
After the placenta is removed, suturing the placental beds and uterine arteries ligation is the critical step that determines the stoppage of bleeding or progression to internal iliac arteries ligation or hysterectomy. There were no significant differences according to Placental bed sutures regarding demographic and ultrasound findings except for the previous cesarean section (p value= 0.007). [data not tabulated].
Our results showed no significant differences regarding demographic and ultrasound findings according to partial removal of the placental bed except for Placental lacunae feeder vessels, which were significantly more frequent in cases with Partial removal of the placental bed (P=0.037) [Table 4]. We found that the diagnostic characteristics of the final suggestion in predicting were good in excluding the need for partial removal of the placental bed but poor in confirming it [Table 5].
Discussion
Antenatal diagnosis of MAP and a multidisciplinary team approach to care have the potential to reduce maternal and fetal intrapartum complications, including maternal blood loss, requirement for transfusion, hysterectomy, intraoperative urological and gastrointestinal injuries, and even maternal death10.
With grayscale and color Doppler imaging, ultrasound evaluation is the recommended first-line modality for diagnosing MAP11. Assessing sonographic parameters for predicting placenta accreta syndrome and correlating ultrasound assessment with operative judgment and histopathology in hysterectomy cases is of major interest due to potential intraoperative complications12.
Our results and their interpretation
During this study, 53 patients were assessed for eligibility, and 40 were included. Nine eligible patients were excluded from the analysis based on the inclusion criteria, and four refused to participate.
As regards the Ultrasound findings, the current study revealed that the Final suggestion by ultrasound examination was invasion (77.5%), focal invasion (7.5%), and no invasion (15.0%).
Our center performs 18,000 deliveries per year and is considered a tertiary center for receiving all cases of placenta accreta from different hospitals. We do not rush for a hysterectomy unless the patient’s age is above forty and has completed her family. We tried placental separation in our study, and results revealed that difficulty in placental separation was detected in (80.0%). Placental bed sutures were performed in 62.5% of cases.
We partially removed the placental bed in patients with adherent placenta and then sutured the uterine wall in 20.0% of cases.
In our protocol of uterine preservation, we perform uterine artery ligation in all patients. Unlike other protocols, we do not perform prophylactic Internal iliac artery ligation (in our study, we performed it in only 5.0% of the cases).
Regarding the complications, bladder injury occurred in only 10.0% of the cases, reflecting our surgeons’ higher surgical talent. Hysterectomy was performed in only 11 patients (27.5% of the cases), and 57.5% of cases received blood transfusion.
As regards the histopathology findings of hysterectomized cases, our study results revealed that placenta increta was detected in 72.7 % (8/11) and placenta accreta in 27.3% (3/11) with no placenta percreta detected in the histopathology.
As regards the difficulty in placental separation, our study results revealed that Previous section number and the presence of ultrasound findings of loss of clear zone, abnormal placental lacunae, bladder wall interruption-myometrial thinning, placental bulge, uterovesical hypervascularity, bridging vessels-placental lacunae feeder vessels, intra-placental hypervascularity and the final suggestion of invasion were statistically associated with difficulty in placental separation and adherent placenta.
Consequently, the ultrasound parameters for predicting difficult placental separation were abnormal placental lacunae (Sensitivity 93.8% and PPV 93.8%), bladder wall interruption (Sensitivity 84.4% and PPV 96.4%), Myometrial thinning (Sensitivity 93.8%), Uterovesical hypervascularity (Sensitivity 87.5% and PPV 96.6%) and Bridging vessels had high diagnostic characteristics in predicting Difficulty in placental separation and the final diagnostic suggestion demonstrated higher accuracy.
Also, the results revealed that the placental bed sutures and bladder injury were significantly higher in women with an increased number of previous cesarean sections (p value= 0.007, 0.002), respectively.
Comparison of our results with similar studies
Moneim et al13 studied 50 pregnant women at 28 weeks gestation with suspected morbidly adherent placenta (MAP). They used 2D trans-abdominal gray-scale ultrasound to confirm placenta location and identify MAP. 56% experienced challenging placental separation, leading to significant blood loss. The best ultrasound parameters for detecting challenging placental separation and blood loss were abnormal placental lacunae and an exophytic mass invading the bladder. These parameters also helped identify cases requiring emergency hysterectomy.
Our results are inconsistent with those of Tikkanen et al14 who conducted a retrospective case-control study that enrolled 24 women with placenta accreta, they found that the risk factors of placenta accreta include parity, cesarean section, and placenta previa.
In a study by Aboshalk et al15 on 50 pregnant women, 3D ultrasound imaging and Doppler studies were used to diagnose morbidly adherent placenta. They found that 54% of the women had morbidly adherent placenta, with varying classifications. The study also evaluated the accuracy and sensitivity of different ultrasound and Doppler findings15.
Our findings concord with the previous study of Ardakani et al16, who examined 50 pregnant female patients diagnosed with placenta previa. They found various indicators such as obliteration of the retroplacental hypoechoic area, placental lacunae, myometrial thinning, interruption of the bladder-uterine interface, vascular gap, vascularity, and bridging vessel. The tomographic ultrasound image successfully predicted the presence of placenta previa with high sensitivity and accuracy.
Our findings agree with Eid et al12 who conducted a prospective cohort study. In a study of 60 patients with placenta previa and suspected placenta accreta. Among the ultrasound parameters, abnormal lacunae showed the highest accuracy in predicting placenta accreta.
Our results support the findings of a prior study conducted by Darwish et al 17. They examined 150 patients of placenta previa, proposed a scoring system for placenta accreta, and demonstrated its potential in predicting placenta accreta.
Our findings align with a previous study by Firmansha Dilmy et al 18, which included 34 clinically diagnosed women with placenta accreta spectrum (PAS). Three main vascular indices were analyzed in placental vasculature: the vascularization index (VI), the Flow index (FI), and the Vascularization Flow index (VFI). Their results revealed that VI and VFI values were significantly higher in the MAP group than in normal pregnancy, with almost similar FI values. These data may support the fact that VI and VFI could be good placental vasculature markers for predicting the presence of PAS.
In a study by Warshak et al, prenatal diagnosis and delivery planning significantly affected outcomes for patients with placenta accreta. The average gestational age at delivery was 34.7 weeks, and 75% of patients required transfusions (an average of 5.4 units of packed red blood cells). A quarter of the patients experienced major surgical complications, including bladder, ureteral, and bowel injuries. The study concluded that antenatal detection of placenta accreta significantly predicted maternal hemorrhage (p value=0.02). The predelivery diagnosis was made after observing suspicious characteristics on ultrasonography in women with risk factors19.
Our findings support a previous study by Tovbin et al20, which revealed that specific ultrasound features such as Cesarean deliveries, lacunae, and uteroplacental demarcation can predict morbidly adherent placenta, leading to specific antenatal and intrapartum management.
In agreement with our findings, previous studies reported that risk factors of abnormally invasive placentation were placenta previa and previous cesarean delivery, which were the primary cause associated with difficult placental removal and blood transfusion21-22. Other studies found that the presence of placental lacunae in the 3rd-trimester ultrasound is a highly reliable sign for diagnosing accreta in women with prior cesarean delivery, with a 93% sensitivity and positive predictive value. Similarly, abnormal lacunae alone had a 96-100% predictive power for PAS23-24.
The strength points of this study:
The strengths of this study are its cross-sectional design and the absence of patients lost to follow-up during the study period. In addition, the study presents an effective method for enabling the preoperative preparation of women with MAP who are at risk of major maternal complications. Moreover, the study was performed at a single institution with the same surgical team and the same anesthetic protocol, which likely increased the validity of our results.
The limitations of the study:
The findings of this study should be interpreted in light of its limitations. Firstly, the main one was that the surgical team was not blinded to the ultrasound findings, and the surgeons diagnosed MAP during surgery in all cases in which hysterectomy was avoided. Secondly, including a relatively smaller sample size relative to the previous studies, not being a multicentric study, represents a significant risk of publication bias. Thirdly, since our study was not a comparative study, we could not show the superiority of our diagnosis protocol compared with that of others. Fourthly, since our investigations comprised a single institutional study, it is unclear whether similar outcomes would be obtained in other tertiary facilities using the same diagnosis protocol.
Clinical implications of the study: Several ultrasound parameters should be used to expect difficult placental separation in cases where the decision is to do conservative management, and this allows the involvement of a highly skilled surgical team who can perform uterine-sparing surgeries such as partial removal of placental bed and bilateral internal iliac arteries ligation aiming to avoid hysterectomy in patients who did not complete their family.
Conclusion
The best ultrasound parameters for detecting difficult placental separation and placental invasion with high sensitivity in studied cases were Abnormal placental lacunae, Bladder wall interruption, Myometrial thinning, Uterovesical hypervascularity, and Bridging vessels.
Funding
This research received no external funding.
Disclosure of Interest
The authors declare no conflict of interest.
Ethics Approval and Informed Consent to Participate
Following local regulations, the protocol gained Ethical and research approval from the Faculty of Medicine Ain Shams University Research Ethical Committee. We confirm that all methods were performed according to the relevant guidelines and regulations according to the Declaration of Helsinki.
Data Sharing
The datasets used and analyzed during the current study are available from the corresponding author upon reasonable request.
Acknowledgments
Not applicable.
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