Comparison of the efficacy and adverse events between argon-helium cryoablation and microwave ablation for non-small cell lung cancer: a propensity score matching study

Introduction

Lung cancer represents the most prevalent cause of morbidity and mortality from cancer globally (1). A study demonstrated that until 2018, lung cancer remained the leading cause of cancer mortality in men and the second leading cause of cancer mortality in women after breast cancer (2). Non-small cell lung cancer (NSCLC) represents the most prevalent form of lung cancer, accounting for over 80% of all lung cancer diagnoses (3). Despite the significant advances made by immune checkpoint inhibitors in the treatment of NSCLC in recent years, lobectomy remains the gold standard treatment for patients with surgically resectable lung cancer (4). Recently, a study has demonstrated that the combination of multimodality treatment with local ablation significantly extends the overall survival (OS) of select patients with lung cancer (5). Additionally, ablation therapy offers notable advantages, including a low risk of injury and efficient disease management, underscoring its value in multimodality treatment approaches (6). Since pulmonary ablation was first described in a series of cases in 2000, significant advances have been made in the past two decades. Currently, there are numerous techniques for ablative therapy for NSCLC, including microwave ablation (MWA), argon-helium cryoablation (AHC) and radiofrequency ablation (RFA) (7).

Recent tumor-related studies have demonstrated that MWA has the capacity to both directly kill tumor cells through the energy generated by electromagnetic waves and modify the tumor microenvironment, stimulating an immune response through a range of immunomodulatory factors, such as tumor antigens, danger signals and cytokines, thus achieving anti-tumor effects (8,9). AHC is a minimally invasive cryogenic technique commonly used in the clinics. It may modify the tumor microenvironment, which results in the downregulation of TRAF2-mediated NF-κB signaling pathway in NSCLC, thereby inhibiting tumor cell proliferation (10). As MWA and AHC are widely used in the treatment of NSCLC around the world, the question of which is more advantageous in clinical application has become a major focus of current research. Consequently, a comparative study was conducted on NSCLC patients who received MWA and AHC over the past three years. This study provides clinical evidence for NSCLC patients to choose a more appropriate percutaneous ablative treatment under certain conditions. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2228/rc).

Methods

This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Institutional Ethics Review Committee of Dongzhimen Hospital (No. 2024DZMEC-039), and individual consent for this retrospective analysis was waived. However, written informed consent for surgery was obtained from each subject before MWA or AHC, after full explanation of the purpose and nature of the procedure used.

Patients

All patients were selected according to the following inclusion criteria: (I) preoperative diagnosis of NSCLC, confirmed by biopsy pathology, and diagnosis of primary NSCLC in accordance with the Chinese Medical Association guideline for clinical diagnosis and treatment of lung cancer (2023 edition) (11); (II) maximum diameter of a single tumor ≤5 cm; (III) age ≥18 years; (IV) patient receives one MWA or AHC treatment; (V) the Karnofsky performance status (KPS) of the patient ≥70 points. The exclusion criteria were as follows: (I) the presence of an autoimmune disease or the use of immunosuppressive drugs within the previous 6 months; (II) evidence of active infection; (III) patients with incomplete clinical data or follow-up periods of less than 6 months were also excluded.

Methods of treatment

Prior to ablation, a comprehensive assessment of the patient’s general status was conducted, including a chest computed tomography (CT) scan, electrocardiogram, and laboratory tests. This was undertaken to identify any underlying conditions and to manage the symptoms. Laboratory tests included complete blood count, C-reactive protein (CRP), coagulation function, and cardiac enzymes. The KPS score was used as the main evaluation tool for clinical status. The maximum cross-sectional area of the tumor, the size of the tumor, the distribution of blood flow around the tumor, and the distance between the lesion and the pleura were measured according to the preoperative chest CT imaging results. These measurements were then discussed by a multidisciplinary team, including radiologists, thoracic surgeons and respiratory physicians, to determine the optimal position of the patient and the needle insertion point during the operation. This approach aimed to maximise the therapeutic efficacy and safety of the procedure while also preparing for the management of any potential complications. The aforementioned treatment will be conducted in the radiology department, with the operation being carried out by respiratory physicians. Local anesthesia is used for treatment. The SIEMENS (SOMATOM-Emotion 16, Siemens Healthineers, Erlangen, Germany) CT machine was employed as guidance equipment. Following ablation, patients were administered symptomatic supportive therapy in accordance with the specific complications and other conditions.

MWA

MWA was performed under a KY-2000A MWA system (Nanjing Kangyou Medical Technology Co., Ltd., Nanjing, China) and a KY-2450A-1 sterile disposable MWA needle (Nanjing Kangyou Medical Technology Co., Ltd.) at a frequency of 2,450±50 MHz with a continuous wave output power range of 0 to 50 W. The effective length of the MWA needle was 100 to 200 mm, with an outer diameter of 1.4 to 2.4 mm. The surface of the ablation needle was cooled using a water circulation cooling system. The number of MWA needles inserted into the tumor depends on its size and location. Typically, one or two needles are simultaneously inserted into the center of the tumor under CT guidance. The position of the needles is determined by CT scanning, and MWA is performed at a power of 30 or 35 W for 5–10 minutes. Higher power, longer treatment times and even an additional ablation needle may be considered for lesions with a maximum transverse diameter greater than 15 mm. This is dependent on whether the ablation area is seen to cover the lesion completely on the CT scan and ensure that the edge of the ablation area extends to the farthest 5–10 mm of the lesion. Following the procedure, haemostasis was routinely secured with pressure, and the patient’s clinical vital signs, including blood pressure, pulse, respiration, and oxygen saturation, were monitored.

AHC

AHC was conducted under a cryosurgical system, AH-1 (Beijing Sunshine Yibang Medical Technology Co., Ltd., Beijing, China), and a cryoablation needle with a diameter of 2.4 mm. The cryoablation procedure was conducted using high-pressure argon and helium, based on the Joule-Thomson effect. In accordance with the size and location of the tumor, one or two cryoablation needles are simultaneously inserted into the centre of the tumor under CT guidance. Following the determination of the needle location via CT scanning, 2–3 cycles of cryoablation were performed, comprising a 10–15-minute freezing phase (temperature reduced to −170 ℃) and a 5-minute active rewarming phase (temperature rises to 20–45 ℃). After each cycle of rewarming, a CT scan was conducted to ensure that the ablation area encompassed the lesion and that it extended beyond the lesion by approximately 5–10 mm. Following the procedure, haemostasis was routinely secured with pressure, and the patient’s clinical vital signs, including blood pressure, pulse, respiration, and oxygen saturation, were monitored.

Postoperative follow-up

On the second day following treatment, a chest X-ray, complete blood count, and CRP were performed to identify any potential complications. The number of common adverse events during the treatment period was recorded and graded according to the Common Terminology Criteria for Adverse Events version 5.0 (12). Furthermore, survival follow-up assessments were initiated 6 months postoperatively, with annual telephone follow-ups conducted thereafter.

Statistical analysis

The primary objective of this study was to determine the occurrence of adverse events following treatment. The secondary objective was to assess patient survival beyond 6 months. To reduce the potential for confounding bias due to non-randomised retrospective allocation, propensity score matching (PSM) was employed to balance the preablation data between the two groups (13). The propensity score is the conditional probability of receiving an exposure given a vector of the measured covariates. In our study, propensity scores for all patients were estimated by multiple logistic regression models using the following baseline characteristics as covariates: gender, age, smoke, alcohol consumption, chronic obstructive pulmonary disease (COPD), hypertension, diabetes mellitus, coronary heart disease, and maximum cross-sectional area of tumor (cm²). Prior to matching, the mean propensity scores of patients in the MWA group (n=42) and patients in the AHC group (n=83) were 0.618 and 0.689, respectively. The nearest neighbour method of matching for PSM was employed in a 1:1 matching with a caliper value of 0.05. Following matching, the mean propensity scores of patients in the MWA group (n=42) and patients in the AHC group (n=42) were 0.602 and 0.622 (P=0.46). The statistical significance of qualitative variables was evaluated using the χ² test or Fisher’s exact test, both before and after 1:1 matching. Quantitative information that was normally distributed was compared using the independent samples t-test. Quantitative data that was normally distributed before and after the treatment of the same patient was compared by paired-samples t-test. A Kaplan-Meier analysis was conducted to assess survival rates, which were then compared using a log-rank test. The factors affecting prognosis were analysed using Cox regression. Continuous variables are expressed as mean ± standard deviation, while categorical variables are presented as frequency (N) and percentage (%). All statistical analyses were conducted using SPSS software version 26.0 (IBM SPSS Inc., Chicago, IL, USA) and the R functions. The results were considered statistically significant when the P value was less than 0.05.

Results

Patient characteristics

A total of 125 patients with primary NSCLC were treated with percutaneous transluminal lung ablation between July 2020 and October 2023. Figure 1 illustrates the intraoperative and 2 weeks postoperative follow-up chest CT images of MWA and AHC. All patients met the inclusion and exclusion criteria for this study. Patients were categorised into two groups according to the different ablation modalities they received: the MWA group (n=42) and the AHC group (n=83). Table 1 presents the clinical baseline and demographic parameters. Due to unavoidable selection bias, there was a statistically significant difference in the maximum cross-sectional area of tumors between the two groups of patients before PSM (P=0.04). After PSM, 42 matched pairs of patients were created, as shown in Table 1, and no statistically significant differences were observed in the clinical baseline and demographic parameters. The screening flowchart is presented in Figure 2.

Figure 1 Intraoperative and 2 weeks postoperative CT images of microwave ablation and argon-helium cryoablation. (A) Intraoperative CT scan images of microwave ablation. (B) Two weeks after microwave ablation, CT scan showed nodular scarring at the treatment site. (C) Intraoperative CT scan images of argon-helium cryoablation. (D) Two weeks after argon-helium cryoablation, CT scan showed nodular scarring at the treatment site. CT, computed tomography.

Figure 2 Process flow chart summarizes patient selection. MWA group, patients treated with microwave ablation. AHC group, patients treated with argon-helium cryoablation. AHC, argon-helium cryoablation; MWA, microwave ablation; PSM, propensity score matching.

Inflammatory response, the red blood cells (RBCs), and hemoglobin (HGB) before and after operation

There was no statistically significant difference in systemic inflammation-related indicators, including white blood cells (WBCs) (P=0.52) and CRP (P=0.52), between the two groups prior to treatment. Following treatment, the MWA group exhibited elevated WBCs (P=0.001) and CRP (P=0.005) levels, with a statistically significant difference. The WBCs (P=0.19) and CRP (P=0.17) levels were found to be slightly elevated in the AHC group following treatment, although the difference was not statistically significant. The results are presented in Figure 3. There was no statistically significant difference between the two groups in pre-treatment indices related to bleeding, including RBCs (P=0.46) and HGB (P=0.50). Following treatment, both the RBCs (P=0.006) and HGB (P=0.003) levels were reduced in MWA groups, with statistically significant differences. In the AHC group, both RBCs (P=0.04) and HGB (P=0.05) levels exhibited a statistically significant decrease compared to pretreatment values. The results are presented in Figure 4.

Figure 3 Comparison of changes in systemic inflammatory indexes before and after two kinds of ablation treatment. **, P<0.01. AHC, argon-helium cryoablation; CRP, C-reactive protein; MWA, microwave ablation; WBC, white blood cell.

Figure 4 Comparison of changes in RBC and hemoglobin before and after two kinds of ablation treatment. *, P<0.05. AHC, argon-helium cryoablation; HGB, hemoglobin; MWA, microwave ablation; RBC, red blood cell.

Adverse events during treatment and its grading

Adverse events were recorded in both groups during the treatment period. Treatment-related ache occurring within 1 week postoperatively was categorized as an adverse event. Moreover, any postoperative bleeding was also classified as an adverse event. The most common adverse events during this period in both groups were pneumothorax, bleed, pleural effusion, ache, pharyngeal discomfort, subcutaneous emphysema, and fever. Statistical analysis of the adverse events of the two groups of patients revealed that there were more patients with bleeding in the AHC group than in the WMA group, while there were more patients with ache in the WMA group than in the AHC group. All the above differences were found to be statistically significant. The results are presented in Table 2.

No fatalities related to the surgical procedure were observed in either group of patients. Further grading of the adverse events that occurred during treatment in both groups revealed that there was no statistically significant difference in the severity of adverse events in both groups (P=0.33), as shown in Table 2.

Prognostic analysis

We proceeded to examine the postoperative survival of patients in both groups. The mean follow-up duration was 22.38 months in the MWA group and 29.58 months in the AHC group. The comparative analysis revealed comparable 2-year OS outcomes between the two treatment groups, with rates of 69.9% (MWA group) and 66.0% (AHC group), respectively (P=0.69, not statistically significant) (14). The specific results are presented in Figure 5. We further analysed the prognosis of patients treated with ablation using a Cox regression analysis. The univariate analysis identified several factors that influence patient prognosis, including gender, smoking, alcohol consumption, COPD, radiotherapy and subcutaneous emphysema. The results of the multifactorial analysis indicated that smoking, COPD and radiotherapy were independent prognostic factors affecting OS. The specific results are presented in Table 3.

Figure 5 Comparison of overall survival after two different treatments.

Discussion

Lung cancer, as a primary disease that represents a significant threat to human health, has a profound impact on patient survival and quality of life. It is the leading cause of death among cancer patients worldwide (15). Currently, more than 85% of cases are classified as NSCLC, with the predicted 5-year survival rate being only 15.9% (16). Consequently, the academic community has placed a significant focus on the question of how to improve the quality of life and prolong the survival of patients with NSCLC. In general, surgical resection is the primary treatment option for this disease. However, less than 30% of patients can receive surgical resection due to advanced age, underlying diseases, and the numerous complications associated with surgery (17). Over the past two decades, technological advances have led to the development of numerous localised lung ablation techniques, including MWA, AHC, and RFA. These techniques have demonstrated efficacy in clinical settings, as evidenced by their ability to achieve favourable therapeutic outcomes (18,19). MWA has been widely studied in local ablation therapy for lung cancer in recent years and has been more and more widely used in the clinic in the last two decades. MWA is a new technology based on microwave electromagnetic field, which has a faster heating and higher temperature thermal zone compared with RFA. It can better concentrate the heat and reduce the ablation procedure time while also reducing damage to surrounding tissues (20). Currently, the studies related to lung ablation are mainly retrospective, with a limited number of cases included. There is a lack of further analysis of the adverse effects of MWA lung treatment (21,22). AHC is a representative local ablation technique of cryoablation, and it has been widely used in the clinic due to its effectiveness in local ablation treatments. Some studies have demonstrated that AHC can destroy tumor cells, release cytokines and danger signals, and promote the maturation of antigen-presenting cells and the proliferation of lymphocytes, thereby enhancing the immune response and thus promoting anti-tumor activity (23,24). Nevertheless, due to the distinctive freezing mechanism of AHC and the larger surgical area, some researchers have postulated that it may potentially present a risk of cryoshock (25). Currently, there are few studies on MWA and AHC. Those that do exist are mainly focused on the clinical efficacy of liver, breast, and thyroid cancers. There are no comparative studies on lung treatment in the same centre to guide the clinical application of the two ablation modalities in lung cancer. The research team has conducted a significant number of lungs MWA and AHC ablation treatments at the respiratory disease centre of a top-ranked hospital, which provides the necessary support for clinical research on the efficacy of the two modalities in NSCLC.

Firstly, the maximum cross-sectional area of the tumor was originally statistically different between the two groups. Furthermore, there were significantly more patients in the AHC group than in the MWA group. This may be related to the operative preference of the operator. To address the potential for selection bias and confounding in the retrospective study, we employed PSM to limit selection bias and reduce confounding. Following PSM, the baseline matching of demographic and clinical characteristics between the two groups was favourable. Subsequently, we conducted a comparative analysis of the systemic inflammatory response status, RBCs, and haemoglobin concentration of the two ablation modalities prior to the procedure and 2 days post-procedure. Furthermore, we collated and graded the adverse events that occurred during the treatment. Finally, we evaluated patient survival at 6 months post-procedure to assess long-term prognosis.

It is well established that invasive surgical procedures elicit a spectrum of inflammatory responses in the body, which may be associated with a range of clinical events and may even influence the prognosis of the disease. The systemic inflammatory response caused by such surgical procedures may be associated with the recruitment of multiple inflammatory factors and the activation of inflammatory pathways, which may result in the occurrence of postoperative adverse events and even trigger systemic inflammatory response syndrome (26). Previous studies have demonstrated that both MWA and AHC facilitate cytokine release, thereby augmenting local immune responses subsequent to treatment (27,28). It is a phenomenon that enhances the body’s anti-tumor ability, but the necessary assessment of the systemic inflammatory response induced by both is lacking. In the present study, by matching the MWA and AHC groups, it was found that the postoperative WBCs and CRP of patients in the MWA group were significantly elevated in comparison to the preoperative period. In contrast, the postoperative WBCs and CRP of patients in the AHC group were elevated in comparison to the preoperative period, although there was no statistically significant difference. This may be attributed to the fact that cryoablation exerts an immunomodulatory effect and minimizes the possibility of an excessive inflammatory response (29,30). A comparison of postoperative RBCs and HGB levels in both groups revealed a significant decrease compared to preoperative levels. This suggests that either MWA or AHC causes a decrease in organismal RBCs and HGB, which is consistent with previous studies (31,32). Given the anatomical structure of the lung, which has a rich blood supply and is adjacent to the aorta, it is important to monitor the RBCs and HGB of ablation patients during ablation treatments. This should be done in conjunction with evaluation of the potential risk of bleeding in conjunction with coagulation-related indexes. Regular monitoring of the blood counts and chest CT in the postoperative period is also essential. The use of hemostatic drugs to prevent bleeding or to stop bleeding if necessary is recommended to avoid the occurrence of adverse events.

A further statistical analysis was performed on the adverse events that occurred during the treatment of patients in the MWA group and the AHC group. The analysis revealed that the most common adverse events following ablation were pneumothorax, haemorrhage, pleural effusion, ache, pharyngeal discomfort, subcutaneous emphysema, and fever. In our study, we found that the overall number of adverse events occurred more frequently in patients in the AHC group than in the MWA group. Further analysis revealed that the AHC group experienced more bleeding events than the MWA group, while the MWA group experienced more aching events than the AHC group. The remaining adverse events did not exhibit any statistically significant differences in occurrence. Despite our pre-operative hemostatic measures, the AHC group exhibited a higher risk of bleeding. This is consistent with previous findings that cold ablation is associated with a higher bleeding rate and effusion than heat ablation (33). The appearance of bleeding variability in lung ablation treatments may be related to the fact that the lungs have a richer capillary distribution, while heat ablation has the characteristic of promoting coagulation (34). During treatment, patients in the MWA group exhibited a greater incidence of ache events than those in the AHC group. A previous study has indicated that hot ablation may result in more severe ache, particularly in the proximal pleural range. This ache may also be indicative of the occurrence of serious adverse events to some extent (35). Additionally, the occurrence of adverse events during treatment was evaluated in both the MWA and AHC groups. The results demonstrated that there was no significant difference in the grading of adverse events during treatment between the two groups of patients. This indicates that the severity of adverse events was comparable between the two ablation modalities, and that they had a similar safety profile. Nevertheless, two patients in the MWA group required urgent management, primarily due to pneumothorax, subcutaneous emphysema and aches, which may be attributed to the influence of heat conduction in the surrounding tissues, the location of the ablation in closer proximity to the pleura, and the damage to the airway cartilage caused by heat ablation.

At the end of the study, we followed up the survival status of patients who were more than 6 months postoperatively, and we found that there was no significant difference in postoperative OS between patients in the MWA and AHC groups. Although the effects of MWA and AHC on patient survival have been rarely mentioned in previous studies, it has been suggested that there is no significant difference in OS between NSCLC patients treated with heat ablation and cold ablation (33,36). Furthermore, a Cox regression analysis was conducted to identify the factors influencing patient prognosis. The analysis revealed that smoking, COPD and radiotherapy were independent predictors of patient prognosis following ablation. It is not only smoking that is a major risk factor for the development and progression of lung cancer; tobacco smoke also continuously induces chronic inflammation in the lungs, which negatively affects the recovery of patients’ postoperative lung function and may also lead to the recurrence of postoperative lung cancer (37). Patients with COPD are accompanied by irreversible lung function damage and decreased lung function reserve, which makes them more susceptible to adverse events during ablation treatments, which is not favourable for the patients’ postoperative recovery (38). Furthermore, it has been found that both smoke and COPD contribute to prolonged postoperative hospitalisation in patients treated with ablation treatment (39). In the study, ablation patients underwent radiotherapy demonstrated unfavorable prognosis, which may be attributed to radiation-induced pneumonitis and pulmonary function impairment resulting from lung tissue exposure to ionizing radiation (40). Recent research has demonstrated that radiotherapy can induce the aggregation of local inflammatory factors and stimulate angiogenesis, consequently modifying the tumor microenvironment and potentially facilitating tumor recurrence (41). Consequently, it is imperative to meticulously assess the pulmonary function and general condition of patients with smoke inhalation, COPD and radiotherapy prior to ablation treatments. Furthermore, it is crucial to reinforce the evaluation and management of these patients’ post-procedure, with the objective of minimizing the occurrence of adverse events. At the same time, it is of paramount importance to monitor the recovery of lung function and the risk of tumor recurrence following the procedure.

The study aimed to determine the effects and adverse events of MWA and AHC treatments in patients with NSCLC, as well as their impact on patient survival. However, there are still some limitations in this study. Firstly, this study was not conducted as a prospective study. As a retrospective study, the choice of ablative treatments could not be randomised despite performing PSM, which may affect the analysis of the results. Secondly, the metrics collected in this study were limited. Finally, the sample size of this study was relatively small. Consequently, we intend to conduct a multicenter clinical trial with a large sample size in a follow-up study to enhance the conclusions.

Conclusions

In conclusion, both MWA and AHC represent viable options for interventional ablation treatments in NSCLC patients. Although both ablative treatments may result in some degree of damage, the overall adverse events are controllable and have a certain degree of safety in clinical application. Considering the distinctive characteristics of the two ablation treatments, it is imperative to consider the patient’s symptoms, laboratory parameters, and tumor location when formulating an individualised ablation treatment plan for each patient. This approach aims to minimise the occurrence of adverse events and eradicate the lesion as much as possible during the treatment process.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2228/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2228/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2228/prf

Funding: This study was supported by the New Teacher Initiation Fund Project of Beijing University of Chinese Medicine (No. 2023-JYB-XJSJJ-040) and Horizontal Research Project on Percutaneous Transluminal Ablation Therapy in Lung Cancer (No. HX-DZM-202257).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2228/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. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Institutional Ethics Review Committee of Dongzhimen Hospital (No. 2024DZMEC-039), and individual consent for this retrospective analysis was waived.

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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