Journal of Cancer Research and Therapeutics

ORIGINAL ARTICLE
Year
: 2020  |  Volume : 16  |  Issue : 5  |  Page : 1151--1156

Magnetic resonance imaging-guided microwave ablation of hepatic malignancies: Feasibility, efficacy, safety, and follow-up


Nannan Yang1, Ju Gong1, Linyan Yao1, Chen Wang2, Jun Chen2, Jiangwen Liu2, Zhongmin Wang3, Jian Lu1,  
1 Department of Radiology, Ruijin Hospital/Luwan Branch, School of Medicine, Shanghai Jiaotong University, Shanghai, China
2 Department of Vascular and Interventional Radiology, The Third Affiliated Hospital, Shihezi University, Xinjiang, China
3 Department of Radiology, Ruijin Hospital/Luwan Branch, School of Medicine, Shanghai Jiaotong University, Shanghai; Department of Vascular and Interventional Radiology, The Third Affiliated Hospital, Shihezi University, Xinjiang, China

Correspondence Address:
Zhongmin Wang
Jian Lu, Jiangwen Liu, Department of Radiology, Ruijin Hospital/Luwan Branch, School of Medicine,Shanghai Jiaotong University, Shanghai; Department of Vascular and Interventional Radiology, The Third Affiliated Hospital, Shihezi University, Xinjiang
China

Abstract

Context: Percutaneous image-guided thermal ablation has emerged as a valuable therapeutic approach for hepatic malignancies. Magnetic resonance imaging (MRI) has shown potential for great soft-tissue resolution and multiplanar capabilities in arbitrary imaging planes, which are also critical for treatment planning, targeting, and evaluation. Aims: The aim of this study was to investigate the feasibility, technical success, safety, and follow-up of hepatic malignancies treated with MRI-guided microwave ablation (MWA). Materials and Methods: MRI-guided MWA was performed in a closed-bore 1.5 T MR system. T1-weighted imaging was used as a monitoring tool during surgery. T2-weighted imaging was performed to obtain an adequate tumor margin, to calculate the tumor size. Multi-b-value diffusion-weighted imaging (DWI) was performed postprocedurally. Enhanced MRI was performed at 4 weeks, to assess the technical success, and every 3–6 months as a follow-up. Results: Twenty-six patients (38 lesions) were enrolled in the study. A primary efficacy rate of 100% was achieved, and no major complications were observed. Two patient cohorts were identified based on lesion size. Six lesions with incomplete circles on reconstructed DWI appeared immediately postprocedure, and persistent hyperintense signals developed into new lesions over the subsequent 6–12 months. Conclusion: MRI-guided ablation is feasible and effective for planning and evaluating MWA in hepatic malignancies. The available clinical data strongly support the advantages of the assessment of tumors through 3D imaging versus routine axial images.



How to cite this article:
Yang N, Gong J, Yao L, Wang C, Chen J, Liu J, Wang Z, Lu J. Magnetic resonance imaging-guided microwave ablation of hepatic malignancies: Feasibility, efficacy, safety, and follow-up.J Can Res Ther 2020;16:1151-1156


How to cite this URL:
Yang N, Gong J, Yao L, Wang C, Chen J, Liu J, Wang Z, Lu J. Magnetic resonance imaging-guided microwave ablation of hepatic malignancies: Feasibility, efficacy, safety, and follow-up. J Can Res Ther [serial online] 2020 [cited 2020 Dec 4 ];16:1151-1156
Available from: https://www.cancerjournal.net/text.asp?2020/16/5/1151/296419


Full Text



 Introduction



In patients for whom partial hepatectomy alone is not an option because of anatomical or functional reasons, percutaneous image-guided thermal ablation has emerged as a valuable therapeutic approach that is used either alone or in combination with partial hepatectomy. It has been officially included in the treatment guidelines over the last decade,[1] especially in patients with recurrent colorectal liver metastasis (CRLM).[2] Microwave ablation (MWA) features a higher temperature, faster ablation time, larger ablation zones, and lower susceptibility to heat sink than radiofrequency ablation (RFA). Therefore, MWA may be preferable to RFA, especially for tumors ≥3 cm in diameter or those located close to large vessels, regardless of size.[3],[4]

An ideal imaging modality that can be used for ablation procedures must meet several requirements. One requirement is the reliable visualization of the target tumor and the accurate delineation of critical anatomical structures adjacent to the target area for preoperative planning. Ultrasound (US) and computed tomography (CT) are the most common image-guidance techniques used in clinical practice because of their widespread availability and low cost, despite their relatively poor soft-tissue contrast. Regarding lesions <1 cm, a common CT scan shows poor positivity; however, contrast-enhanced imaging is restricted to a short time window for adjustments during operation. Other requirements include the reliable visualization of the applicator, the possibility of real-time imaging, multiplanar capabilities, and a reliable margin assessment of ablation zones.[5]

Over the last decade, magnetic resonance imaging (MRI) has shown potential for great soft-tissue resolution and multiplanar capabilities in arbitrary imaging planes, which are critical for treatment planning, targeting, and evaluation. Moreover, neither the patient nor the operator has to be exposed to radiation.

Therefore, in this study, we aimed to investigate the feasibility, technical success, and safety of MRI-guided MWA for the treatment of hepatic malignancies, and we discuss the advantages of 3D imaging with respect to planning and follow-up.

 Materials and Methods



This retrospective study was approved by the local ethics committee, which waived the requirement for written informed consent.

Patient cohort

Between August 2015 and February 2019, 26 patients (38 lesions) were enrolled in the study. Routine MRI included T1-weighted imaging (T1WI), T2-weighted imaging (T2WI), multi-b-value diffusion-weighted imaging (DWI), and enhanced MRI, which were performed before treatment and during the follow-up (range, 3–36 months). A summary of the details of these modalities is provided in [Table 1], and the parameters used are provided in [Table 2]. The endpoints of this study were death or disease recurrence.{Table 1}{Table 2}

Ablation procedure

Magnetic resonance imaging equipment

All MR procedures were performed using a closed configuration 1.5 T Avanto MR unit (Siemens, Germany) with a bore size of 60 cm.

Microwave ablation equipment

A microwave delivery system (FORSEA; Qinghai Microwave Electronic Institute, Nanjing, China) was used in all studies. This system consisted of an MTC-3 microwave generator with a frequency of 2450 MHz. A steady-flow pump (BT01-100 LanGe-Pump; LanGe Steady Flow Pump, Baoding, China) was used to push the chilled saline solution circulating with the lumina of the antenna shaft at 50–60 ml/min.

Ablation technique

(1) Baseline images (T1WI/T2WI/DWI) were obtained to visualize the target tumor, and the percutaneous entry route was chosen based on lesion size, morphology, location, adjacent structures (especially vessels), and access route. A T1WI-volumetric interpolated breath-hold examination was chosen as the monitoring sequence for quick assessment during surgery; if the lesion was not visible, anatomical landmarks and DW images were used. After localization, T2WI was performed to obtain an adequate tumor margin to calculate the tumor size, and 3D images were obtained to measure the path length needed. (2) MWA was performed under local anesthesia with 1% lidocaine, and conscious-sedation analgesia was induced through the intravenous administration of 0.1 mg of tramadol. An ablation power of 60 W/5 min was set for lesions <1 cm in size, and a higher power (60–80 W) and longer time (5–15 min) were set according to the size of the lesion. To prevent possible tumor seeding, the needle track was cauterized for 10 s when withdrawing the antenna. All needle insertions were performed by two attending interventional radiologists with 10 years of percutaneous biopsy and ablation experience.

Feasibility and technical success

The feasibility evaluation included the successful and reliable detection of the target tumor without contrast agent, tumor delineation under MRI during targeting, and monitoring. Technical success was defined as a successful performance of the ablation procedure as initially intended, as well as the achievement of a coagulation zone covering the target tumor with a safety margin (>5 mm) at the end of the intervention. T2WI/multi-b-value DWI was performed postprocedurally to evaluate technical success.

Technique efficacy

Technique efficacy was evaluated on contrast-enhanced MR follow-up imaging performed 4 weeks after ablation. The complete ablation of macroscopic tumors was defined as a primary technique efficacy, which was assessed by two senior radiologists. Symptoms that occurred within 1 month after treatment were considered treatment-related complications.

Safety

The safety evaluation was based on procedure-related complications according to the clinical practice guidelines of the Society of Interventional Radiology.

Data analysis

The data were analyzed using SPSS for Windows version 17.0 (IBM, Chicago, IL, USA).

Follow-up protocol

The first T1WI/T2WI/multi-b-value DWI postprocedural control imaging was scheduled between 3 days and 1 week after the procedure, together with enhanced MRI imaging, followed by subsequent imaging every 3 months. Local tumor progression (LTP) was defined as the appearance of tumor foci at the edge of the ablation zone after at least one contrast-enhanced follow-up study had documented adequate ablation, together with an absence of viable tissue in the target tumor and the surrounding areas, as assessed using imaging criteria.

 Results



Patient cohort and ablation procedures

Patients were followed up by MRI until February 2019 (follow-up: 17.5 ± 10.3 months; range: 3–36 months). Two patient cohorts were defined according to the applied power, which was 60 W/5 min for lesions <1 cm and higher for other lesions. The details are provided in [Table 3].{Table 3}

Feasibility and technical success

All lesions in our study were clearly observed on DWI, and 30 lesions were delineated by T1WI. In eight lesions with blurred delineation, nearby vessels and the bile duct were used to help locate the target [Figure 1]. As all tumors were completely ablated, the ablation rate was 100%.{Figure 1}

Most patients complained of Grade 1 intraprocedural pain (NCI Common Toxicity Criteria) in the upper abdomen, which stopped immediately after the end of the ablation procedure. Grade 1 postprocedural pain was observed in 61.5% (16/26) of the patients after ablation; this pain usually resolved within 1 week. No skin burns, tumor seeding, or treatment-related death was observed. No mortality or major complications occurred as a result of the procedures.

Technique efficacy

Follow-up imaging at 4 weeks after the ablation procedure demonstrated a primary efficacy rate of 100%.

Safety

No major complications were observed in our study.

Magnetic resonance imaging findings

All images were assessed by two senior radiologists. In the planning, 78.9% (30/38) of the lesions were observed with unenhanced T1WI, whereas DWI showed all lesions. All lesions showed a clear margin with complete hyperintensity on T1WI-enhanced MRI (ranging from 1 to 4 weeks after ablation). Six lesions in the patient cohort with lesions >1 cm showed incomplete circles on 3D-visualized DWI immediately after the procedure, and persistent hyperintense signals were recorded between 3 days and 1 week after the ablation. LTP developed within 6–24 months postoperatively [Figure 2]. Two patient cohorts were identified based on lesion size. In the lesion ≤1 cm group, the tumor size was 0.67 ± 0.2 cm and the applied energy was 18 kJ. The ablation zone showed a mean long-axis diameter (LAD) of 3.24 ± 0.79 cm and a mean short-axis diameter (SAD) of 1.9 ± 0.65 cm, with a sphericity index (SI; SI = SAD2/LAD2) of 0.43. In the lesion >1 cm group, the tumor size was LAD 2.37 ± 1.29 cm, SAD was 1.9 ± 0.65 cm, SI was 0.42 ± 0.2, the energy was 18–48 kJ, and the ablation zone was 4.72 ± 1.11 cm.{Figure 2}

 Discussion



As a 100% primary efficacy rate was achieved and no major complications were observed, we consider that MR guidance is a safe and effective treatment for hepatic malignancies. The data strongly support the advantages of 3D-visualized MRI tumor assessment over assessment based on routine axial images for precise planning, targeting, and evaluation.

Lesion detection is the first important and challenging part of thermal ablation in liver malignancies. Nonenhanced MRI offers a repeatable visualization of the tumor tissue and the ablation zone.[6] US and CT are the most frequently used imaging modalities in clinical practice because of their widespread availability and low cost, despite their relatively poor soft-tissue contrast. In particular, for lesions under 1 cm, a common CT scan shows poor positivity, whereas contrast-enhanced imaging provides a short time window for adjustments during the operation. Lesions abutting the diaphragm and capsule are generally nonvisualized or conspicuous through ultrasonography. In our study, 78.9% (30/38) of the lesions were observed with unenhanced T1WI, whereas DWI showed all lesions.

Nevertheless, T1WI was chosen as the guiding sequence because of its higher spatial resolution and signal-to-noise ratio and shorter acquisition time. In the liver, DWI data quality is limited because of signal variations caused by respiratory and cardiac motion and because of low signal-to-noise ratios. Thus, DWI was performed only at the end of the ablation procedure for confirmation. The surrounding vessels and bile duct helped locate the tumor, with 100% target area coverage. Even the applicator showed a clearer delineation on T2WI, but it was excluded because it is relatively time-consuming.

Access path planning is another important and challenging part of thermal ablation. Typically, access path planning comprises the target area and the skin entry point in 2D image slices, such as those obtained using US or CT. The organs surrounding the tumor margin and access route are identified through visual inspection by the clinician, which is sometimes cumbersome and nonobjective. This method has serious shortcomings that are partially related to the personal experience of the operator. Image fusion (US/CT, US/MRI) may lead to good results. Unfortunately, it is not easy to obtain DICOM imaging data, and a lack of reliable software remains a problem in certain circumstances. Several studies have demonstrated that the visualization approach may allow a better judgment of the distance of the selected path to the risk structures compared with the 2D image.[7],[8] 3D visualization techniques facilitate scientific preoperative decisions, real-time intraoperative navigation, and objective postoperative evaluation for MWA surgery. In our study, 3D visualization based on T1WI imaging was used to aid access path planning. All operations were carried out as planned [Figure 1].

Thus, the MRI and 3D visualization techniques provide a feasible and reliable choice for planning and targeting MWA, especially for lesions that are too small to be detected by US or CT.

An accurate margin assessment is considered a critical parameter of local ablation efficacy. Usually, a safe margin (>5 mm) is required for achieving the optimal treatment outcome.[9] However, it is difficult or impossible to plan the 3D diameter of the ablation zone before the operation because of the lack of clinical data on the applied energy and the volume of the ablation zone. Therefore, the assessment of coagulation tissue during the procedure was important for achieving technique success. However, on a CT scan, the tumor, ablation zone, and surrounding inflammatory area appear as hypodense tissue of similar density, even with contrast agents, making it difficult to define coagulated tissue and a precise margin. A preregistration system may improve the present situation,[10] although it still requires a custom system and radiation exposure. In contrast, a signal switch from T1W hypointense to T1W hyperintense indicates successfully ablated tissue. The switch occurs almost immediately during energy application, which allows the size of the ablation zone to be monitored instantaneously. In animals, MRI has the ability to map dynamic changes in the ablation area clearly and accurately, not only regarding the size and border but also regarding histological features.[11] Paradoxically, in patients, MWA shows a higher percentage of ill-defined perilesional enhancement compared with RFA and cryoablation,[12] which is mostly because data on animals are based on normal liver parenchyma without tumor lesions and underlying liver disease. Kaye et al. suggested that the volumetric semi-automated 3D assessment of the ablation zone in the liver can improve the accuracy of 2-year long-term prediction following RFA of CRLM.[13] A complete hyperintense circle is usually thought to represent solidified tissue, and as a reliable marker, it is suggested to have technical success. In our study, however, all lesions showed a clear margin with complete hyperintensity on T1WI-enhanced MRI (ranging from 1 to 4 weeks after ablation) and no LTP at the 3-month follow-up. Six lesions with incomplete circles on 3D-visualized DWI immediately postprocedure, as well as persistent hyperintense signals, were recorded between 3 days and 1 week after ablation [Figure 2]. All of them developed LTP within the next 6–24 months. In contrast, only 33% (2/6) of the recurring lesions were observed in the traditional axial images then, 1 of which was mistaken as an interlayer spacing artifact.

The inflammatory response receded and ultimately disappeared in 2 weeks, as reflected by a signal becoming hypointense over time on T2WI, decreased enhancement on T1WI, and fibrosis of the 4-week inflammatory zone, shown as a clear circular margin on enhanced T1WI. Thus, a reliable follow-up MRI was usually performed at 4 weeks after ablation. DWI is designed to reflect molecular diffusion by MRI. Different gradient durations and amplitudes combined with b-values can be used to measure the rates of the diffusion of microscopic water within tissues, which may reflect cellularity. Completely necrotic lesions lose their cellularity, develop coagulation necrosis, and contain few diffusion barriers. Several models based on multi-b-value DWI, such as diffusion kurtosis imaging (DKI) and intravoxel incoherent motion, were designed to evaluate the early treatment response. Few studies have addressed the use of multi-b-value DWI in MWA therapy, whereas in other thermal therapies, such as high-intensity focused ultrasound (HIFU), DWI with different b-values can be useful for treatment evaluation, as low b-values seem to be the best choice to emphasize perfusion effects after MR-HIFU.[14] DWI has also been reported to have the ability to detect intraprocedural changes in ex vivo muscle with HIFU bone treatments.[15] DKI with three or more b-values can be used as an independent predictor of the recurrence of early-stage single hepatocellular carcinomas treated with RFA.[16] Thus, 3D-visualized DWI performed 3–7 days after ablation may have the potential to predict tumor residue or LTP in the ablation zone at the early stage. Further data are required to reveal the association between microstructural changes and signals on multi-b-value DWI in the early stage after ablation.

Most liver tumors treated with MWA are spherical, and a spherical ablation zone is required to achieve a sufficient ablation margin. However, most ablation systems create ellipsoidal ablation zones with poor sphericity values. However, the sharp volume changes observed in different liver parenchyma states and vessels hinder their clinical application. Reports including clinical data are scarce; thus, standard reports describing ablation experiments should be encouraged.[17] An ablation power of 60 W/5 min was set for lesions <1 cm in size, whereas additional treatment and/or a higher power were set for larger lesions. In the 60 W/5 min group, the ablation zone showed a mean LAD of 3.24 ± 0.79 cm and a mean SAD of 1.9 ± 0.65 cm. When combined with previous data, the results were 3.5 ± 0.55 cm and 2.0 ± 0.32 cm, respectively.[18]

Blood vessels are another major cause of insufficient ablation margin. Kim et al. reported that blood vessels were associated with 50.5% (48/95 cases) of insufficient ablation margins in lesions >2 cm and <5 cm.[19] Seven lesions located beside large vessels (three beside the right hepatic vein, three beside the right portal vein, and one beside both) were enrolled in our study. All vessels showed a clear margin on both T1WI and 3D visualization imaging, which facilitated the development of a thoughtful plan. No LTP occurred during the 6–12-month follow-up. No vessel injuries, such as thrombosis, occurred, consistent with previous reports.

Based on these results, we consider MR-guided percutaneous tumor ablation a feasible, safe, and accurate approach for the treatment of hepatic tumors, and the available clinical data strongly support the advantages of 3D-visualized tumor assessment over assessment based on routine axial images, which requires the reliable visualization of the target tumor and of the applicator throughout the entire ablation procedure.

Our study had several limitations. Given the sample size, a meaningful subanalysis was not feasible. Thus, we chose to combine primary and secondary hepatic malignancies. However, the combined survival analysis may be clinically questionable, which was not discussed in this study. Further studies are required to reveal the association between microstructural changes and signals on multi-b-value DWI in the early stage after ablation.

 Conclusion



There is growing evidence supporting the use of MRI for diagnostic and follow-up purposes in patients with liver cancer treated with local-regional therapies. First, we successfully performed MWA under MR guidance both safely and efficiently. 3D visualization has provided novel and precise information for evaluation and follow-up. Furthermore, DWI shows a potential ability to evaluate changes in the ablation area in the early stage. In conclusion, the benefit of 3D visualization assessment over existing techniques lies in its ability to provide complete tumor information that is pathologically more accurate and representative. The available clinical data strongly support the advantages of 3D-visualized tumor assessment over assessment based on routine axial images.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

This work was supported by the Project of Medical Key Specialty of Shanghai Municipal Health Commission (No. ZK2019A02) and Shanghai Municipal Health Commission (General Program No. 201840058) and the Project of Science and Technology Project of Huangpu District Science and Technology Commission (No. HKW201603) (No. 2019GG04, HKW201603). Clinical key specialist construction project of Shanghai municipal health commission (Interventional Radiology [No. shslczdzk06002] & 3D Printing [No. shslczdzk07002].

Conflicts of interest

There are no conflicts of interest.

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