The MRI estimations of cervical length and cervical volume correlate with massive hemorrhage in patients with placenta accreta spectrum disorders

doi:10.21203/rs.3.rs-4659075/v1

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Research Article

The MRI estimations of cervical length and cervical volume correlate with massive hemorrhage in patients with placenta accreta spectrum disorders

https://doi.org/10.21203/rs.3.rs-4659075/v1

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Objective

The purpose of this study is to evaluate the capacity of two MRI parameters to predict massive hemorrhage in pregnancies with placenta accreta spectrum disorders.

Methods and materials:

This case-control study evaluated 174 patients who underwent MRI for placental assessment. MRI images were reviewed by two experienced radiologists blinded to all clinical data. Multivariate logistic regression was performed to analyze the risk factors for patients with massive hemorrhage. The area under the curve were used to compare the predictive ability between cervical length and cervical volume.

Results

Patients with massive hemorrhage exhibited smaller neonatal birthweight (P < 0.001), longer operation time (P < 0.001), and more blood loss (P < 0.001). The percentage of ICU admission and hysterectomy were both significantly higher than patients without massive hemorrhage. The area under the curve of cervical length and cervical volume in predicting MH were 0.812 and 0.845, respectively. And the area under the curve increased to 0.906 by the two combined parameters.

Conclusion

Shorter cervical length and smaller cervical volume are associated with massive hemorrhage during cesarean section. These methods can be utilized to better predict massive hemorrhage in placenta accreta spectrum disorders.

Complete placenta previa

Magnetic resonance imaging

Massive hemorrhage

Placenta accreta spectrum

The placenta accreta spectrum (PAS) disorders were mainly attributed to the failure of normal decidualization and the placental chorionic villi penetrating into the muscular layer, serosa layer and even adjacent tissues and organs. This serious maternal complication was classified into three types according to the depth: placenta increta, placenta percreta, and placenta accreta ^{1, 2}. The most common risk factors were previous cesarean delivery and placental previa³. The remarkable incidence of PAS was owing to the increasing rate of cesarean section, affecting about 0.01–1.1% pregnancies⁴. Unpredictable life-threatening hemorrhage was a major cause of maternal morbidity and mortality⁵. Nevertheless, there was a paucity of validated prediction model for intraoperative hemorrhage.

Several observational studies focused on the relationship between cervical length and hemorrhage in PAS^{6, 7}. Shortening of the cervix limited the contraction of lower uterine segment and made it difficult for surgical operation for hemostasis⁸. The three-dimensional multiplanar volume assessment might increase the predictive value of intraoperative hemorrhage.

Ultrasound was the primary modality for diagnosing PAS. However, posterior location of the placenta or thick abdominal fat would contribute to distortion of the diagnosis. MRI provided greater spatial resolution of the entire placenta and accessed the depth of invasion. Numerous researches manifested that MRI was highly specific and sensitive in the diagnosis of PAS⁹. The purpose of this study was to observe the effect of cervical length and cervical volume on postpartum hemorrhage in patients with placenta accreta spectrum disorders by MRI.

Study Population

This study was a case-control design by screening the patients with placenta accreta spectrum disorders from January 2016 to October 2023 and was approved by the Ethics Committee of the Affiliated Suzhou Hospital of Nanjing Medical University (K-2022-015-K01). Considering the anonymous patient data, informed consents were waived by the committee. The research was conducted according to the Declaration of Helsinki.

The inclusion criteria were:1) singleton pregnancy, 2) at least one previous cesarean section, 3) placenta accreta spectrum confirmed by ultrasound and MRI in the third trimester. Patients with incomplete images and antenatal examination information were excluded. All patients had regular prenatal ultrasonic testing and underwent MRI before the C-section. Finally, 174 patients were incorporated into the study (Fig. 1).

Definitions and References of Maternal Complications

Placenta accreta spectrum disorders were stratified into levels by placenta increta, placenta percreta, and placenta accreta, including clinical criteria and histologic criteria¹⁰. This study defined massive hemorrhage (MH) as > 2000ml during 24 hours after cesarean deliveries¹¹. Postpartum blood loss was estimated through volume method and weighing method.

MR Assessment of Cervical Length and Volume

MR imaging was performed in a 3.0T MRI system (Siemens Medical Solutions, Erlangen, Germany) with an identical protocol using pelvic phased-array coil and any intravenous injection were not used. T1 and T2-weighted images in the axial, sagittal, and coronal orientations were obtained. Imaging parameters were a repetition time of 700 msec, an effective echo time of 87 msec, a bandwidth 698 Hz/px, a 432*432 matrix over a field of view of 380*380 mm, and a 5 mm slice thickness. Cervical length was measured between lines a and b in sagittal images. Cervical volume, as measured in millimeters, was calculated with 3D Slicer software (version 5.2.1, available at www.slicer.org) (Fig. 2). All MRI imaging data were analyzed in consensus by 2 experienced radiologists. After identification of the cervical parameters, another radiologist completed volume measurement. Radiologists were blinded to the clinical diagnosis and treatment.

Data Collection and Analysis

The baseline characteristics, including maternal age, body mass index (BMI) and reproductive history were collected. Researchers also recorded the following delivery information: gestational age at delivery, neonatal birth weight, operation time, intraoperative blood loss, blood transfusion, ICU admission, hysterectomy.

All statistical analyses were analyzed by SPSS 23.0 statistics software (SPSS, Inc., Chicago, IL, USA). The graphs were performed using GraphPad Prism 8.0 software. The variables were expressed as mean ± standard deviation or median (interquartile range) according to the distribution of the data. The difference of variables was compared with T test, Mann-Whitney U test, Chi-square test or Fisher exact test. All reported P values were with two tails. The agreement between observers were assessed using Kappa test. A Kappa value of 0.75 signified strong consistency, while a Kappa value between 0.4 and 0.75 indicated moderate consistency. Receiver operating characteristic curve (ROC) was used to evaluate the diagnostic value of different cervical parameters. P < 0.05 was considered to be of statistical significance.

One hundred and seventy-four cases were included in this study. The baseline information of PAS patients was demonstrated in Table 1. 81 of 174 patients were diagnosed of PAS intraoperatively (accreta, n = 33; increta, n = 28; percreta, n = 20). All patients were accepted cesarean section deliveries. No statistically significance could be detected regarding to maternal age, BMI, gravidity, parity, previous cesarean deliveries and the gestational age at MRI examination.

Table 1

Clinical Features of the Study Groups (n/%)
Characteristic	Patients with MH (n = 81)	Patients without MH (n = 93)	Statistic ( t//Z/χ2 )	P value
Maternal age	32.04 ± 4.06	31.20 ± 4.17	1.329	0.185
BMI (kg/m2)	25.85 ± 3.19	25.69 ± 3.89	0.301	0.764
Gravidity	3(2, 4)	3(2, 4)	1.200	0.230
Parity	2(1, 2)	2(1, 2)	0.625	0.532
Number of abortions	1(1, 2)	1(1, 2)	1.331	0.183
Number of previous cesarean delivery	1(1, 2)	1(1, 2)	0.552	0.581
Previous history of placental previa	9 (11.11)	5 (5.38)	1.924	0.165
Gestational age at MRI (weeks)	33.33 ± 2.12	33.60 ± 1.76	0.923	0.358
Prenatal vaginal bleeding	27(33.33)	25(26.88)	0.860	0.354
Gestational age at delivery (weeks)	35.23 ± 1.48	35.95 ± 1.14	3.621	< 0.001
Neonatal birthweight (g)	2415.56 ± 365.99	2723.66 ± 422.18	5.106	< 0.001
Operation time (min)	92.30 ± 26.59	79.51 ± 28.29	3.058	0.003
Intraoperative blood loss (mL)	2377.70 ± 657.17	1214.01 ± 364.06	14.688	< 0.001
Blood transfusion (mL)	1802.10 ± 634.35	751.51 ± 396.05	13.277	< 0.001
ICU admission	17 (20.99)	7 (7.53)	6.597	0.010
Hysterectomy	6 (7.41)	1 (1.08)	4.496	0.034
The type of PAS			14.452	0.001
Accreta	33 (40.74)	56 (60.22)
Increta	28 (34.57)	32 (34.41)
Percreta	20 (24.69)	5 (5.38)

The gestational age at delivery (35.23 ± 1.48 vs 35.95 ± 1.14; P < 0.001) in patients with MH were significantly smaller than those in patients without MH, and neonatal birthweight in the MH group was lower (2415.56 ± 365.99 vs 2723.66 ± 422.18; P < 0.001). Longer operating times (92.30 ± 26.59 vs 79.51 ± 28.29; P = 0.003) and more intraoperative blood loss (2377.70 ± 657.17 vs 1214.01 ± 364.06; P < 0.001) were found in the MH group than in the non-MH group. When considering the adverse clinical outcome, 17 (20.99%) parturient admitted into ICU, 6 (7.41%) underwent emergency hysterectomy and more blood transfusion (1802.10 ± 634.35 vs 751.51 ± 396.05; P < 0.001) due to massive bleeding and unstable vital signs (Table 1).

The identification of cervical length and volume between two radiologists reached almost perfect reliability, with Kappa values over 0.75 (Table 2). Table 3 demonstrated the ORs for evaluation of MH in relation to cervical length and volume. Patients with small cervical volume (< 20.00 cm³) got higher odds ratio for MH (6.384, 95% CI 2.517–9.657, P < 0.001).

Table 2

Interobserver Reliability of Magnetic Resonance Imaging (MRI) in the Measurement of MRI Features
MRI features	Either	Both	Agree	Kappa	Interpretation
Cervical length	93 (53.448)	85 (48.851)	95.402	0.908	Almost perfect
Cervical volume	95 (54.598)	88 (50.575)	95.977	0.919	Almost perfect
Presented here as No. (%). Number (and proportion) of studies in which either radiologist or both radiologists reported a finding. Percentage of studies in which they agreed

Table 3

Multivariate Logistic Regression Analysis of Risk Factors for Patients with MH
Variable	OR (95%CI)	P
Cervical length (cm)		< 0.001
> 3.00	1
< 3.00	3.512 (1.836–6.927)
Cervical volume (cm³)		< 0.001
> 20.00	1
< 20.00	6.384 (2.517–9.657)

The optimum cut-off values for the cervical length (30 mm) and cervical volume (20 cm³) were identified by ROC analysis (Table 4).

Table 4

Receiver Operating Characteristic Analyses for Prediction of Massive Hemorrhage Based on Cervical Length and Cervical Area
Variable	Cut-off	Sensitivity % (95% CI)	Specificity % (95% CI)	PPV %	NVP %	P
Cervical length (mm)	28	81.11 (73.55–87.62)	88.33 (80.58–93.39)	85.82	84.30	< 0.001
Cervical length (mm)	30	86.53 (78.81–90.95)	83.94 (77.23–90.65)	82.43	87.74	< 0.001
Cervical length (mm)	32	83.52 (76.81–88.76)	84.08 (79.27–92.85)	82.04	85.41	< 0.001
Cervical volume (cm³)	18	84.46 (79.25–89.90)	87.21 (81.17–91.92)	85.19	86.56	< 0.001
Cervical volume (cm³)	20	91.53 (83.91–94.06)	83.61 (77.88–89.05)	82.94	84.63	< 0.001
Cervical volume (cm³)	22	88.57 (80.54–91.93)	86.35 (80.90-90.38)	84.96	82.47	< 0.001
PPV, Positive predictive value; NPV, Negative predictive value

Subcolumn graphs showed that statistic significance was found in cervical length and volume between patients with MH and patients without MH (Fig. 3). As illustrated by the scatter diagram (Fig. 4), Cervical length and volume correlated negatively with the amount of intraoperative blood loss. Based on the ROC curve, the sensitivity, specificity, positive predictive value (PPV) and negative predictive value (NPV) of the cervical length less than 30 mm for predicting cases at high risk for MH were 86.53%, 83.94%, 82.43%, 87.74%, with an area under the curve (AUC) of 0.812. The sensitivity, specificity, PPV and NPV were 91.53%, 83.61%, 82.94% and 84.63%, respectively, of the cervical volume less than 20 cm³ for the prediction of MH with AUC 0.845 (Fig. 5). The AUC increased to 0.906, combining cervical length with cervical volume.

It is noteworthy that the prevalence of PAS has increased yearly, with the increasing rate of cesarean deliveries and repeated cesarean deliveries. Elective cesarean delivery is the predominant treatment^{12, 13}. Intraoperative bleeding control is the main difficulty in this operation. Previous researches have indicated that cervical length is negatively associated with MH^{6, 7, 14, 15}. Ultrasonography is the primary method to diagnose PAS and measure the length of cervical and other adverse manifestations. MRI has an advantage in evaluating soft tissue from multiple directions and better delineating the relationship between the uterus and the adjacent organs. We presented this retrospective investigation of correlation between cervical length or cervical volume and MH by MRI in the cases of PAS.

Adverse prenatal outcomes were strongly associated with the depth of the villous tissue invasion. Our results showed that the deeper the myometrial invade, the more complex the operation, and the higher the risk of poor outcome, including intraoperative hemorrhage, hysterectomy, and even maternal death. The results were in line with previous studies^{4, 16}.

Our results showed that both cervical length and cervical volume were negatively associated with massive intraoperative bleeding in PAS. Patients with cervical length less than 3.0mm experienced a 3.51-fold increased risk of MH. Amount of researcher have similar findings. Fusen Huang et al. reported that in patients with PAS combined with placental previa, the risk of hemorrhage decreased to 56% when the cervical length was less than 33mm⁸. Another study indicated that the threshold cervical length related to MH was 25mm¹⁴. Furthermore, we found that patients with cervical length less than 20.0cm³ were associated with a more than 6-fold higher risk of MH.

Several studies have summarized the hypotheses about bleeding and cervix, including uterine inertia, difficult hemostasis by surgical operations, depletion of clotting factors caused by antepartum bleeding and variant blood vessels in patients with PAS ^17–20. Due to the mechanisms related to MH, we proposed a new evaluation method that focused on the three-dimension morphologic change of cervix. As shown on the ROC curve, the cervical volume exhibited better performance with an AUC of 0.85 for predicting MH than the individual cervical length. The combination of cervical length and cervical volume provides higher sensitivity and specificity to identify MH in the operation.

As far as we know, this is the first paper to evaluate the strengths of the relationship between cervical volume and MH and to compare the prediction potency of the two MRI signs. Our results suggest a feasible and promising approach to predict MH on the basis of MRI. Additionally, these findings can facilitate the risk stratification in the preoperative preparation and formulating perioperative treatment of pregnancies with PAS.

ADVANTAGES AND LIMITATIONS

The data are representative and reliable because our department is the largest tertiary maternal care center in local area. Experienced radiologists are blind to the clinical treatment procedure to eliminate the bias. However, this is a retrospective study and further prospective researcher are needed to confirm our findings. Furthermore, we will expand the sample size to validate the conclusions.

Shorter cervical length and smaller cervical volume are associated with MH during cesarean section. Evaluating cervical length and volume by MRI could remind obstetricians to take precautions before the operations.

MRI

Magnetic Resonance Imaging

ICU

Intensive Care Unit

massive hemorrhage

PAS

placenta accreta spectrum

ROC

Receiver Operating Characteristic:BMI:Body Mass Index

Odds Ratio

AUC

Area Under the Curve

PPV

Positive Predictive Value

NPV

Negative Predictive Value

FUNDING

This study was supported by Gusu health talent plan (grant number GSWS2023055).

Author Contribution

Min Yuan and Yongfei Yue performed the literature review, study design, and manuscript writing. Yongfei Yue also supervised the research project. Jun Yan, Ye Song, and Yan Kang performed the data collection. Xinfang Zhou provided statistical analysis and medical consultation. All authors read and approved the final manuscript.

Acknowledgement

We thank the participants and clinical site staff for their contributions to this study.

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No competing interests reported.

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You are reading this latest preprint version

The MRI estimations of cervical length and cervical volume correlate with massive hemorrhage in patients with placenta accreta spectrum disorders

Status:

Version 1

Abstract

Objective

Methods and materials:

Results

Conclusion

Figures

INTRODUCTION

MATERIALS AND METHODS

Study Population

Definitions and References of Maternal Complications

MR Assessment of Cervical Length and Volume

Data Collection and Analysis

RESULTS

DISCUSSION

ADVANTAGES AND LIMITATIONS

CONCLUSION

Abbreviations

Declarations

FUNDING

Author Contribution

Acknowledgement

References

Additional Declarations

Status:

Version 1