Diagnostic value of subtraction CT in evaluating the efficacy of transcatheter arterial chemoembolization-treated hepatocellular carcinoma patients compared to conventional CT and MRI

Introduction

Hepatocellular carcinoma (HCC) is a common malignant tumor worldwide. According to the guidelines from the European Association for the Study of the Liver (EASL) and the European Organization for Research and Treatment of Cancer (EORTC), transcatheter arterial chemoembolization (TACE) is regarded as the first-line treatment for liver cancer, especially for HCC (1,2). In traditional TACE, the most commonly used embolic agents are mixtures of iodized oil and chemotherapeutic drugs, which embolize the tumor-feeding arteries, leading to ischemic necrosis of tumor cells and thus achieving therapeutic effects (3,4). After TACE treatment, accurate evaluation of residual tumor viability is crucial for predicting prognosis and guiding subsequent treatment. Clinically, computed tomography (CT) and magnetic resonance imaging (MRI) images are widely used for tumor viability assessment in HCC patients (5,6). However, conventional CT and MRI images would misdiagnose the tumor viability because the high density which caused by iodized oil may mask arterial phase hyperenhancement (APHE) of residual tumor (7,8).

Subtraction CT technique has been applied in clinical based on imaging registration algorithm and motion correction (9). Several studies showed that subtraction CT could effectively improve the diagnostic performance in coronary artery stenosis and pulmonary embolism (10-12). However, studies about diagnostic value of subtraction CT in HCC patients were still rare. Therefore, this study aims to apply subtraction CT technique in assessing the efficacy of TACE in HCC patients compared to conventional CT and MRI images. We present this article in accordance with the STARD reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2679/rc).

Methods

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Ethics Committee of Qingdao University Affiliated Qingdao Third People’s Hospital (No. 2023Y111552). Informed consent was waived in this retrospective study.

Study population

One hundred and forty-six patients who diagnosed with malignant tumors of liver and treated with TACE between July 2021 and March 2024 were retrospectively collected. All HCC diagnoses were pathologically confirmed by ultrasound-guided percutaneous core needle biopsy performed within one week prior to the first TACE treatment. The data were sourced from Qingdao University Affiliated Qingdao Third People’s Hospital and The Affiliated Hospital of Qingdao University. The inclusion criteria were the following: (I) patients who underwent follow-up examination including multiphase enhanced CT and MRI after first TACE treatment; (II) the multiphase enhanced CT and MRI were performed within one week prior to the second TACE treatment; (III) age larger than 18 years old. The exclusion criteria were the following: (I) patients with liver metastases; (II) patients with cholangiocarcinoma; (III) patients with a history of liver surgery; (IV) poor image quality with motion artifacts; (V) patients with poor liver function unable to tolerate second TACE treatment.

CT scanning and post-processing

All patients underwent abdomen multiphase enhanced CT examinations by using 320-row detector CT scanner (Aquilion One Genesis, Canon Medical System, Otawara, Japan). Scanning was performed in the craniocaudal direction from the diaphragm to the groin. Scanning parameters were as follows: detector number: 80 mm × 0.5 mm, tube voltage: 120 kVp, automatic tube current modulation with a standard deviation of 7.5 HU, rotation time: 0.5 s/circle, pitch factor: 0.813, matrix size: 512×512. Images were reconstructed with hybrid IR (Adaptive Iterative Dose Reduction 3-Dimensional, AIDR 3D, FC 08) and slice thickness was 1 mm and slice interval was 0.8 mm. Enhanced scanning was performed by injecting 1.5–2.0 mL/kg of iodinated contrast medium (iopromide, 300 mgI/mL) with a rate of 3–4 mL/s. The arterial phase scan initiated 10 seconds after the abdominal aorta reached a threshold of 180 HU. The portal venous and delay phase were performed 50 and 120 seconds after contrast injection, respectively. The patients were asked to hold the breath at full inspiration during the scan. The non-contrast and arterial phase images were input into post-processing software (^SUREsubtraction iodine mapping) to obtain subtraction images (13).

MRI scanning

Dynamic contrast-enhanced MRI images were obtained using Philips 1.5T MRI scanner (Best, The Netherlands). Patients fasted for 4–6 hours before the examination and were trained to hold their breath by technicians before the scan. The supine position was selected, with the scanning range covering from the diaphragm to the lower edge of the liver. Conventional T1-weighted images (T1WI), T2-weighted spectral presaturation with inversion recovery (T2WI-SPIR) images, and diffusion-weighted images (DWI) were collected first, followed by transverse e-THRIVE-dynamic sequence scanning to obtain dynamic contrast-enhanced images in three phases. The transverse scan parameters were: echo time (TE) and repetition time (TR) set to the shortest time; field of view (FOV) 375 mm × 375 mm; slice thickness 5 mm; matrix size 336×336; number of excitations 1; breath-hold time of 10–20 seconds per phase; completing one full liver volume scan per phase. Gadobutrol was injected intravenously using high-pressure injector with a dose of 0.10 mmol/kg combined with 20 mL of saline at a flow rate of 2 mL/s. Arterial phase images were captured using fluoroscopic trigger method. Patients were instructed to hold their breath before collection, and images were acquired in arterial, portal and delay phases.

Tumor viability assessment

Two radiologists with more than 15 years of experience in abdominal diagnosis independently assessed the tumor viability in multiphase enhanced CT images (group A), multiphase enhanced CT with subtraction images (group B), and multiphase enhanced MRI images (group C). APHE and washout in the portal venous phase were considered as tumor viable (viable or active tumor); the absence of significant enhancement was considered as tumor nonviable (non-viable or inactive tumor); uncertain enhancement was considered as tumor equivocal (uncertain or indeterminate). LR-TR equivocal cases were classified as negative results. True negative cases were defined as nonviable observations which included both LR-TR nonviable and LR-TR equivocal cases. The sensitivity, specificity, accuracy, positive predictive value (PPV), and negative predictive value (NPV) of the three groups were evaluated using the observed tumor viability during TACE treatment as the reference standard.

Diagnostic confidence evaluation

Other two radiologists with more than 20 years of experience in abdominal diagnosis independently evaluated the diagnostic confidence of tumors in the three groups using a 4-point scale (1= insufficient confidence, 2= moderate, 3= good, 4= excellent) (14,15).

TACE treatment

All TACE procedures were performed using Siemens Zee ceiling-mounted angiography system (Beijing, China). Super-selective TACE techniques were used, and during the second intervention, hepatic arteriography was performed first to analyze hemodynamic changes in the hepatic artery/portal vein and observe the deposition of iodized oil in the tumor. The coaxial catheter technique was used to deliver a microcatheter to the tumor-feeding artery, and iodixanol-320 was slowly injected per session to assess the tumor’s blood supply. The angiographic images were independently reviewed by two interventional radiologists (each with >10 years of experience) blinded to all CT and MRI results. Tumor staining (viable) or its absence (nonviable) was recorded. Discordant assessments were adjudicated by consensus with a third senior interventional radiologist (more than 20 years of experience). Residual viable tumors were identified based on the presence of tumor staining, defined as focal, nodular, or mass-like contrast enhancement within the iodized oil deposition area during the arterial phase. A binary classification was used: the presence of staining indicated viability; its complete absence indicated nonviability. Super-selective tumor vessels were embolized using iodized oil chemotherapy emulsion, and gelatin sponge particles was injected slowly via a microcatheter to consolidate the embolization. Post-embolization angiography showed the disappearance of tumor staining and tumor vessels, with deposition of iodized oil in the tumor area.

Statistical analysis

All statistical analysis were performed with SPSS 29.0 software. Cohen’s kappa was used to evaluate the consistency between the two observers in the assessment of tumor viability and diagnostic confidence, with kappa interpreted as follows: 0.00–0.20, 0.21–0.40, 0.41–0.60, 0.61–0.80 and 0.81–1.00 indicated slight, fair, moderate, substantial and almost perfect consistency, respectively. Chi-squared test and Fisher’s exact test were used to compare the sensitivity, specificity, accuracy, PPV, and NPV of the three groups in tumor viability assessment. Kruskal-Wallis test was performed to compare the diagnostic confidence of tumors in the three groups. All test were two tailed, and P value <0.05 was considered statistical significance.

Results

Finally, 99 patients were included in the study, all pathologically confirmed HCC, with a total of 123 tumors (97 tumors larger than 5 mm, 26 tumors smaller than 5 mm), with the maximum diameter ranging from 3 to 78 mm, with an average size of 40±3 mm. This study included 71 males and 28 females, aged between 48 to 75 years, with an average age of 69±5 years (Figure 1).

Figure 1 Study flow chart for patient selection. CT, computed tomography; DSA, digital subtraction angiography; HCC, hepatocellular carcinoma; MRI, magnetic resonance imaging; TACE, transcatheter arterial chemoembolization.

Tumor viability assessment

Both for tumors larger and smaller than 5 mm, two radiologists showed a high level of consistency in tumor viability assessment in the three groups (For tumors larger than 5 mm, kappa of groups A, B and C were 0.88, 0.94 and 0.92, respectively. For tumor smaller than 5mm, kappa of groups A, B and C were 0.77, 0.79 and 0.77, respectively).

For tumors larger than 5 mm, the sensitivity, accuracy and NPV of group B were significantly higher than those of group A (all P<0.05). There were no significant differences in the sensitivity, accuracy and NPV between group B and group C (all P>0.05). The sensitivity, accuracy and NPV of group C were significantly higher than group A (all P<0.05), while the specificity and PPV showed no significant differences among the three groups (all P>0.05) (Table 1). Compared to the group A, the number of tumor equivocal on group B decreased (from 13–14 cases to only 2–3 cases in group B). Besides, the number of tumor equivocal on group B were comparable with those on group C (Table 2) (Figures 2,3).

Figure 2 A 65-year-old male who pathologically confirmed HCC underwent follow-up multiphase enhanced CT and MRI examination. Non-contrast CT images showed iodized oil deposition (A, arrow), and non-contrast MRI images indicated slightly high signal intensity within the tumor (E, arrow). The enhancement of the tumor in the arterial and portal phases of CT and MRI images was unclear (B,C,F,G, arrow). The subtraction images showed no accumulation of iodine contrast agent within the tumor (D, arrow), which was diagnosed as nonviable. DSA showed no staining observed (H). CT, computed tomography; DSA, digital subtraction angiography; HCC, hepatocellular carcinoma; MRI, magnetic resonance imaging.

Figure 3 A 67-year-old male who pathologically confirmed HCC underwent follow-up multiphase enhanced CT and MRI examination. Non-contrast CT showed iodized oil deposition (A, arrow). A slightly enhanced tumor about 15 mm in diameter was observed during the arterial phase (B, arrow), with slight reduction in enhancement during the portal venous phase (C, arrow). On the MRI image (E-G, arrow), patchy enhancement of tumor was observed (F, arrow), but due to the interference from iodized oil within the tumor, it was difficult to determine whether there was abnormal enhancement. The subtraction images showed accumulation of iodine contrast agent within the tumor (D, arrow), which was diagnosed as viable. DSA showed staining observed (H, arrow). CT, computed tomography; DSA, digital subtraction angiography; HCC, hepatocellular carcinoma; MRI, magnetic resonance imaging.

For tumors smaller than 5 mm, the sensitivity, accuracy, PPV and NPV of group B were significantly higher than those of groups A and C (all P<0.05) (Figure 4). The sensitivity, accuracy, PPV and NPV of groups A and C showed no significant differences (all P>0.05), and there was no significant difference in specificity among the three groups (all P>0.05) (Table 3). Compared to the group A and C, the number of tumor equivocal on group B decreased (from 8 cases in group A and C to 1–2 cases in group B) (Table 4).

Figure 4 A 75-year-old male who pathologically confirmed HCC underwent follow-up multiphase enhanced CT and MRI examination. Non-contrast CT showed iodized oil deposition (A, arrow). In the arterial phase, an enhanced tumor about 5 mm in diameter was observed (B, arrow), with a reduction in enhancement during the portal venous phase (C, arrow). This tumor was diagnosed as nonviable on MRI images (E-G); however, the subtraction images showed accumulation of iodine contrast agent within the tumor, which was diagnosed as viable (D, arrow). DSA showed staining observed (H, arrow). CT, computed tomography; DSA, digital subtraction angiography; HCC, hepatocellular carcinoma; MRI, magnetic resonance imaging.

Diagnostic confidence evaluation

The diagnostic confidence was highly consistent between the two radiologists (kappa of groups A, B and C were 0.89, 0.96 and 0.93, respectively). The diagnostic confidence of group B and C were significantly higher than group A (both P<0.05), however the diagnostic confidence of group B was comparable with group C (P>0.05) (Table 5).

Discussion

In this study, we compared the tumor viability and diagnostic confidence of different diameter of tumors in conventional multiphase enhanced CT images, multiphase enhanced CT with subtraction images and conventional multiphase enhanced MRI images and found that the combination of multiphase enhanced CT with subtraction images could significantly improve the sensitivity, accuracy, PPV and NPV in assessing the tumor viability. The significant reduction in the number of tumors categorized as ‘equivocal’ when using subtraction CT serves as an objective indicator of its ability to improve diagnostic certainty. The two radiologists showed a high level of consistency and diagnostic confidence of tumors by multiphase enhanced CT with subtraction images.

Clinically, subtraction techniques have already been applied in assessment of coronary artery stenosis, calcifications can be removed by subtracting the non-contrast CT images from the corresponding enhanced CT images (10,16), and assessment of pulmonary perfusion by iodine distribution within the lung parenchyma (17). However, few studies focused on evaluating tumor viability after TACE treatment in HCC patients by using subtraction techniques.

Many studies shown that HCC was primarily supplied by the hepatic artery, and the arterial phase was the key phase for assessing the tumor viability in HCC patients. Previous studies indicated that APHE is an important indicator for determining the residual tumor viability in HCC patients after TACE treatment (18-20). In this study, we also directly used APHE as the primary criterion for assessing the tumor viability. The results showed that conventional multiphase enhanced CT images have high specificity in assessing the tumor viability, however the sensitivity and accuracy were low. The main reason for these results was the high-density artifacts generated by the iodized oil affected the tumor viability assessment and numbers of tumors were classified as viable by mistake and some tumors were classified as equivocal. Clinically, MRI was used to avoid the influence of high-density artifacts of iodized oil (5,21), however our study showed that for tumors smaller than 5 mm, the sensitivity, accuracy, PPV, and NPV are relatively low. This limitation is primarily due to the slice thickness of MRI (5.0 mm) and the physiological motion artifacts caused by heartbeats and breathing (22,23). Subtraction techniques could remove the high-density artifacts of iodized oil and clearly reveal the viable tumors (24), therefore the combination of multiphase enhanced CT with subtraction images could significantly improve the sensitivity, accuracy, PPV and NPV in assessing the tumor viability. Additionally, the slice thickness of CT images (1.0 mm) allowed assessment of small tumors (25).

Huh et al. (15) demonstrated that adding subtraction images to conventional multiphase enhanced CT images improved the sensitivity and diagnostic confidence in assessing tumor viability. Our study further explored the diagnostic performance based on tumor diameter. Besides, our study further compared the multiphase enhanced CT with subtraction images to conventional multiphase enhanced MRI images and found that for small tumors, the multiphase enhanced CT with subtraction images could improve the diagnostic performance in tumor viability assessment. Additionally, we used the observed tumor viability during TACE treatment as the reference standard for assessing tumor viability (26), so our results were accurate and reliable.

This study has some limitations: (I) this is a retrospective, single-center study; (II) the sample size is relatively small, which may limit the generalizability of the results, and future studies should expand the sample size; (III) this study only included TACE treatments using iodized oil chemotherapy emulsions, which is the traditional locoregional treatment (LRT). Further studies should explore diagnostic performance in new treatment methods in the future; (IV) 1.5T MRI, a 5-mm slice thickness, and an extracellular contrast agent (gadobutrol) does not reflect contemporary optimal liver MRI practice, which often employs 3T systems, thinner slices (≤3 mm), and hepatobiliary-specific agents (e.g., gadoxetic acid). These technical factors likely contributed to the suboptimal performance of MRI, particularly for small lesions, and may have underestimated its potential diagnostic capability.

Conclusions

In conclusion, compared to conventional multiphase enhanced CT and multiphase enhanced MRI images, the combination of multiphase CT with subtraction images may improve the diagnostic performance in evaluating the efficacy of TACE-treated HCC patients. These findings warrant further validation in larger, prospective, and multi-center studies.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STARD reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2679/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2679/dss

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2679/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Ethics Committee of Qingdao University Affiliated Qingdao Third People’s Hospital (No. 2023Y111552). Informed consent was waived in this retrospective study.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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