INTRODUCTION
Sublobar resection or lobectomy with lymph node excision remains the standard treatment for stage I non-small cell lung cancer (NSCLC).[ 1 ] According to statistics, 20% to 25% of lung cancer patients, particularly those with poor cardiopulmonary function, little pulmonary reserve, or advanced age, cannot withstand surgical resection.[ 2 ] Stereotactic body radiation therapy (SBRT) is also an alternative therapy, particularly for inoperable patients of early-stage NSCLC.[ 3 ] While it is important to remember that some individuals who are unable to undergo surgery also make poor SBRT candidates or refuse treatment. Percutaneous image-guided thermal ablation (IGTA) therapy, which includes radiofrequency ablation (RFA), microwave ablation (MWA), cryoablation, and laser ablation, is an effective and yield promising local tumor control technique of NSCLC.[ 4 , 5 ] Among these, MWA has received more study attention because it is a relatively new treatment approach. It is reported that MWA has been a curative strategy for stage I NSCLC patients with a median survival of 64.2 months, and the OS was 54.1% at 5 years.[ 4 ] MWA is a procedure that depends on the experience of the ablationist. The determination of the optimum puncture path and correct ablative parameters influences the efficacy and complications. A precise ablation of lung tumors depends on a well-planned pre-procedure.[ 6 ]
Conventionally, ablationist are needed to manually plan the puncture path of the antenna, and ablative parameters, based on the pre-procedure image like CT or MRI, or ultrasound.[ 7–9 ] However, a well-planned pre-procedure depends on the experience of the ablationist and remains time-consuming. In this study, we design the three-dimensional visualization ablation planning system (3D-VAPS) with a computational model for pre-procedure planning of both the puncture path of the antenna and ablative parameters in MWA of early-stage NSCLC. The purpose of this study was to confirm the viability and safety of 3D-VAPS in MWA of lung tumors.
MATERIALS AND METHODS
Patients and tumors
From May 2020 to July 2022, 113 patients with histologically verified NSCLC who had 120 sessions of CT-guided MWA, were retrospectively analyzed. This study included 58 males and 55 females. The mean age of patients was 65 ± 10.44 years. The mean diameter for these lesions was 1.9 ± 0.4 cm (range 0.9-2.5 cm). Adenocarcinoma (100, 88.49%), squamous cell carcinomas (11, 9.73%), and indeterminate NSCLC (2, 1.76%) were the three most prevalent histological types. The baseline characteristics of patients and tumors were listed in Table 1 . There were 6 inclusion criteria presented as follows: (1) patients age ≥18 years; (2) peripheral tumors; (3) tumors with a maximum diameter:≥5.0 mm and ≤25.0 mm; (4) patients who are medically inoperable, or refusal to surgery as well as SBRT; (5) patients that do not receive systemic therapy or local control before MWA therapy; (6) the score of eastern cooperative oncology group performance status from 0 to 2. The exclusion requirement were as follows: 1) lesions larger than 25.0 mm; 2) severe pulmonary fibrosis and pulmonary hypertension; 3) platelet count <50 × 109
Table 1: Baseline characteristics of patients and tumors
Procedures
3D-VAPS
3D-VAPS (ECO Medical Instrument Co., Ltd. and our team jointly exploited the product) was used for NSCLC patients underwent CT-guided percutaneous MWA to determine the pre-procedure plan. The enhanced CT scanning (DICOM format data) within 15 days before MWA was loaded into the software. (1) verifying the gross tumor region (GTR)[ 10 ] : the lesion was chosen specifically based on target markers such as its location, size, form, and proximity to important anatomical structures. A 3D image of the GTR was developed by the software in the axial, coronal, and sagittal planes. (2) identifying the preferred ablative zone: employing a set of target markers to outline the intended ablative zone, including markers for the body position, pierced sites, puncture path, and “target-skin distance.” The desired ablative zone could overlap and move around GTR, and its range could be adjusted in three dimensions with the computer mouse. Furthermore, based on the desired ablative zone, the antenna inserting angle, puncture path, target-skin distance, and its position within GTR could also be adjusted by the ablationist. With such a strategy, the ideal puncture path can be discovered to prevent harm to vital structures along the puncture path. (3) preliminarily determining ablative parameters: based on the range of the ablative zone and between the minimum and maximum margin covered around GTR, the software calculated the range of power output and duration of MWA treatment. These parameters presented as important references to the ablationst for actual procedure [Figure 1 ].
Figure 1: The application of 3D visualization planning system (3D-VAPS) for CT-guided microwave ablation of stage I non-small cell lung cancer. (a-c) Pre-procedure CT images showing the target tumor with a maximum diameter of 10.0 mm in the left lower lobe of the lung (arrow) in the axial, coronal and sagittal planes. (d) 3D-VAPS displaying the spatial relationship between the lesion and vital organs around, such as the thoracic aorta, left inferior pulmonary vein, pulmonary artery, and heart. (e) 3D-VAPS is depicted on the computer screen, and it entails choosing the lung tumor with the region of interest marker (green circle). (f) The software then produces a three-dimensional image of the lesion. The targeted ablative zone is then shown by the region of interest (red circle) that is positioned around the tumor.(g-h) The software also show the microwave antenna needs to be positioned within the tumor to create this ablative zone and display the spatial relationship between the lesion and vital organs or blood vessels around in three-dimensional image. (i) Intra-procedure CT images showing the microwave antenna positioned within the tumor according to the 3D-VAPS. (j-k) The software shows the microwave antenna to be positioned within the tumor in the coronal and sagittal planes. (l) At the 24-hour follow-up CT, the index tumor was completely covered by ablative zone
Three microwave ablation systems were applied for MWA treatment in this study, including the ECO-100A1 MWA system (ECO Medical Instrument), MTC-3C MWA system (Vison Medical Inc., Jiangsu, China), and KY-2450B MWA system (CANYOU medical). The MWA was carried out under CT supervision (uCT760, United Imaging Healthcare Co., Ltd, Shanghai, China). The frequency of the MWA system was 2450 ± 50 MHz and the output power was between 0 and 100 W. There were several different types of ablation antennas employed, with effective lengths between 100 and 180 mm and outer diameters between 16 G and 19 G. A water circulation cooling system was added to keep the antennas’ surface cool.
Satisfactory anesthesia was essential before the MWA procedure, which include local anesthesia (1%lidocaine) and intravenous anesthesia (sufentanil, 0.25 mg/kg).[ 10 ] Once anesthesia achieved, the procedure is conducted as planned by an ablationist with more than 5 years of experience. Detailed ablation procedures were presented in precious paper.[ 11 ] A chest CT scan was conducted immediately after the MWA operation to assess the post-ablation target zone (PTZ) and complications. To determine whether some typical problems, such as pneumothorax, pleural effusion, chest bleeding, and so forth, had occurred 24 hours later, a second chest CT was performed. Once moderate or larger pneumothorax, as well as pleural effusion, occurred during or after the MWA procedure, insertion of a chest tube is necessary. The International Working Group on Imagine-Guided Tumor Ablation categorized complications into three categories in 2014, as follows.[ 12 ] (1) Major complications: Major complications were considered those clinical symptoms that could cause organic damage or irreversible functional damage, even life-threatening without immediate treatment, and even increase the length of hospital stay and mortality. (2) Minor complications: Patients who received MWA treatment with minor complications did not require hospitalization or had self-limiting disease courses. (3) Side effects: Side effects are normal and, while frequent, seldom result in complications or morbidity. These included pain, post-ablation syndrome, minor asymptomatic hemorrhage, or effusion that could be observed in the CT images.
Follow-up and outcomes
All patients were followed up with a protocol for surveillance imaging including performing contrast-enhanced CT at 1, 2, 3, 6, 9, 12, 18, and 24 months; and every year thereafter. This study followed up on four different types of treatment study goals, including technical success, technique efficacy, complications, and clinical outcomes. About complications of MWA treatment have presented above in the materials and methods part. Technically successful is defined as the tumor that is treated according to protocol and the ablative zone completely covered over the lesion, even the ablative margin beyond the tumor border at least 5.0 mm.[ 12 ] Regarding technique efficacy, we concentrated on the complete ablation rate and local tumor progression in the follow-up of this study. The complete ablation rate indicated the proportion of patients who have complete ablation at some time after MWA. The criteria for evaluating complete ablation are as follows: (1) a clinical disappearance of the targeted tumor; (2) the formation of the cavity completely; (3) no abnormal enhancement showed on the CT scan of the ablated lesion, which was commonly presented as fibrosis, scar, involuted nodule, or even no change.[ 13 ] While incomplete ablation includes any one of the following patterns: (1) partial loss of microwave ablated lesions with cavity formation was found, with some solid parts or liquid components remaining, and the irregular peripheral or abnormal enhancement revealed on CT scan; (2) the residual lesions presented as partial fibrosis with a solid component, but no changed or enlarged solid nodule was shown irregular peripheral or abnormal enhancement on CT scan.[ 13 ] Local tumor progression showed two following patterns: (1) the residual lesions were increased by at least 10.0 mm, with enlarged irregular or internal abnormal enhancement signs shown on the CT scan; (2) one or more new lesions appeared locally, and the CT scan revealed irregular peripheral or abnormal enhancement of the new lesions;[ 13 ] Overall survival (OS) and local progression-free survival (LPFS) were the investigation’s secondary study goals. OS was calculated from the beginning date of MWA treatment to the date of death or last follow-up. LPFS was defined as the time from randomization to ablated tumor progression or death from any cause, whichever occurred first. It is more frequently used to gauge how well tumor ablation works for achieving local tumor control.
Statistical analysis
The data were analyzed using the SPSS 19.0 version for windows (SPSS Inc, Chicago, IL, USA). The data of patients and tumors are expressed as a mean ± standard deviation or median. Qualitative data are displayed as a percentage. P < 0.05 was considered to show a difference with statistical significance.
RESULTS
Technical success and complete ablation rate.
In all NSCLCs, 3D visualization preoperative treatment planning was achieved effectively. The technical success rate was 100% in 113 sessions. After 3 months of the initial MWA, 110 of the 113 lesions were completely ablated and 3 lesions were incomplete. The primary complete ablation rate was 97.35% (110/113). Three incompletely ablated lesions underwent a second MWA, which revealed full ablation (after 3 months the second MWA). For the ablation of one tumor in one session, the mean actual power output and planning were 42.58 ± 4.23 W and 40.48 ± 5.54 W (P = 0.578), the mean actual duration and planning were 5.34 ± 1.28 min and 5.17 ± 1.05 min (P = 0.291), and the mean actual and planning target-skin distance were 11.62 ± 5.03 mm and 11.02 ± 4.12 mm (P = 0.465) [shown in Table 1 ].
LPFS and OS
The median follow-up period was 19.0 months (ranging from 6.0-26.0 months) and no patient was lost to follow-up. There was recurrence at the treated site in 4 patients at 5, 9, 13, and 14 months after MWA treatment [shown in Table 2 ]. The patients underwent a second inpatient ablation and received a complete ablation. During the follow-up period, none of the 113 patients died and no mediastinal lymph node or distant metastasis was observed. As a result, the 1 and 2-year LPFS were 98.23% and 96.46%, respectively. The 1 and 2-year overall survival rates were 100% and 100%. Tumor size was identified as significant prognostic factors for local recurrence.
Table 2: 113 cases of patients with local recurrence rate
Side effects and complications
All 113 patients received with MWA in 120 sessions, all of which achieved technical success and well tolerance. No patient died during the procedure or after 30 days of MWA treatment [Table 3 ].
Table 3: Side effects and complications during and post-MWA
Side effects were summarized as follows: (1) Pain-during the procedure, the pain was one of the common side effects under local anesthesia conditions. In 120 sessions of MWA, the patients in 58 sessions reported mild to moderate pain, and no severe. After the procedure of MWA, 31 patients suffered from mild to moderate pain, without severe post-ablation pain. (2) Cough-in 120 sessions of MWA, the patients in 35 sessions suffered from moderate-to-severe cough, of which 9 sessions were severe. The procedure was stopped with severe cough, and it was followed by subcutaneous injection of midazolam, or the procedure would be intermitted. (3) Post-ablation syndrome—the main symptoms presented as fever (lower than 38.5°C), fatigue, general malaise, nausea, vomiting, etc., which was a transient and self-limiting process. A total of 51 patients showed above post-ablation syndrome.
Complications are listed in Table 3 . Pneumothorax was the most frequent complication. There were a total of 46 (38.33%, 46/120) sessions of pneumothorax, of which 29 sessions (25.66%, 29/120) needed chest tube drainage. There were 32 (26.67%, 32/120) sessions of pleural effusion, of which 3 sessions (2.5%, 3/120) had chest tube drainage. There were 4 sessions (3.33%, 4/120) of hydropneumothorax, in which 2 sessions (1.67%, 2/120) underwent chest tube drainage. Three sessions (2.50%, 3/120) suffered from pneumonia after the MWA treatment, which could be cured by antibiotics based on the results of the sputum. A small amount intrapulmonary hemorrhage was observed in 38 sessions (31.67%, 38/120), which requiring no special treatment.
DISCUSSION
Percutaneous IGTA is an effective and safe technique in local tumor control of solid tumors, especially for RFA and MWA.[ 14 ] Over the past decades, MWA has undergone extensive research as a novel therapy option for local tumor control.[ 15 ] Compared with RFA, MWA generally produces larger, more spherical and predictable ablation zones for lung tumors, because the microwave field penetrates the lung tissue uniformly and is less dependent on its properties.[ 16 ] According to many clinical studies, MWA is an effective, safe, and potentially curative therapy for early-stage NSCLC patients who are medically inoperable.[ 4 ] For NSCLC, the actual structure of the tumor and the relationship with surrounding organs could not be illustrated clearly on 2D imaging and require reconstructing in the ablationists’ perception, which is mainly dependent on their spatial awareness and experience of MWA procedure subjectively. The most crucial step is to precisely calculate the thermal field, particularly when the lesion is close to vital organs (such as the mediastinum, superior vena cava, and diaphragm) and the distance is less than 5.0 mm, which may result in incomplete ablation and/or major complications, and further affect the therapy efficiency. As a result, how reconstructing the actual relationship between the tumor and surrounding organs, calculating the thermal field of ablation (ablative parameters), minimizing the number of punctures, and optimizing the puncture path is the key to the success of MWA.
3D-VAPS has been used in surgery for many years, but seldom in percutaneous IGTA.[ 17 ] IGTA therapy needs the quantitative calculation of the tumor volume and the distance between the tumor and surrounding vital structures. Additionally, it’s crucial to simulate the particular thermal field accurately and design the piercing path beforehand. A novel 3D-VAPS application for US-PMWA of HCC therapy was made in 2012, which considerably increased the rate of primary complete ablation and long-term effectiveness.[ 18 ] According to another report, 3D-VAPS could speed up the ablation process and improve precision by demonstrating the spatial stereoscopical construction of the tumor and its surrounding organs.[ 19 ] Several factors may have contributed to these results. First of all, compared with traditional 2D visualization, 3D-VAPS could unfolded three-dimensional reconstructions, a full view of the target tumor and the complete spatial relationship between the tumor and adjacent structures. While in the past, using 2D visualization to obtain similar information is mainly dependent on the experience and spatial awareness of ablationist. Second, the simulated thermal field of 3D-VAPS could aid ablationists in making decisions to provide precise ablation energy to avoid incomplete tumor ablation or harm to the surrounding structures before the operation of MWA treatment. It can optimize the ablation planning, detect the risks, reduce MWA procedure time, and decrease complications, especially for novice ablationist who haven’t accumulated enough experience.[ 20 ] Third, the precise fusion imaging of 3D-VAPS could present the exact location of the target tumor without the influence of the hyperechoic area such as intrapulmonary hemorrhage or perilesional exudation of the target tumor during ablation, which makes inserting the microwave antenna more exact and ablation parameters more accurately.[ 21 ] Additionally, the benefit of intraprocedural 3D-VAPS fusion imaging, which enables the ablationist to instantly assess the technique’s efficacy and enables prompt supplemental ablation to be carried out without delay, should also be noted.
This study verified the clinical application of three-dimensional visualization planning system software to calculate the ablative parameters for MWA procedure in a pilot study of patients with stage I NSCLC. The outcome showed that there is a significant overlap between the tumor and the simulated ablation in the registration and simulation program. There is no significant difference between the mean actual power output, actual duration, or puncture depth and planning. Additionally, after the three-month operation, the technical success rate was 100% and the complete ablation rate was 97.35%. The 1 and 2-year LPFS were 98.23% and 96.46%, respectively. These results suggested that 3D-VAPS-assisted MWA was efficient in treating patients with stage I NSCLC. However, four local progressions of ablated lesions occurred during follow-up, which was attributed to variations in the thermal fields between the simulated and real worlds, which caused the actual ablation to diverge from the intended ablation. The main reason for this inconsistency should be attributed to the heat sink effect.[ 22 , 23 ] The blood flow could take part of the heat away from the tumors adjacent to large blood vessels, for which more energy was required. As a result, the heat sink effect should be integrated into the simulated ablation zone and immediate ablation zone validation module of 3D-VAPS to further enhance the accuracy of ablation parameters and increase the technical success and complete ablation rate.[ 24 ]
Planning an appropriate puncture path pre-procedure and minimize the number of punctures during procedures were also significant for safety and efficient MWA treatments, which greatly reduces tissue damage and complications. Presently, there is no report on the complication of intrapulmonary hemorrhage in the treatment of early-stage lung cancer by microwave ablation. According to the previous statistics of our team, the incidence rate is more than half. By using the 3D-VAPS, we tried to avoid the bronchus and blood vessels around the lesion when planning and designing the needle path before the MWA procedure. According to our findings, the prevalence of intrapulmonary bleeding dramatically decreased, falling to 31.67%. The result should be attributed to the application of 3D-VAPS, which potentially regarding an improvement of targeting accuracy and tumor accessibility of pre-procedure estimation, especially for lesions surrounded by vital structures. Furthermore, we believe that 3D-VAPS has its greatest merit when aiming at target lesions in difficult intrapulmonary locations requiring more complex targeting trajectories.[ 25 ] Additionally, employing 3D-VAPS made it simpler to access the target tumors, allowing ablationists who are just beginning the MWA process to safely treat more difficult lesions.[ 26 ] Therefore, good operational accessibility and repeatability along with reproducibility and comparability of ablated images when using 3D-VAPS leads to the standardization of the MWA technique as well as minimizing time consumption and achieving operational simplicity.
This research has some limitations. First, it was a retrospective study, a relatively short follow-up duration post-procedure of MWA. Second, only a single ablative antenna of one lesion with a diameter ≤ 2.5 cm were studied, but the influence of multiple ablative antennas in one lesion or larger lesions with multiple ablative antennas was not studied. Third, the effectiveness and complication rates of 3D-VAPS and traditional 2D CT-guide MWA were not compared in this study. Furthermore, there is no efficacy verification and recurrence prediction for lesions after microwave ablation. As a result, a multicenter, prospective, randomized study is needed in the future to illuminate the safety and efficiency of 3D-VAPS in treating early-stage NSCLC patients.
In conclusion, this report describes and confirms that 3D -VAPS is a safe and effective treatment technique for MWA of stage I NSCLC. 3D-VAPS may be precise in optimizing the puncture path, and presetting ablation parameters. The clinical application value of 3D- VAPS is relatively high.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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