Predictive Value of Ablative Margin Assessment After Microwave Ablation for Local Tumor Progression in Medium and Large Hepatocellular Carcinoma: Computed Tomography–Computed Tomography Image Fusion Method Versus Side-by-Side Method : Journal of Computer Assisted Tomography

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Abdominopelvic Imaging: Gastrointestinal

Predictive Value of Ablative Margin Assessment After Microwave Ablation for Local Tumor Progression in Medium and Large Hepatocellular Carcinoma: Computed Tomography–Computed Tomography Image Fusion Method Versus Side-by-Side Method

Zhou, Hongyu MS∗,†; Yang, Guanghao MS; Jing, Xiang BS∗,†; Zhou, Yan MD∗,†; Ding, Jianmin MD∗,†; Wang, Yandong MS∗,†; Wang, Fengmei MD∗,†; Zhao, Lei MS

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Journal of Computer Assisted Tomography 47(1):p 31-37, 1/2 2023. | DOI: 10.1097/RCT.0000000000001395
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Abstract

Thermal ablation is now considered a curative treatment for small hepatocellular carcinoma (HCC) (<3 cm),1–3 and it is also an effective treatment for medium (3–5 cm) and large liver cancer (>5 cm).4,5 For lesions smaller than 2 cm, thermal ablation, including radiofrequency ablation and microwave ablation (MWA), has a comparable long-term outcome, namely, progression-free survival and overall survival rates, to liver resection.6 The local tumor progression (LTP) rate (the incidence of disease progression among all patients) is higher in HCC (>2 cm) patients receiving thermal ablation therapy than in those treated with surgery; attainment of safe margins and tumor diameter are important influence factors for LTP.7–11 With increasing tumor volumes, the technical difficulty in treatment increases, requiring multiple antenna placement to compensate for a geometric increase in ablation volume. Irregular tumor growth further increases the difficulty of antenna placement, resulting in an increased risk of residual tumor and decreased therapeutic efficacy.12 The LTP rates were reported to range from 2% to 58.1%7–10; Ablative margin (AM) is another important factor affecting LTP; AM has been conventionally assessed through side-by-side comparison of computed tomography (CT)/magnetic resonance imaging (MRI) images before and after ablation. A new approach, which fuses preablation and postablation CT images to combine HCC and the ablation zone, has been reported to be accurate for assessing the size of AM.11 It has been demonstrated that the 3-year LTP for patients with AM >5 mm, evaluated by CT-CT fusion image, was 4.1%, which was much less than that of patients with AM <5 mm (35.1%).11 There are few studies to compare the 2 AM assessment methods in predicting LTP. This study aims to compare the predictive value for LTP of the conventional side-by-side method and the CT-CT image fusion method and to explore factors affecting LTP.

MATERIALS AND METHODS

Patients

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. This is an observational study. The Third Central Hospital of Tianjin Research Ethics Committee has confirmed that no ethical approval is required. Patient consent for the study was waived, as it was retrospective and anonymized.

A total of 2357 patients who were admitted to our hospital from January 2010 to December 2019 and received percutaneous MWA therapy in our central were included in this study. Seventy-one patients meeting the following inclusion criteria were enrolled in this retrospective study: (1) with pathologically confirmed HCC through core needle biopsy; (2) with a first-onset, single lesion with a maximum diameter ≥3 cm; (3) with the liver function of Child-Pugh classification A or B; (4) without treatment before MWA of HCC; (5) with complete contrast-enhanced computed tomography (CECT) data within 2 weeks before therapy and 1 month after therapy, and complete follow-up data; and (6) with complete ablation of the lesion 1 month after MWA therapy according to the CECT findings. The exclusion criteria were the following: (1) with lesion <3 cm or multiple lesions, (2) undergoing MWA without pathologically confirmed HCC, (3) with recurrent HCC, (4) underwent MWA combined with other treatments, (5) without CECT data within 2 weeks before or within 1 month after ablation, and (6) with incomplete ablation. Flow chart of patients included in this study is shown in Figure 1.

F1
FIGURE 1:
Flow chart of the study.

MWA Procedure

Microwave ablation was performed using an microwave tissue coagulation-3 microwave therapy instrument (Forsea Microwave & Electronic Research Institute, Nanjing, China) with a frequency of 2450 MHz and an output power of 40 to 80 W. The microwave antenna was a 16-gauge monopolar needle (15-cm long) with a circulating cooling system.

All MWA procedures were performed by a single physician with more than 11 years of experience in thermal ablation therapy. Microwave electrodes were inserted under ultrasound guidance. Treatment with the microwave device was performed at an output power of 60 to 80 W. According to the tumor shape, size, and position, multipoint overlapping ablations were developed based on the principles of multipoint puncture, multiple antennae, and multipoint ablation. Particularly, placement of the electrode was based on mathematic models. For example, 4 ablation points were needed for 4.0-cm lesions and 6 ablation points were needed for 5.0-cm lesions. When we finished 1 targeted site, the electrode tip was inserted 1.5 to 2.0 cm proximal to above site.13

The strategy of percutaneous ablation of tumor supplying artery before tumor ablation was used for hypervascular HCC.14 Water was injected in the abdominal or thoracic cavity as an auxiliary approach for tumors adjacent to the stomach, intestine, and other important organs, or those located at the top of the liver.15 Water injection in the gallbladder bed was performed as an auxiliary approach for tumors adjacent to gallbladder. Conventional parallel vascular supplementary ablation was performed for tumors adjacent to blood vessels. Whenever possible, the ablation zone covered the tumor and normal liver tissues up to 0.5 cm to 1.0 cm surrounding the tumor.

CT Image

Contrast-enhanced computed tomography was performed using the Somatom Definition Flash dual-source CT scanning device (Siemens Healthineers, Forchheim, Germany). Iohexol (350 mg/mL; Beijing Beilu Pharmaceutical Co, Ltd) as the contrast agent was injected through the median cubital vein at 3.5 mL/s and 1.2 mL/kg by using a high-pressure syringe. Triple-phase dynamic CECT imaging was performed at 25 to 35 seconds, 60 to 70 seconds, and 180 seconds after the contrast agent injection. The scanning parameters were as follows: tube voltage, 120 kV; reference tube current, 210 mAs; collimation, 64 × 0.6 mm; pitch, 0.8:1; slice thickness, 1.0 mm; slice gap, 1.0 mm; and matrix, 512 × 512. The patients were in the supine position, and the scan range was from the diaphragmatic dome to the lower poles of both kidneys.

The Side-by-Side Assessment Method

A doctor with 10 years of experience in radiology measured the size of the tumor on pretreatment CT images and the ablation zone on posttreatment CT images, slice by slice, and calculated the minimum distance between the 2 boundaries as minimum ablative margin (min-AM).

CT Image Fusion

Image fusion was performed with a color ultrasound diagnostic apparatus of Philips EPIQ7 with the PercuNav 5.5 (Philips, WA) by a physician with >5 years of experience who was unaware of the treatment details and follow-up results. One CECT thin-slice sequence each, obtained before and after therapy, which clearly displayed the lesion/ablated lesion and the intrahepatic vessels (portal or hepatic veins), was selected. The patients' CT data were imported into the PercuNav system in Digital Imaging and Communications in Medicine format via a USB flash driver. The system simultaneously displayed the multiplanar reconstruction of both CT images, namely, the axial, coronal, and sagittal planes. Three anatomical landmarks around the region of interest that were visible in both CT images were used for a paired-point rigid registration method. Considering the effects of tissue contraction on imaging fusion, the target registration error (TRE)16 was used as an indicator of quality central. Particularly, TRE was defined as the distance of another anatomical landmark around the region of interest visible in both CT images. The registration was considered successful if the TRE was below 3 mm, whereas the registration was considered failed after this criterion was not met after 3 attempts; the time required for fusion imaging was recorded.

After successful fusion, registration, and superimposition, the boundary of the tumor on pretreatment CT images and the boundary of the ablation zone were manually contoured layer by layer, and the shortest distances between the 2 boundaries were measured in the axial, coronal, and sagittal planes. Then, the center of the lesion was used as the origin, and the lesion was divided into 8 quadrants according to the axial, coronal, and sagittal planes passing through the origin. The min-AM and its position were recorded. Lesions adjacent to major blood vessels (<5 mm) were recorded.

Based on the tumor coverage by the ablated lesion and the min-AM value, the lesions were divided into 3 groups: min-AM <0 mm (group I, incomplete coverage of tumor by ablated lesion), 0 mm ≤ min-AM <5 mm (group II), and min-AM ≥5 mm (group III).

Follow-up

All patients were followed up regularly after ablation therapy to evaluate. Particularly, for ablation efficacy, all patients underwent CECT at 1 and 3 months after therapy to determine the therapeutic efficacy, followed by ultrasound or contrast-enhanced ultrasound and tumor marker examinations every 2 to 3 months and CECT/MRI every 6 months. Complete ablation was defined as no enhancement of the tumor at 1 month after therapy on CECT/MRI. Local tumor progression was defined as nodular or annular tumor reoccurrence at the edge of the ablation zone after complete ablation of the tumor, hyperenhancement in the arterial phase on CECT/MRI, washout in the portal venous phase or delayed phase, or a confirmed pathological diagnosis.17,18 The follow-up of all patients was completed in December 2020. All patients were followed up for 5 to 128 months after therapy.

Statistical Analyses

The SPSS version 22.0 software (IBM, Armonk, NY) was used for statistical analysis. Quantitative data were represented as mean ± SD, whereas categorical variables were represented as frequencies. The χ2 test or Fisher exact test was used for qualitative data, and the Kaplan-Meier method was used to calculate the LTP rate. The κ coefficient was calculated to assess the degree of agreement between the AM data of CT- CT image fusion assessment and side-by-side assessment (κ = 0, no agreement; 0–0.20, slight agreement; 0.2–0.4, fair; 0.4–0.6, moderate; 0.6–0.8, substantial; 0.8–1, excellent). A total of 10 factors, including sex, age, Child-Pugh classification of liver function, maximum lesion diameter, α-fetoprotein concentration, number of lesions adjacent to blood vessels, number of subcapsular lesions, HCC differentiation, min-AM from CT-CT image fusion assessment, and min-AM from side-by-side assessment were included in Cox regression. The Cox proportional hazards regression analysis was used to investigate the factors affecting LTP. A P value of <0.05 was considered to indicate a statistically significant.

RESULTS

Basic Clinical Features of the Patients Enrolled in the Study

A total of 71 patients with 71 lesions were enrolled in this study. The fusion of CT images was successful for 69 lesions (69 of 71 [97.2%]). The fusion of 2 lesions failed because of obvious changes in the local anatomical structure after therapy caused by tissue contraction effects after therapy.

The time spent on image fusion and safety margin assessment for single lesions ranged from 9 to 19 minutes, averaging 12.7 ± 2.3 minutes. Pathological diagnosis was obtained through core needle biopsy before ablation, and the basic clinical features of all patients are shown in Table 1. All patients were followed up from 5 to 128 months.

TABLE 1 - Basic Clinical Features of the Patients Enrolled in the Study
Clinical Features Value Percentage
Patients 71
Mean age, y 57.0 ± 10.3
Sex
 Male 52 73%
 Female 19 27%
Etiology
 HBV 63 89%
 HCV 3 4%
 Alcohol 3 4%
 Other 2 3%
AFP, ng/mL 191 ± 358
Child-Pugh class
 A 64 90%
 B 7 10%
Maximum lesion diameter, mean ± SD, cm 4.0 ± 1.1
Maximum lesion diameter range, cm 3.0–8.5
No. lesions adjacent to blood vessels 32
Min-AM close to blood vessels in the group with lesions adjacent to blood vessel
 Yes 27 84%
 No 5 16%
AFP, α-fetoprotein; min-AM, minimal ablative margin; HBV, hepatitis B virus; HCV, hepatitis C virus.

The Cumulative LTP Rates of Patients Over 1, 3, 5, 7, and 10 Years

Local tumor progression was found in 20 patients, and LTP was located at min-AM on fused CT images in 17 patients (coincidence rate, 17 of 20 [85%]) (Fig. 2). The LTP time was 5 to 66 months. The cumulative LTP rates of patients over 1, 3, 5, 7, and 10 years were 10.3%, 29.6%, 33.0%, 38.1%, and 38.1%, respectively (Fig. 3).

F2
FIGURE 2:
A male patient aged 73 years, with HCC in liver segment IV: (A) fusing image shows that the AM is 0 mm (black arrowhead); (B) CECT before ablation shows an HCC with a size of 5.3 cm × 4.2 cm; (C) CECT at 1 month after ablation shows that the lesion was ablated completely; and (D) at 2 months after treatment, the local progression (black arrowhead), consistent with the position of min-AM from CT-CT image fusion, is founded by CECT. Figure 2 can be viewed online in color at www.jcat.org.
F3
FIGURE 3:
The cumulative LTP rates of patients over 1, 3, 5, 7, and 10 years were 10.3%, 29.6%, 33.0%, 38.1%, and 38.1%, respectively.

The AM Assessment

The AM data of CT-CT image fusion assessment and side-by-side assessment are shown in Table 2.

TABLE 2 - The AM Data of CT-CT Image Fusion Assessment and Side-by-Side Assessment
CT-CT Image Fusion I II III Total (%) LTP (%)
Side by side
 I 1 1 0 2 (2.9) 1 (50.0)
 II 6 23 0 29 (42.0) 9 (31.0)
 III 6 25 7 38 (55.1) 10 (26.3)
Total (%) 13 (18.8) 49 (71.0) 7 (10.1) 69
LTP (%) 9 (69.2) 11 (22.4) 0

The κ coefficient for the agreement between the 2 methods was 0.14 (P = 0.028).

Cumulative LTP rate showed a significant difference between groups by min-AM from CT-CT image fusion assessment (P < 0.05), which was decreased as the safety margin increased. No significant difference was observed in cumulative LTP rate between groups by min-AM from side-by-side assessment (P = 0.807). The results are shown in Figure 4.

F4
FIGURE 4:
Comparison of cumulative LTP rates between different min-AM groups by CT-CT image fusion assessment and by side-by-side assessment: (A) CT-CT image fusion; (B) side by side.

The Factors That Could Affect LTP Rate After MWA

Cox regression analysis further showed that, of the 10 analyzed factors, only min-AM by CT-CT image fusion assessment affected LTP (Table 3).

TABLE 3 - Univariate Cox Regression Analysis of the Factors That Could Affect LTP Rate After MWA of Medium and Large HCC
Clinical Features n P
Age (>60/≤60), y 30/41 0.776
Sex (male/female) 52/19 0.598
AFP (>200/≤200 ng/mL) 16/55 0.080
Child-Pugh (class A/B/C) 64/7/0 0.159
Maximum lesion diameter (3–5/5–8.5 cm), cm 59/12 0.313
lesions adjacent to blood vessels (yes/no) 32/39 0.875
subcapsular lesions (yes/no) 24/47 0.249
Min-AM (I/II/III) from CT-CT fusion imaging 13/49/7 0.005
Min-AM (I/II/III) from side by side 2/29/38 0.888
HCC differentiation (high, medium, and low) 53/15/3 0.209
AFP, α-fetoprotein.

DISCUSSION

Thermal ablation has a comparable long-term outcome to liver resection for lesions smaller than 2 cm.6 However, the LTP rate is significantly higher in HCC with size larger than 2 cm in patients receiving thermal ablation therapy than in those treated with surgery, and AM is an important factor affecting LTP.19–21 Imaging performed in ablation therapy assists in decision making and patient management by evaluating the AM and accurately identifying residual tumor to determine if supplementary ablation is indicated. Current studies show that patients with safety margins ≥5 mm have a significantly lower risk of LTP.22 A previous study demonstrated the intraprocedural CECT monitoring of minimal AM. About 18.9% lesions underwent immediate additional ablation to get the sufficient margin by intraprocedural CECT monitoring.23 However, there are some difficulties in evaluating the safety margin using CECT immediately or within 3 days after therapy in clinical practice. For example, the hyperemia of the peripheral ablation zone may hamper the evaluation of AM. Furthermore, CECT examinations have radiation damage and increase the additional financial burdens for patients. Thus, the application of AM evaluation by fusion imaging immediately or within 3 days after therapy is limited in clinical practice.

In clinical practice, CECT examination is often performed 1 month after therapy to evaluate the ablation efficacy and determine whether the lesion is completely ablated. This avoids the influence of liver parenchymal hyperemia and inflammatory response immediately after thermal ablation therapy on the accuracy of detecting ablated lesion residue.24 This study further applied the CT-CT image fusion method and the side-by-side method to evaluate the AM. However, the CECT used in aforementioned procedures was performed 1 month after therapy. On the one hand, the tissue contraction and anatomical distortion 1 month after thermal ablation may result in fusion failure. On the other hand, the AM measured by the side-by-side method and CT-CT image fusion method was different from that measured immediately after ablation. The success rate of image fusion was 97.2%. The time spent on image fusion and safety margin assessment was 12.7 minutes. As suggested by the results, it is feasible, simple, convenient, and efficient to use CT-CT image fusion at 1 month after treatment to assess safety margin.

Our data showed poor agreement between the side-by-side method and the CT-CT image fusion method in assessing AM. As we know, pathological diagnosis is the reference standard for safety margin. However, the acceptability of pathological diagnosis for safety margin is poor in clinical practice. Local tumor progression is an important quantity to verify the accuracy of evaluated AM. The use of LTP can help avoid invasive biopsy. Cumulative LTP rate differed significantly between groups by min-AM from CT-CT image fusion assessment and was decreased as the safety margin increased, suggesting predictive value of this method for LTP. Moreover, 85% of the LTP lesions at min-AM on fused images showed high consistency. Thus, frequent follow-up or additional ablation should be considered when CT-CT fusing images show that the AM was less than 5 mm. There was no significant difference in cumulative LTP rate between groups by min-AM from side-by-side assessment, indicating no predictive value for LTP of the conventional method. Therefore, min-AM from CT-CT image fusion assessment can better predict LTP after MWA than that from side-by-side assessment. Further analysis found that the lesions classified into group I by the image fusion method were commonly distributed in groups II and III by the side-by-side method, and some lesions in group II by the image fusion method were classified into group III by the side-by-side method. The results indicated that the safety margin of the side-by-side method was larger than that of the image fusion method. This is because that the size of ablation zone and tumor was measured in side-by-side procedure and then just subtracted of the diameters of the 2 numbers and it is very difficult to precisely mark the initial tumor boundary in the ablation zone, tending to overestimate the min-AM of eccentrically ablated lesions. In addition, malignant tumors usually grow into an irregular shape, which is especially significant for the tumors ≥3 cm in diameter in this study, imposing a great challenge for doctors to compare pretreatment and posttreatment CT images side by side. Computed tomography-CT image fusion is advantageous in that it precisely overlaps pretreatment and posttreatment images on the basis of anatomical alignment and precisely outlines the initial lesion and ablation zone to produce an accurate measure of the distance between the 2 boundaries. Therefore, compared with the side-by-side method, the CT-CT image fusion method can more accurately assess AM, particularly in eccentrically ablated lesions, and has better predictive value for LTP.

In this study, Cox regression analysis further showed that, of the 10 analyzed factors, only min-AM by CT-CT image fusion assessment affected LTP. However, Jiang et al reported that tumor size and blood vessels adjacent to lesions also influenced LTP.11,25–28 The inconsistency may be explained by the fact that patients involved in this study only includes medium-large HCCs. We analyzed the min-AM of lesions adjacent to blood vessels and found that the min-AM of 84.4% (27 of 32) lesions was located close to blood vessels, which is consistent with studies that reported that lesions adjacent to blood vessels were less likely to have safety margins.29 However, there was no significant difference in the LTP rate between the groups with and without lesions adjacent to blood vessels, which may be related to the conventional parallel vascular supplementary ablation performed during the MWA of lesions adjacent to blood vessels.

The main limitation of our study is that the CECT examination was performed 1 month after therapy; therefore, the degree of lesion reduction was unclear. In local thermal ablation therapy, 5 mm of ablation beyond the lesion is usually considered as the safety margin, which is also used in the evaluation immediately or within 3 days after therapy. In this study, however, only 8.7% (6 of 69) of patients achieved the safety margins of ≥5 mm as shown by CECT 1 month after therapy, which is substantially lower than the value of (10%–77.1%) in recent evaluation reports immediately after therapy.22,25,30 The different results between previous studies and this study may be due to the different techniques and methods to measure the margin. Furthermore, the AM <5 mm at 1 month after therapy was due to the retraction caused by tissue healing and scar formation in the coagulative necrotic zone after ablation. Guibal et al31 reported that the volume of ablation zone reached its maximum at 1 week after ablation and then gradually decreased with time. Cassinotto et al32 found that the ablation zone was reduced by approximately 30% at 1.6 months after radiofrequency ablation. In this study, 10 years of regular follow-up showed that the cumulative LTP rates at 1, 3, 5, 7, and 10 years were 10.3%, 29.6%, 33.0%, 38.1%, and 38.1%, respectively. These values were similar to the report,22 suggesting that a sufficient safety margin of ablation was achieved in most lesions. Second, further studies are required to investigate whether our conclusions on large HCCs can be extended to small HCCs.

CONCLUSIONS

It is feasible to personalize follow-up for patients with HCC by using contrast-enhanced CT images 1 month after ablation to assess ablation efficacy and safety margin and predict LTP. Compared with the side-by-side method, the CT-CT image fusion method is more accurate in assessing the AM of eccentrically ablated lesions. The min-AM based on CT-CT image fusion assessment is an important influencing factor for LTP.

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Keywords:

microwave ablation; hepatocellular carcinoma; CT image fusion; local tumor progression; ablative margin

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