Histogram analysis of whole placental T2-weighted magnetic resonance image-derived in patients with Pre-eclampsia

doi:10.21203/rs.3.rs-4814008/v1

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Research Article

Histogram analysis of whole placental T2-weighted magnetic resonance image-derived in patients with Pre-eclampsia

https://doi.org/10.21203/rs.3.rs-4814008/v1

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Background

The placenta plays a pivotal role in the development of pre-eclampsia (PE). The purpose of this retrospective study was to distinguish the patients with PE from normal pregnant women using the whole placental T2-weighted image(T2W) histograms.

Methods

The clinical and prenatal pelvic MRI data of 22 patients with PE and 22 normal pregnant women were retrospectively analyzed. Histogram parameters including mean, variances, skewness, kurtosis, entropy, 10th percentile, 50th percentile, 90th percentile and 99th percentile were calculated from the whole-volume placental of T2W. The volume and thickness were recorded as the morphological parameters. Histological examinations of placenta were conducted following delivery. Student-t test or Mann-Whitney U test was used to compare the continuous data between the two groups. Chi-square test was used to compare the categorical data. The diagnostic efficacy for PE with parameters was analyzed by receiver operating characteristic (ROC).

Results

The difference between the two groups in two histogram parameters (variance and 99th percentile) and one morphological parameter (volume) were statistically significant (P < 0.05). The distinguishing ability of variances, 99th percentile and volume for PE was good, with area under the ROC (AUC) were 0.713, 0.693 and 0.709 respectively.The combined AUC value of the three parameters was higher than that of a single parameter (AUC = 0.899, P = 0.000), with sensitivity of 86.36% and specificity of 77.27%.

Conclusions

The histogram parameters of the whole placenta T2W have good diagnostic efficacy, which provides a novel method for distinguishing the patients with PE from the normal pregnant women.

Pre-eclampsia

T2-weighted image

Histogram

Magnetic resonance imaging

Whole placenta

Pre-eclampsia (PE) is a pathological condition that manifests in pregnant individuals, characterized by the development of hypertension after the 20 weeks of gestation[1]. The prevalence of this ailment varies between 3% and 5% across different nations[2]. PE is often accompanied by various forms of organ impairment, fetal growth restriction, and premature birth, thereby exerting detrimental effects on the well-being and overall quality of life for both the mother and the newborn[3].

Despite the fact that the etiology of PE is not fully comprehended, it has been firmly established that the placenta plays a pivotal role in the development of this disease[2, 4]. Placental oxidative stress and placental ischemia have been recognized as significant factors contributing to the pathogenesis of PE[5]. Presently, the assessment of placental function in vivo can be indirectly conducted through the evaluation of fetal growth and umbilical artery velocity using ultrasound. Moreover, it is becoming increasingly apparent that placental magnetic resonance imaging(MRI) offers valuable insights into both placental structure and function[6].The quantitative identification of the pre-eclamptic placental phenotype can be achieved through the determination of the placental T2* value[7]. However, conventional MRI sequences pose challenges in detecting the pathological changes of the placenta in patients with PE. Therefore, there is still a significant knowledge gap regarding the impact of PE on the placenta using MRI.

Recently, the role of texture features in placental MR images has been confirmed in other placental diseases, such as placenta accreta spectrum[8, 9]. Placenta accreta spectrum is characterized by placental infarction, which can result in local ischemia of the placenta and shares similarities with PE to some extent. The researchers[10] employed artificial intelligence and deep learning mechanisms to analyze placental ultrasound images of hypertensive women, and observed distinct textures compared to a control group with normal blood pressure.Within the field of radiomics, histogram analysis has been extensively utilized to assess medical images, yielding promising outcomes[11]. By examining the inter-relationships and distribution of pixels within the image, histogram analysis offers a quantitative evaluation of placental heterogeneity. Furthermore, it has been established that placentas associated with PE exhibit low-signal intensity, advanced lobularity, and high granularity within lobules on T2-weighted (T2W) imaging, although a quantitative assessment is lacking[7].The investigation of the feasibility of histogram analysis of placental MR images as a potential tool for discriminating PE is of significant interest.

Currently, there is a lack of research on the histogram analysis of placental MR images in women with PE. Consequently, the purpose of this study was to extract histogram features from T2W images in order to identify discernible differences in the placenta that could effectively distinguish patients with PE from normal pregnant women.

Patients

This study employed a prospective approach to define PE in accordance with the internationally agreed-upon definition [2]. Specifically, it encompassed pregnant women who developed gestational hypertension at or after 20 weeks' gestation and exhibited any of the subsequent conditions: proteinuria, acute kidney injury, liver involvement, neurological complications, hematological complications, and utero-placental dysfunction.

The investigation was conducted retrospectively at the Third Affiliated Hospital, Guangzhou Medical University in China, with a sample size of 22 patients diagnosed with PE within the period spanning from January 2018 to December 2022. The inclusion criteria for this study are as follows: (1) a clinical diagnosis of PE made by a senior obstetrician in accordance with established diagnostic criteria and classification of hypertensive disorders during pregnancy; (2) a singleton pregnancy; (3) absence of any evident malformation or chromosome abnormality detected during routine prenatal screening examinations; (4) performance of placental MRI during the second or third trimester of pregnancy; (5) absence of claustrophobia and contraindications for MRI. The exclusion criteria include: (1) a history of adverse pregnancy outcomes; (2) a history of hypertension and immune diseases prior to pregnancy,, as well as gestational diabetes mellitus; (3) congenital diseases such as congenital heart disease; (4) obvious image artifact. Additionally, a control group consisting of 22 pregnant individuals, comparable in terms of age and gestational age at the time of MRI examination, was incorporated. Following childbirth, data regarding the gestational week, birth weight, and Apgar score at 1 minute, 5 minutes, and 10 minutes were recorded for all newborns. Furthermore, each participant provided informed consent after being briefed on the study's objectives by the hospital's ethics committee.

MR Assessment

All participants underwent scanning using a 3.0 T MRI unit (Achieva; Philips Medical Systems, Best, Netherlands) and an 8-channel Sense-XL-Torso phased array surface coil. The patient was positioned in a supine or left-sided position, with the bladder maintained at a semi-filled state. The scanning range extended from the pubic symphysis to the uterine fundus. A scanning protocol optimized for pregnant women was employed, with a duration of less than 20 minutes.

Only T2-weighted sequences were utilized for imaging analysis. T2 weighted turbo spin echo (T2W-TSE) sequences were acquired in three planes, using the following parameters: echo time (TE)/repetition time (TR): 80/1250ms, slice thickness: 5 mm, gap: 1mm, number of excitations (NSA):1, sensitivity encoding (SENSE), field of view (FOV) and slices varied according to the maternal actual situation, such as gestational age, fetal and placenta position.

The MRI image data were independently examined by two radiologists (Tang:25 years of experience; Chen:7 years of experience) who possess expertise in diagnosing gynecology and obstetrics diseases using MRI. These radiologists were unaware of any clinical or surgical information. The images of all participants were extracted in DICOM format from the Picture Archiving and Communication System (PACS), and the sagittal T2W images were subsequently imported into firevoxel software (https://www.firevoxel.org)for manual delineation of the region of interest (ROI). The radiologists manually traced the ROI layer by layer along the placental edge on the T2W images, and subsequently generated a histogram encompassing all ROIs of the whole placenta, as shown in Fig. 1. The histogram recording parameters included mean, variances, skewness, kurtosis, entropy, 10th percentile, 50th percentile, 90th percentile and 99th percentile.

The morphological parameters of volume and thickness were documented. And the volume of the whole placenta was recorded in conjunction with the aforementioned procedures. In PACS, the thickest section of the placenta at the mid-sagittal plane was measured twice for each patient, the average thickness was ascertained [12].

Placental Histology Assessment

Histological examinations of placentas were performed at the hospital subsequent to delivery, whenever feasible. Placentas were preserved in 10% buffered formalin. A standard dehydration procedure, transparency assessment, staining with hematoxylin/eosin, and immersion in wax were employed to generate 5µm sections. Placental lesions were categorized based on the Amsterdam criteria into two groups: maternal vascular malperfusion (characterized by augmented syncytial nodules, increased fibroin deposition amidst villi, and developed villous) and fetal vascular malperfusion ( thrombosis of the chorionic plate vessels, avascular villi, and dilation of villous interstitium vessels, among other abnormalities).The sections were examined and evaluated by two pathologists using a light microscope set at a magnification of ×400.

Statistical Analysis

The data underwent normality testing using the Shapro-wilk test. Continuous variables were presented as standard deviation (SD) and interquartile range (IQR), while categorical variables were presented as counts. To compare continuous variables between the two groups, either the Student-t test or Mann-Whitney U test was employed. The Chi-square test was utilized to compare categorical variables. The diagnostic efficacy of parameters in predicting PE was assessed using the ROC curve, with the area under the curve (AUC) serving as a quantitative measure. The AUC ranged from 0.5 to 1, with values closer to 1 indicating better predictive ability. Sensitivity, specificity, and cutoff values were calculated for each parameter.All statistical analyses were performed on a personal computer using the SPSS 20.0 statistical package (Chicago, IL, USA). We considered differences to be significant at P < 0.05 (2-tailed).

Study group

Among the cohort of 22 patients diagnosed with PE, 12 exhibited early-onset PE (≤ 34 weeks’ gestation), while the remaining 10 experienced late-onset PE (> 34 weeks’ gestation). No instances of maternal or neonatal mortality were documented. The demographic and clinical characteristics of both the PE and control groups were presented in Table 1. Notably, there were no statistically significant difference observed in terms of age, gestational age, gravidity, parity, or Apgar scores at 5 minutes. Furthermore, it was observed that 50% of the PE patients were born prematurely(P = 0.002), resulting in lower neonatal birthweights (P = 0.004) and diminished Apgar scores at 1 and 10 minutes (P = 0.009, P = 0.038).

Fifty percent (11/22) of the placentas from both groups were subjected to pathologic examination. Within the PE group, eight subjects displayed maternal vascular malperfusion, with two subjects additionally presenting fetal vascular malperfusion. Furthermore, five subjects were identified as having early-onset PE, resulting in preterm birth and low birth weight. The remaining three subjects in the PE group, who did not exhibit maternal vascular malperfusion, experienced elevated blood pressure after 36 weeks of gestation. Conversely, no instances of maternal or fetal vascular malperfusion were observed in the control group, as shown in Table 2.

Table 1

Demographics and clinical characteristics for PE and control group
	PE (n = 22)	Control group (n = 22)	t/Z/χ2	P value
Age(year)¹	34 ± 6	31 ± 5	-1.434	0.159
Gestational age(week)²	30 ± 5	33 ± 4	1.800	0.079
Gravidity³	3(1,4)	2(2,3)	-0.473	0.636
Parity⁴	1(1,2)	1(0,1)	-0.760	0.447
Preterm infant⁵	50.0%(11/22)	4.5%(1/22)	-	0.002*
Neonatal birthweight(g)⁶	2408 ± 904	3033 ± 338	3.039	0.004*
Apgar score at 1min⁷	10(8,10)	10(10,10)	-2.608	0.009*
Apgar score at 5min⁸	10(10,10)	10(10,10)	-1.428	0.153
Apgar score at 10min⁹	10(10,10)	10(10,10)	-2.074	0.038*
Note:^1,2,6 were used the independent sample t test to analyze the difference among the two groups.

and the results were expressed by (mean standard ± deviation); ^3,4,7,8,9was used Mann-Whitney U test to analyze the difference among the two groups, and the results were expressed by (median (interquartile interval)); ⁵was used Fisher exact test to analyze the difference among the two groups; *P < 0.05 was considered to be statistically significant.

Table 2

Histology Findings of Placental Tissue
Placental Histology Features	PE	Control group
No. of placenta for evaluation	11	11
Maternal vascular malperfusion features	8(72.7%)	0
Fetal vascular malperfusion features	2(18.2%)	0
Hypertensive pathology during pregnancy	8(72.7%)	0

Analysis of T2W image histogram and morphological parameters of whole-volume placenta of PE and control groups

There were statistically significant differences in variances (P = 0.004) and the 99th percentile (P = 0.029) between the PE group and the control group. However, no significant differences were observed between the two groups for other parameters, such as mean, sskewness, kurtosis, entropy, 10th percentile, 50th percentile, and 90th percentile, as indicated in Table 3 and Fig. 3–5. In terms of morphological changes, the mean placental volume in the PE group was 8.81×10²±3.1×10² cm³, while it was 6.48×10²±4.05×10² cm³ in the control group, demonstrating a significant difference between the two groups (P = 0.039). However, the thickness did not reach statistical significance( Figs. 2 and 3,Table 3).

Table 3

The difference between PE and control groups of histogram parameters and morphological characters of the whole placenta
Feature	Parameter	PE group (n = 22)	Control group (n = 22)	t/Z value	P value
Histogram	Mean¹	6.39×10²±2.59×10²	5.37×10²±2.04×10²	-1.445	0.156
	Variances²	4.74×10⁴±3.59×10⁴	2.30×10⁴±1.05×10⁴	-3.067	0.004*
	skewness³	0.48(0.19,0.85)	0.60(0.05,0.92)	-0.023	0.981
	Kurtosis⁴	-0.03(-0.48,1.99)	0.60(-0.21,1.57)	-0.634	0.526
	Entropy⁵	3.79 ± 0.25	3.68 ± 0.19	-1.685	0.099
	10th percentile⁶	3.95×10²±1.85×10²	3.60×10²±1.63×10²	-0.662	0.512
	50th percentile⁷	6.19×10²±2.64×10²	5.23×10²±1.63×10²	-1.318	0.195
	90th percentile⁸	9.13×10²±3.52×10²	7.34×10²±2.36×10²	-1.968	0.056
	99th percentile⁹	11.5×10²±4.09×10²	9.15×10²±2.66×10²	-2.258	0.029*
Morphological	Volume(cm³)¹⁰	8.81×10²±3.11×10²	6.48×10²±4.05×10²	2.131	0.039*
	Thickness(mm)¹¹	47.42 ± 20.51	40.28 ± 8.08	2.370	0.136

Note:^{1,2,5,6,7,8,9,10,11} were used the independent sample t test to analyze the difference among the two groups. and the results were expressed by (mean standard ± deviation); ^3,4was used Mann-Whitney U test to analyze the difference among the two groups, and the results were expressed by (median (interquartile interval)); *P < 0.05 was considered to be statistically significant.

The diagnostic efficiency of histogram parameters and volume to differentiate PE and control groups

The variances, 99th percentile, and volume for PE demonstrated a notable distinguishing ability, as evidenced by AUC values of 0.713 (95%CI 0.749–0.908, P = 0.016), 0.693 (95%CI 0.531–0.855, P = 0.028), and 0.709(95%CI 0.552–0.886, P = 0.018), respectively. The corresponding sensitivities were 50%, 54.55%, and 90.91%, while the specificities were 95.45%, 90.91%, and 54.55%, respectively (Table 4 and Fig. 6). Furthermore, when these three parameters were combined, the AUC value increased to 0.899 (95%CI 0.808–0.985, P = 0.000), with a sensitivity of 86.36% and specificity of 77.27% (Table 4 and Fig. 4).

Table 4

The diagnostic efficiency of histogram parameters and volume to differentiate PE and control groups
Parameters	AUC	P value	95%CI	Cutoff	Sensitivity	Specificity
Variances	0.713	0.016*	0.554–0.871	3.81×10⁴	50.00%	95.45%
99th percentile	0.693	0.028*	0.531–0.855	12.35×10²	54.55%	90.91%
Volume	0.709	0.018*	0.552–0.886	5.46×10²	90.91%	54.55%
Combined	0.899	0.000*	0.808–0.985	-	86.36%	77.27%

In the current study, the utilization of routine MRI sequence T2W image of the placenta has demonstrated the potential to extract histogram features, which hold significant value in distinguishing patients with PE from normal pregnant women. To the best of our knowledge, this research represents the first investigation into the texture features of placental MR images in individuals diagnosed with PE. Moreover, this non-invasive approach offers the ability to detect placental abnormalities in PE patients prior to delivery.

The placental pathological alterations observed in patients with PE differed significantly from those observed in normal pregnant women, indicating a direct reflection of placental function and a close association with adverse maternal and infant outcomes[13, 14]. The poorly oxygenated regions in preeclamptic placentae exhibited low-signal intensity on T2W image, displaying varying sizes and shapes[7]. In this study, histogram analysis was employed to quantitatively assess placental heterogeneity visually, revealing higher values of variance and the 99th percentile in the PE group.The variance is defined as the average of the squared distances between each intensity value and the mean value. In clinical contexts, a higher variance value suggests a greater heterogeneity of tissues within the region of interest (ROI). Additionally, the N% percentile can partially reflect disparities in the composition, structure, or distribution of the lesion. Previous research{Hutter, 2019 #475, 15, 16] has indicated that the PE group exhibited a higher 99% percentile value, potentially attributed to placental hypoxia, which triggers calcium deposition and the subsequent formation of microcalcifications, thereby resulting in elevated local grayscale values. Furthermore, our morphological measurement analysis demonstrated a significant increase in placental volume among patients diagnosed with PE. Similar observations were made in pathological investigations, where enlarged placental mass or surface area were frequently associated with this condition[13, 14].

Prior to the onset of PE, it is possible to predict and differentiate it through the consideration of maternal factors, biomarkers (such as plasma placental growth factor), and ultrasound Doppler. The sensitivity and specificity of these predictive methods range between 30–80% and 60–90%, respectively[17–19]. Previous research on the analysis of placental image texture using ultrasound had demonstrated that the specificity and sensitivity of placental texture features are superior to those of PIGF and uterine artery pulsatility index for predicting hypertension during pregnancy[10]. It had been observed that healthy pregnancies exhibit an elevation in skew and kurtosis, derived from histograms of T2* values in placental MR images, as gestational age progresses[15]. However, in women with chronic hypertension, these values overlapped with those of the control group.In our study, we observed statistically significant differences in two histogram parameters between the PE and normal groups. These parameters can be utilized to differentiate between the two groups, demonstrating acceptable diagnostic efficacy with good AUCs approaching 0.7. While the sensitivity for a single parameter was limited to over 50%, the specificity was high, exceeding 90%. This observation may be attributed to the composition of cases within the PE group, which included 10 instances of late-onset PE and only approximately 50% of patients exhibiting pathological changes in placental histology pathology examination indicative of PE.Based on the existing body of literature[1–4], it has been observed that late-onset PE exhibited comparatively less severe clinical symptoms and pathological damage in comparison to early-onset PE. Furthermore, the predictive ability for late-onset PE was relatively lower[20]. In our study, patients with late-onset PE demonstrated mild placental damage, which could potentially account for the slightly reduced sensitivity observed. Notably, the combined AUC value of the three parameters approached 0.9, with a heightened sensitivity. Therefore, it was advisable to employ multiple parameters or a combined approach in order to enhance the prediction and differentiation of PE.

The study encountered several limitations. Firstly, it was a retrospective study with a relatively small number of cases in the PE group. To enhance the statistical power and validate our findings, the sample size will be increased. Secondly, although a whole-volume ROI was utilized, the placement of ROIs was done manually, resulting in measurement variability. The implementation of a semiautomatic placenta segmentation method could mitigate this variability and enhance reproducibility[8]. Future research should focus on optimizing the method for defining ROIs. Finally, in order to adhere to the pre-established diagnostic objectives for MRI examinations of pregnant women, we exclusively employ T2W image for histogram analysis, as it was imperative to minimize exposure[21–23]. In subsequent scanning plans, we aim to incorporate additional functional MRI sequences for texture analysis, guided by the jointly formulated practice guidelines of the American College of Radiology and the Society for Pediatric Radiology [22, 23].

The development of PE is characterized by complexity and variability, as pregnant women with non-severe PE may experience a gradual progression towards severe PE or eclampsia. Additionally, the condition can worsen suddenly without evident prodromal symptoms, resulting in seizures[24]. Consequently, it is imperative to closely monitor changes in the condition, comprehend its severity and progression, in order to intervene promptly and prevent adverse pregnancy outcomes. Our study provided a novel method for distinguishing the PE group from the normal group, which may also have a positive effect on disease monitoring and prediction.

PE: pre-eclampsia; MRI: Magnetic resonance imaging; T2W: T2-weighted; ROI:Region of interest; ROC:Receiver operating characteristic; AUC: Area under the receiver operating characteristic;

Acknowledgements

We thank all the women who participated in the study, their midwives and obstetricians involved in study recruitment.

Authors’ contributions

YLC,WYT, YL and TS were involved in study conception,design, data acquisition and analysis. QS were involved in data analysis. YMD, JWH and ZRL contributed to data acquisition. YLC, WYT and TS drafted the manuscript. All authors authors reviewed the manuscript.

Funding

This work was supported by the Guangdong Medical Science and Technology Research Foundation (CN) [grant numbers A2024117] .

Availability of data and materials

The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

Ethics approval and consent to participate

This retrospective study was approved by the institutional review board at the third afliated hospital, Guangzhou Medical University, and the requirement of patients’ informed consent was waived.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Author details

1.Department of Radiology, The Third Affiliated Hospital, Guangzhou Medical University, No. 63 Duobao Road, Guangzhou 510150, People’s Republic of China

2.Guangdong Provincial Key Laboratory of Major Obstetric Diseases, The Third Affiliated Hospital, Guangzhou Medical University, No. 63 Duobao Road, Guangzhou 510150, People’s Republic of China

3.Guangdong Provincial Clinical Research Center for Obstetrics and Gynecology, The Third Affiliated Hospital, Guangzhou Medical University, No. 63 Duobao Road, Guangzhou 510150, People’s Republic of China

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Histogram analysis of whole placental T2-weighted magnetic resonance image-derived in patients with Pre-eclampsia

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Abstract

Background

Methods

Results

Conclusions

Figures

Background

Methods

Patients

MR Assessment

Placental Histology Assessment

Statistical Analysis

Results

Study group

The diagnostic efficiency of histogram parameters and volume to differentiate PE and control groups

Discussion

Conclusions

Abbreviations

Declarations

References

Additional Declarations

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Version 1