Comparison between electron density imaging with dual-energy computed tomography without contrast medium and magnetic resonance imaging for high-grade glioma

doi:10.21203/rs.3.rs-4708655/v1

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Research Article

Comparison between electron density imaging with dual-energy computed tomography without contrast medium and magnetic resonance imaging for high-grade glioma

https://doi.org/10.21203/rs.3.rs-4708655/v1

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Background

Dual-energy computed tomography (DECT) has been used for the prediction of glioma grading and malignancy, in addition to magnetic resonance imaging (MRI) findings. In DECT, electron density (ED) can be quantitatively measured and determined with high accuracy. However, no studies have demonstrated whether DECT alone can detect tumor-infiltrating areas or evaluate malignancy. Therefore, we evaluated the use of ED imaging with DECT showing high-density areas of high-grade glioma (HGG), compared it with MRI gadolinium-enhanced T1-weighted image (GdT1) enhancing area, and analyzed its effectiveness in evaluating malignancy.

Methods

Ten patients with enhanced masses on GdT1 MRI were enrolled in this retrospective study. Ten slices of ED and GdT1 images of 10 patients with HGG were analyzed by three raters. The relationships between the area of high ED on DECT and enhanced area on GdT1 and between the relative ED of the high ED area and contralateral white matter on DECT were determined.

Results

Linear regression analysis revealed a positive correlation between areas of high ED and Gd enhancement among all raters (rater A: R² = 0.910, P < 0.0001, B: R² = 0.857, P = 0.0001, C: R² = 0.717, P = 0.002), and the intraclass correlation coefficient was 0.75. A comparison of the relative ED between the tumor and contralateral white matter revealed that the mean and maximum relative ED of the tumor area was significantly higher than that of the contralateral white matter (mean: P = 0.049, maximum: P = 0.0002).

Conclusions

ED images of DECT show a high ED area similar to the Gd enhancement area in HGG, and the mean and maximum relative EDs of this area are significantly higher than those of the contralateral white matter.

Dual-energy CT

electron density imaging

gadolinium-enhanced imaging

high-grade glioma

Glioma is an aggressive tumor, with the treatment of high-grade glioma (HGG) being difficult, especially glioblastoma, isocitrate dehydrogenase (IDH)-wildtype and astrocytoma, IDH-mutant, grade IV [3, 24]. HGG treatment consists of surgical resection, followed by radiation and chemotherapy. Therefore, the surgical resection rate and grading of HGG are related to prognosis; further, preoperative diagnosis, including genetic information and prediction of infiltrating tumor cells, is important [9, 17, 19]. During glioma surgery, several imaging studies are required for safe and maximal resection. Magnetic resonance imaging (MRI) is the gold standard for diagnosing glioma, especially in HGG, and gadolinium-enhanced T1-weighted image (GdT1) is effective for determining diagnosis for subtypes, tumor-infiltrating area and malignancy [22].

Recent studies have reported that advanced MRI techniques, including diffusion-weighted imaging, amide proton transfer imaging, arterial spin labeling, and MR spectroscopy, are useful for grading gliomas, determining tumor resection area, and predicting recurrence [1, 4, 8, 14, 16, 20, 23]. Although MRI is essential for glioma treatment, it cannot be performed on some patients due to claustrophobia or because of the presence of metal or pacemaker in their body. Artifacts due to the presence of metal (coil, clip) and movement over a long examination time may decrease MRI accuracy. Furthermore, MRI is expensive and requires maintenance procedures. Additionally, several patients with HGG require an examination using a contrast medium [22]. Using a contrast medium is invasive due to insertion of needle and risk of allergy and anaphylactic shock, and it cannot be used in some patients because of renal dysfunction or allergy. In the MRI era, the use of X-ray computed tomography (CT) to detect brain tumors, including glioma, is relatively ineffective. Recently, dual-energy CT (DECT) has been reported to be useful for differentiating glioma grade and recurrence [2, 13].

DECT is a CT technique that uses two different photon spectra. A major advantage of DECT is its material-differentiation ability, which is based on high- and low-peak X-ray tube voltage acquisition [21]. One aspect that can be measured using DECT is electron density (ED). ED indicates the probability of an electron being present at a specific point in space, which depends on the type of tissue [5]. Several studies have used DECT for the prediction of glioma grading and malignancy, in addition to MRI findings [6, 13]. However, no studies have demonstrated that DECT alone can detect tumor-infiltrating areas or evaluate malignancy. In DECT, ED can be quantitatively measured and determined with high accuracy.

Here, we aimed to study the ED image obtained using DECT to compare the enhancing area of HGG obtained on GdT1 MRI and analyze its effectiveness in evaluating malignancy.

Patients

This retrospective study was single-institution study. This study was conducted according to the principles of the Declaration of Helsinki, and approved by the research ethics committee of university of Fukui (IRB#20230130), and the requirement for informed consent was waived.

Patients diagnosed with HGG based on the 2021 World Health Organization guidelines, histopathological findings, and genetic patterns who underwent DECT and MRI between January 2021 and October 2023 in our hospital were included in this study [11]. The time interval from DECT to MRI being performed for evaluation in this study was up to 2 weeks. Patients with noticeable enhanced masses on GdT1 MRI were included; those without enhanced masses or with only ring-enhanced masses were excluded because of the large heterogeneity due to necrosis and edema of cell density in the tumor. Finally, 10 patients—9 with glioblastomas and 1 with astrocytoma, grade IV—were enrolled in this study, comprising 4 males and 6 female patients (median age, 69.5 [range, 30–82] years, Table 1).

Table 1

Characteristics of the study patients
Characteristic					Value
Age, years (median, range)					69.5, 30-82
Sex (no, %)
Male					4 (40)
Female					6 (60)
Diagnosis (no, %)
Glioblastoma					9 (90)
Astrocytoma, grade IV					1 (10)
Minimum rED of the tumor area					1.026 ± 0.005
Minimum rED of the CLWM area					1.025 ± 0.004
Mean rED of the tumor area					1.031 ± 0.005
Mean rED of the CLWM area					1.028 ± 0.004
Maximum rED of the tumor area					1.036 ± 0.005
Maximum rED of the CLWM area					1.031 ± 0.004
ED = electron density, rED = relative electron density, CLWM = contralateral white matter

Dual-energy computed tomography

All CT examinations were performed using a dual-source DECT scanner (SOMATOM Force; Siemens Healthineers, Forchheim, Germany). Non-contrast DECT acquisition was performed in a dual-energy acquisition mode with the following scan parameters: pair of tube voltages, 80 kV and 150 kV with tin filtration (Sn150 kV); X-ray beam width, 64 × 0.6 mm; rotation time, 1.0 s; and pitch, 0.8. The effective tube current time values were set to 800 mAs at 80 kV and 533 mAs at Sn150 kV. The mean CT volume dose index was approximately 65.82 mGy.

DE datasets (80 kV and Sn150 kV) were reconstructed using a quantitative convolution kernel of Qr40 and an iterative reconstruction algorithm ADMIRE (Siemens Healthineers, Forchheim Germany) of strength 3, with an increment of 0.6 mm and a slice thickness of 1 mm. All image data were transferred to a dedicated dual-energy application software on a workstation syngo.via (Siemens Healthineers, Forchheim, Germany) to generate the ED images.

Magnetic resonance imaging

All MRI scans were obtained using a 3.0-T clinical MRI unit (Discovery MR750, GE Healthcare, Milwaukee, WI, USA) with a 32-channel head receiver array and a body transmission coil system. Standard MRIs (plain and GdT1) were performed during the examination. The acquisition parameters of standard MRIs were as follows: GdT1, three-dimensional (3D) inversion-recovery prepared spoiled gradient recalled echo sequence; repetition time, 6.6 ms; echo time, 2.1 ms; field of view, 240 × 216 mm; slice thickness, 1.4 mm; inversion time, 700 ms; flip angle, 10°; matrix size, 420 × 192; parallel imaging factor, 2; and average, 1.

Data processing and image evaluation

First, an enhanced mass was assessed using GdT1 MRI (Fig. 1a and b). All ED images were smoothed using 3D median and Gaussian blur filters using the ImageJ software (version 1.54g, National Institutes of Health, Bethesda, Maryland, USA) to remove significant image noise. A lookup table of the GEM was used, and the display window level/width was optimized to emphasize the tumor (Fig. 1c and d).

A radiological technician with 29 years of experience performed the data processing. Two board-certified neurosurgeons with 13 and 14 years of experience and a radiologist with 12 years of experience analyzed the area of each image. For measurement, a slice of the gadolinium-enhanced image with the maximum enhanced mass area was selected by a radiologist with 12 years of experience and neurosurgeon with 13 years of experience, and the same slice on the ED image was selected. In the ED image after processing, the area of high ED was surrounded freehand as a region of interest (ROI) on ImageJ (Fig. 2a and b). The high ED area was defined as upper density than density of contralateral structure visually. This ROI was drawn based on the following rules for both DECT and MRI: continuous high ED area without cysts and ring enhancement with an evident necrotic core on MRI, excluding skip lesions with high ED on the same surrounding edema. As the ratios of length and width in each CT and MRI were different, the length and width of the brain on the same slice were measured to correct for the differences between CT and MRI measurements (Fig. 2c). On GdT1 MRI, the enhanced area was surrounded and the length and width of the brain on the same slice were measured using the same method (Fig. 2e and f).

In the ED image, the Hounsfield unit (HU) on a round ROI of 200 mm² in the normal contralateral white matter (CLWM) based on FLAIR image was measured by a board-certified neurosurgeon with 13 years of experience to compare the relative ED (rED, relative to ED of water) between the tumor area (Fig. 2b) and the CLWM (Fig. 2d). rED was manually calculated using the following formula:

ρ _e (rED) = ΔHU/1000 + 1

Statistical analyses

Linear regression analysis was performed between the areas after correction by each brain (brain: length × width) on CT and MRI for each rater. Inter-rater reliability (IRR) for the area ratio of high ED/brain, Gd enhancement/brain, ratio of area ratio of high ED/brain (HEDA), and Gd enhancement/brain (GDA) was evaluated using the intraclass correlation coefficient (ICC). The minimum, mean and maximum rED were examined using Student’s t-test. The sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of rED and CLWM were calculated. Receiver operating characteristic (ROC) curve analysis and the area under the curve (AUC) for rED were calculated. All analyses were performed using the JMP® 12.2 software (SAS Institute Inc., Cary, NC, USA). In all tests, a p value < 0.05 was considered statistically significant.

Relationship between high ED and gadolinium enhancement area

Ten slices of ED and GdT1 images from 10 patients with HGG were measured by three raters (two board-certified neurosurgeons with 13 and 14 years of experience and a radiologist with 12 years of experience). In regression analysis, the area ratios of high ED/brain and Gd enhancement/brain were linearly related. The graph showed a positive correlation between the area ratio of high ED/brain and Gd enhancement/brain in all raters (Fig. 3a: R² = 0.910, P < .0001, board-certified neurosurgeon with 13 years of experience; B: R² = 0.857, P = 0.0001, board-certified neurosurgeon with 14 years of experience; C: R² = 0.717, P = 0.002, radiologist with 12 years of experience).

Among the three raters, the ICCs of HEDA, GDA, and the HEDA/GDA ratio were 0.98, 0.97 and 0.75, respectively (Table 2).

Table 2

Inter-rater reliability for the area ratio of high ED and Gd enhancement
Parameter	ICC
Area ratio of high ED/brain	0.98
Area ratio of Gd enhancement/brain	0.97
Ratio of HEDA/GDA	0.75
ED = electron density, Gd = gadolinium, ICC = intraclass correlation coefficient, HEDA = area ratio of high ED/brain, GDA = area ratio of Gd enhancement/brain

Comparison between relative ED of the tumor area and CLWM

In rED measurement (Table 1), the minimum rEDs of the tumor area and CLWM were 1.026 ± 0.005 and 1.025 ± 0.004, and the difference was not significant (Fig. 4a, P = 0.441). However, the mean and maximum rEDs of the tumor area and CLWM were 1.031 ± 0.005 and 1.028 ± 0.04, and 1.036 ± 0.005 and 1.031 ± 0.04, respectively. The mean and maximum rED of the tumor area were significantly higher than that of the CLWM (Fig. 4c: mean rED, P = 0.049/4e: maximum rED, P = 0.0002). In a representative case, specimens from the high ED- and Gd-enhanced areas showed high cell density (Fig. 2g) and 10% in Ki-67 (Fig. 2h). Figure 4 [b (minimum rED), d (mean rED), and f (maximum rED)] shows the ROC curves. In the minimum rED, the AUC, cut-off value, sensitivity, specificity, PPV, and NPV were 0.654, 1.025, 55.6%, 77.8%, 75.0% and 70.0%, respectively. In the mean rED, the AUC, cut-off value, sensitivity, specificity, PPV, and NPV were 0.802, 1.028, 77.8%, 77.8%, 77.8% and 77.8%, respectively. In contrast, in the maximum rED, the AUC, cut-off value, sensitivity, specificity, PPV, and NPV were 0.962, 1.031, 100%, 77.8%, 81.8%, and 100%, respectively (Table 3).

Table 3

Diagnostic accuracy of rED in differentiating HGG and CLWM
Parameter	AUC	Cut-off value	Sensitivity (%)	Specificity (%)	PPV (%)	NPV (%)
Minimum rED	0.654	1.025	55.6	77.8	75.0	70.0
Mean rED	0.802	1.028	77.8	77.8	77.8	77.8
Maximum rED	0.962	1.031	100	77.8	81.8	100
rED = relative electron density, HGG = high-grade glioma, CLWM = contralateral white matter, AUC = area under curve, PPV = positive predictive value, NPV = negative predictive value

DECT and rED are primarily used in calculating radiotherapy dose and treatment planning [7]. DECT is effective for differentiating benign and malignant tumors in hepatocellular carcinoma, prostate carcinoma, and cervical cancer [10, 12, 18, 25, 26]. In brain tumors, ED may correlate with tumor histology, glioma grading, and recurrence [2, 6, 13]. However, several quantitative studies have been conducted on this aspect. When used only for cerebral infarctions, Noguchi et al. reported that X-map, a novel imaging technique in DECT, could visualize ischemic lesions [15]. In this study, we emphasized and visualized HGG lesions using ED images, such as Gd-enhanced MRI (Figs. 1 and 2). This is the first study to visualize and emphasize brain tumor-like enhanced images without contrast medium. Our data showed that the high ED area of the HGG correlated with the Gd enhancement area on the image. Although a difference existed in the range of correlation among the raters, including radiological technician, experienced neurosurgeons, all measurements from each of the three raters showed significant results. In various evaluations from different positions and experiences, the ICC for the HEDA/GDA ratio was 0.75 (value of over 0.7 means OK in IRR). Our results indicate that ED images obtained with DECT without a contrast medium may be capable of drawing images, such as GdT1 in HGG.

MR images are effective for deciding tumor invasion area and using contrast medium emphasizes more. However, MRI cannot be performed for certain reasons, such as the presence of pacemaker, shunt system, and body metal and art, and conditions such as claustrophobia. Furthermore, the use of gadolinium in patients with allergy, asthma, and renal dysfunction remains a challenge. In this study, ED image without contrast medium resembled Gd-enhanced image on HGG. HGG patients in whom enhanced MRI cannot be conducted, due to the above-mentioned reasons, ED image may be useful. Furthermore, CT is inexpensive and requires a shorter examination time than does MRI. Contrast medium imaging emphasizes vessels, high blood volume, and disruption of the blood–brain barrier, whereas ED imaging emphasizes high ED tissues. Our Gd-enhanced sample and high ED area showed high cell density and malignancy (Fig. 2g and h), and the rED in the tumor area was higher than that in the CLWM in this study. Both contrast medium and ED images indirectly reveal the presence of tumor cells, and abnormal emphasis in the brain may predict the presence of high malignancy and density of tumor cells. Some studies have reported that ED and rED can predict glioma malignancy [2, 6]. Based on our results, both area and quantitative analyses of the ED-emphasized area on ED images may show high-density areas in HGG with the same Gd enhancement on MRI as the gold standard for HGG.

In the quantitative analysis of rEDs, the maximum rED showed the biggest difference (Fig. 4a, c, and e). HGG includes strong tumor heterogeneity through a homogeneously enhanced mass, and ED may reflect tumor heterogeneity. By contrast, cell heterogeneity is rare in normal brains, and the presence of heterogeneity in ED images may indicate high malignancy. Our results demonstrated the usefulness of using the ED on CT in HGG with only an evident mass. A cut-off value of 1.031 of the maximum rED distinguishes high density of tumor cells from normal brain.

Typical HGG and glioblastoma often exhibit ring enhancement, with several contents such as abnormal vessels, necrosis, inflammatory cells, and tumor cells are noted in this area. We presume that high ED implies high cell density; however, thin membrane of the ring enhancement indicates abnormal vessel and not high cell density. Furthermore, the inside of the ring enhancement is almost necrosis. We excluded the ring-enhanced shape due to risk of uncertain measurement of ED, and only 10 cases with noticeably enhanced mass were included. However, as several HGGs exhibit ring enhancement, ED images of all HGG shapes should be included in future studies. Furthermore, our study presents results from only one shape with noticeable mass, from among the several types of HGG shape. ED tends to be higher near the bone because of CT; however, the underlying mechanism of this type of occurrence in HGG remains unclear. Thus, elucidation of this aspect and the pathological evidence needs to be clarified. It is challenging to visualize all shapes of HGG, including cysts and ring enhancements. In future studies, additional cases may make our results more applicable to HGGs with various shapes.

To our knowledge, this is the first study to visualize brain tumor using ED image obtained with DECT, which showed a high ED area, similar to the Gd enhancement area in the HGG; furthermore, the rED was higher in this area than in the CLWM, especially remarkable in the maximum rED. This method may help diagnose HGG in patients who cannot undergo MRI because of various limitations.

Acknowledgments

We would like to express our appreciation to Yuki Matta and Koki Takahashi (Department of Radiology, University of Fukui Hospital) who helped with the data processing.

Conflicts of interest

All authors have no financial conflicts of interest to disclose concerning this article.

Author contributions

All authors contributed to the study’s conception and design. Material preparation, data collection and analysis were performed by Takahiro Yamauchi, Tomokazu Ishida, Toshihide Itoh, Tadahiro Tsubota, Kenji Takata, Yoshifumi Higashino, Tetsuya Tsujikawa and Ken-ichiro Kikuta. The first draft of the manuscript was written by Takahiro Yamauchi and all authors commented on the previous manuscript. All authors read and approved the final manuscript.

Supplementary information

Funding

No funding was received for the research.

Data availability

Code availability

Ethical approval

This retrospective study was approved by the research ethics committee of university of Fukui (IRB#20230130).

Consent to participate

Opt-out method was received in this study.

Consent for publication

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You are reading this latest preprint version

Comparison between electron density imaging with dual-energy computed tomography without contrast medium and magnetic resonance imaging for high-grade glioma

Status:

Version 1

Abstract

Background

Methods

Results

Conclusions

Figures

Introduction

Material and Methods

Patients

Dual-energy computed tomography

Magnetic resonance imaging

Data processing and image evaluation

Statistical analyses

Results

Relationship between high ED and gadolinium enhancement area

Comparison between relative ED of the tumor area and CLWM

Discussion

Conclusions

Declarations

References

Additional Declarations

Status:

Version 1