Complications of synchronous microwave ablation and biopsy versus microwave ablation alone for pulmonary sub-solid nodules: a retrospective, large sample, case-control study

Introduction

Pulmonary sub-solid nodules are also called ground-glass nodules (GGNs). GGNs are usually classified into pure and mixed GGNs (1). With the widespread adoption of high-resolution and low-dose computed tomography (CT), there has been a significant increase in the detection of nodules that present as ground-glass opacities (2). Regular chest CT needs to be conducted in patients with GGNs as long as the size increases or solid components enlarge (3,4). GGNs considered malignant require aggressive treatment, and resection is the standard method. However, some patients are unfit for surgery because of high-risk factors such as cardiopulmonary insufficiency or advanced age (5). Recently, several studies have been conducted on the treatment of GGNs by thermal ablation, including radiofrequency ablation, cryoablation, and microwave ablation (MWA). With the rapid advancement of thermal ablation technology, it has become an effective, super minimally invasive and alternative treatment strategy for patients with unresectable GGNs (6-12).

Generally, according to the clinical diagnosis and treatment process, a percutaneous puncture biopsy should be performed prior to ablation. However, this strategy has some limitations. A puncture biopsy can cause complications such as pulmonary hemorrhage, pneumothorax, hemoptysis, and hemothorax, especially in patients with poor pulmonary function (13). This will inevitably hinder the ablation treatment. Furthermore, the biopsy may yield false-negative results. The diagnostic accuracy of puncture biopsy for small nodules reportedly ranges from 51.4% to 95.8% (14,15).

There are some conditions that are not suitable for pathological diagnosis before or during ablation: (I) one of multiple GGNs has been surgically confirmed as malignant; (II) the patient refuses to undergo a puncture biopsy because of concerns of complications; (III) the GGN is located in a dangerous region; and (IV) the positivity rate of biopsy of smaller nodules is not high. However, some patients request ablation treatment because of serious psychological stress (16,17).

Previous studies have shown the diagnostic ability of percutaneous core biopsy immediately after MWA for GGNs. The complications associated with this method are mild and tolerable (7,18-22). However, the relatively small sample sizes have limited the power of these findings. Furthermore, there is no comparison of the complication rate between synchronous MWA and biopsy and MWA alone. Therefore, we conducted a larger retrospective study to compare the complication rates between synchronous MWA with biopsy and MWA alone. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-906/rc).

Methods

Study population and design

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). This retrospective study was approved by the Institutional Ethics Committee of The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital (No. QX-C010-01), and individual consent for this retrospective analysis was waived. From May 2020 to December 2021, a total of 326 patients with GGNs in our department were divided into the following two groups: group A, patients who underwent lung MWA without biopsy; and group B patients who underwent synchronous MWA and biopsy. The treatment strategy was evaluated by a multidisciplinary team consisting of respirologists, thoracic surgeons, oncologists, radiologists, and interventional radiologists. The inclusion criteria were as follows: (I) GGNs confirmed by chest CT, which were suspected to be malignant because of the increase in diameter or growth of the solid component during follow-up; (II) use of only one ablation antenna with no shift in its direction in one session; (III) Eastern Cooperative Oncology Group (ECOG) performance status of 0–2; (IV) patients aged ≥18 years and non-pregnant women; (V) multiple GGNs, most of which were considered malignant; (VI) and GGNs unsuitable for surgical resection because the patient had previously undergone surgery, was of advanced age, had poor cardiopulmonary functions or other comorbidities, or refused surgery due to high anxiety or fear. The exclusion criteria were as follows: (I) presence of regional lymph node metastasis or distant metastasis confirmed by enhanced CT, enhanced magnetic resonance imaging, and positron emission tomography-computed tomography (PET-CT); (II) poorly controlled infection; (III) severe coagulation disorder that cannot be corrected; (IV) platelet count ≤50×10⁹/L; (V) serious disease of the heart, lung, brain, and other organs; and (VI) renal or hepatic failure (Figure 1). The primary outcomes were the rate of complications and technical success rate in groups A and B.

Figure 1 Flow diagram. Group A underwent MWA alone; Group B underwent MWA and biopsy. MWA, microwave ablation; GGN, ground-glass nodule.

Instruments and the MWA procedure

The MWA was guided by CT (Lightspeed 64 V; United Imaging Healthcare, Shanghai, China) and performed using MTC-3C (Vison-China Medical Devices R&D Center, Nanjing, Jiangsu, China), ECO-100A1 (ECO Medical Instrument Co., Ltd., Nanjing, China), or KY-2450B (Canyon Medical Inc., Nanjing, China). The frequency was 2,450±50 MHz, and the continuous wave output power (0–100 W) was adjustable. The effective length of the microwave antenna was 100–180 mm, the outer diameter was 14–20 G, and the radiating tip (tapered end) was 1.5 cm long. A water- circulating cooling system was used to reduce the surface temperature of the antenna.

According to the size and location of the tumor, an ablation plan was designed using real-time CT to determine the appropriate body posture, surface puncture point, and optimal puncture trajectory. All MWA procedures were performed under local anesthesia. The antenna gradually penetrated the target lesion, and a predetermined power was applied for a predetermined duration. If pathological diagnosis was required, the ablation was suspended after 1 minute. The target lesion was punctured with a 16-G sleeve-core needle and an 18-G biopsy needle to obtain the first specimen. The decision to obtain additional specimens was based on the patient’s response; however, generally, no more than three specimens were obtained. The ablation was continued to work until a complete ablation zone was achieved, encompassing the lesion with an optimal circumferential margin of at least 1 cm. If required, another specimen was extracted when the ablation was almost completed. Track ablation was performed after the ablation procedures. Disinfection and dressing were applied to the puncture wound. CT of the whole lung was obtained immediately at the end of the session and again 24 hours after the procedure to determine the technical success and identify complications. The procedure was considered successful if the tumor was treated as planned and the ablation zone area completely covered the target (Figure 2).

Figure 2 A 58-year-old male patient with mixed GGN in the right lower lung lobe underwent synchronous MWA and biopsy. (A) A 13×9 mm mixed GGN in the lower lobe of the right lung (arrow). (B,C) An ablation antenna was inserted into the GGN, and a core biopsy needle was inserted into the lesion margin to obtain a biopsy specimen (long arrows: ablation antenna; short arrows: biopsy needle). (D) CT performed immediately post-ablation showing a GGN that was completely covered by ground gross opacity (arrow). Minimal pneumothorax was observed, and there was no intrapulmonary hemorrhage. (E) CT performed 24 hours post-ablation showing that the area of ablation had enlarged completely covered the GGN (arrow). (F-H) Fibrous hyperplasia of ablated area involuted at 1 month, 9 months, and 24 months post-ablation (arrows). (I) GGN was diagnosed as invasive adenocarcinoma (staining method: hematoxylin-eosin; magnification: ×40). GGN, ground-glass nodule; MWA, microwave ablation; mm, millimeter; CT, computed tomography.

Pathological diagnosis

The strips of specimens obtained during MWA were preserved in 10% buffered formalin and transported to the pathology department to determine the pathological diagnosis. In this study, a positive biopsy was defined as the detection of atypical adenomatous hyperplasia (AAH), adenocarcinoma in situ (AIS), minimally invasive adenocarcinoma (MIA), or invasive adenocarcinoma (IA) based on pathological examination of the samples.

Complications and side effects

Major complications were defined as events that resulted in significant morbidity and disability, an increase in the level of care, hospital admission, or substantially prolonged hospital stays. Cases that required interventional drainage were also included. All other complications were considered minor (23,24). Peri-procedure and post-ablation side effects, including pain, post-ablation syndrome, cough, and post-ablation chronic pain syndrome, were recorded (10,17).

Statistical analysis

The single-sample Kolmogorov-Smirnov test was used to assess the normality of distribution of the sample. The independent samples t-test was used to analyze numerical variables. Categorical variables were analyzed using the χ² or Fisher’s exact test. A P value of <0.05 was considered statistically significant. All statistical analyses were performed using the software SPSS 20.0 (IBM Corp., Armonk, NY, USA).

Results

Patient characteristics

A total of 164 patients (103 females and 61 males; mean age: 58.8±13.4 years; range, 28–93 years) were included in group A and 162 patients (96 females and 66 males; mean age: 59.8±12.2 years; range, 33–86 years) were included in group B. Detailed patient characteristics are listed in Table 1.

Procedure characteristics

The mean tumor diameter of the enrolled patients in group A was 9.7±3.9 mm (range, 4–23 mm). Of the 164 patients, 113 had tumors sized <10 mm, eight had tumors sized ≥20 mm, and 43 had tumors sized 10–20 mm. The mean tumor diameter of the enrolled patients in group B was 11.8±3.9 mm (range, 5–24 mm). Of the 162 patients, 69 had tumors sized <10 mm, seven patients had tumors sized ≥20 mm, and 86 had tumors sized 10–20 mm. All patients were treated with one ablation antennas. The output power was 30, 40, or 50 W. The mean ablation time was 4.9±1.4 minutes (range, 3.0–12 min) and 5.7±1.4 minutes (range, 3.0–10.5 min) in groups A and B, respectively. The mean procedure time in group A was 32.2±10.7 minutes (range, 15–70 min), and 38.9±10.7 minutes (range, 20–70 min) in groups A and B, respectively (Table 2).

Pathological findings

There were 121 (73.8%) pure GGNs and 43 (26.2%) mixed GGNs in group A. There were 89 (54.9%) pure GGNs and 73 (45.1%) mixed GGNs in group B. Analyses of the 162 specimens in group B, revealed that 46 (28.4%) nodules were IA, 26 (16.1%) were MIA, 49 (30.2%) were AIS, 22 (13.6%) were AAH, and 19 (11.7%) were benign (Table 3). The positive rate of biopsy was 88.3%.

Complications and side effects

All patients included in this study had completed 12-month follow-up. No deaths occurred during the procedure in either group. The major complications that occurred were pneumothorax, hemothorax, pleural effusion requiring a chest tube, and pulmonary infection. Other major complications, such as massive hemoptysis, bronchopleural fistula, and air embolism did not occur. A total of 66 (40.2%) patients in group A developed pneumothorax, of which 32 (19.5%) required a chest tube. In group B, 70 (43.2%) patients developed pneumothorax, of which 22 (13.6%) required a chest tube. One patient in group A and two patients in group B developed a hemothorax after MWA. Percutaneous catheter drainage was performed and approximately 500 mL of blood was drained in each patient. None of these patients received blood transfusions. After 7–14 days, the catheter was removed, and the patient was discharged. Eight patients in group A and 10 patients in group B developed pulmonary infection. All 18 recovered after antibiotic treatment. Pleural effusion developed in 79 (48.2%) patients in group A and 82 (50.6%) patients in group B; however, only two patients in group A and one patient in group B required chest tubes. Furthermore, 47 (28.7%) patients in group A had intrapulmonary hemorrhage and 101 (62.3%) patients in group B developed intrapulmonary hemorrhage (P<0.001), a minor complication (Table 4).

Intraprocedural or postprocedural pain was observed in 51 (31.1%) patients in group A and 60 (37%) patients in group B. All patients experienced relief after symptomatic treatment. A total of 34 (20.7%) patients in group A and 42 (25.9%) patients in group B developed cough. Post-ablation syndrome, which is characterized by low-grade fever (<38.5 ℃), nausea, vomiting, and general malaise, was observed in 42 (25.6%) patients in group A and 46 (28.4%) patients in group B. Post-ablation chronic pain syndrome, which is characterized by mild chest wall pain or chest skin sensory disturbances, was observed in seven (4.3%) patients in group A and 11 (6.8%) patients in group B. There was no significant difference in the incidence of side effects between the two groups (Table 4).

Efficacy

The technical success rate was 100% in both groups. All patients tolerated MWA well. No patient died due to MWA. By the end of July 2023, all 326 patients had completed the 12-month follow-up, were alive, and were undergoing regular follow-up without disease relapse.

Discussion

To the best of our knowledge, this is the first study to compare the complications of synchronous MWA and biopsy those of MWA alone for treating GGNs. Our study demonstrated that the rate of major complications was similar for the two methods. Although the incidence of intrapulmonary hemorrhage, a minor complication, in synchronous MWA and biopsy was higher than that in MWA alone, it was well controlled after conservative treatment.

The synchronous use of MWA and biopsy has been reported in several small-sized sample studies. Kong et al. analyzed 66 patients who underwent MWA followed by core-needle biopsy. The technical success rate was 100%. The positivity rate can reach 74.2% (21). Wang et al. studied the pathological findings of 74 patients who underwent biopsies before and after MWA. They demonstrated that the positive diagnosis rate of a pre-MWA biopsy was 85.1% and that of a post-MWA biopsy was 74.3%. However, the difference was not statistically significant. Nonetheless, the comprehensive positivity rate was 90.5%, which was higher than that of pre-MWA biopsy (18). The positive diagnosis rate of group B in our study was 88.3% which is similar to that of previous studies.

Pneumothorax is the most common complication following MWA. Lower location of a lung tumor, older age, smaller tumor size, longer trajectory through the aerated lung, and pulmonary emphysema are risk factors for pneumothorax. The rate of pneumothorax ranges from 3.7% to 59% following radiofrequency ablation for lung cancer (25,26). Pneumothorax might develop as a major complication, which requires a chest tube. In the study by Kong et al., the incidence of pneumothorax in the 66 patients who underwent synchronous MWA followed by core-needle biopsy was 36.4%, and 29.2% of these patients required chest tubes (21). In the study by Wang et al., the incidence of pneumothorax was 60.8% and approximately 14.9% of these patients required a drainage tube (18). Zheng et al. analyzed major complications after lung MWA (204 sessions); the incidence of pneumothorax requiring a chest tube was 15.7% (27). In our study, the incidence of pneumothorax was 40.2% in group A and 43.2% in group B, with 19.5% and 13.6% of these patients, respectively, requiring chest tubes. The difference between the two groups was not statistically significant. Therefore, synchronous MWA and biopsy does not increase the incidence of pneumothorax.

Synchronous MWA and biopsy increases the risk of intrapulmonary hemorrhage. In our study, intrapulmonary hemorrhage developed in 28.7% of patients in group A and 62.3% of patients in group B (P<0.001). Although the difference between the two groups was statistically significant, it was a minor complication. Complications of lung ablation in patients in whom synchronous MWA and biopsy have not been performed have been reported. The major complication rate of bleeding was 1.6% and the minor complication rate of hemoptysis was 6% in a single-center study by Kashima et al. of 1,000 lung radiofrequency ablation sessions in 420 patients (28). Splatt et al. reported a 2.9% incidence of significant pulmonary hemorrhage after 70 MWAs for lung malignancies (29). In a study by Wang et al. on synchronous of lung ablation and biopsy for the treatment of GGNs, the major complication rate of hemoptysis was 32.4% (18). Kong et al. demonstrated that the minor complication rate of hemorrhage was 72.7%, which is similar to our study findings (21). In our study, we recorded intrapulmonary hemorrhage, rather than hemoptysis. Any radiographic decrease in transmittance of the lung parenchyma other than post-ablation changes was recorded as intrapulmonary hemorrhage. Given the comprehensive and complex nature of the factors influencing complications, we enrolled tumors with a relatively small volume and did not shift the ablation antenna direction during the procedure. We did this to render the postoperative complications of the two groups comparable.

Pleural effusion is a complication that often develops as a sympathetic response to ablation injury. However, most pleural effusions are self-limiting and rarely require catheter drainage. Important factors in the increased incidence of pleural effusion are the use of a cluster electrode, decreased distance to the nearest pleura, and decreased length of aerated lung traversed by the electrode (25). Zheng et al. demonstrated that the incidence of effusion requiring drainage was 2.9% (27). Wolf et al. reported a 20.7% rate of pleural effusion; however, no patient required drainage (30). Wang et al. demonstrated that the rate of mild ipsilateral pleural effusion was 52.7% and that of mild contralateral pleural effusion was 14.9% (18). In our study, the rate of pleural effusion was similar to that reported by Wang et al. Furthermore, there was no statistical difference between the two groups.

Pain, cough, post-ablation syndrome, and post-ablation chronic pain syndrome are common side effects of MWA. In this study, the rate of side effects was consistent with that of our previous report. Furthermore, the difference between the two groups was not statistically significant (10,31). This shows that synchronous MWA and biopsy does not increase the rate of side effects when compared with MWA alone. Pain, cough, and post-ablation syndrome generally resolve quickly after active treatment. However, post-ablation chronic pain syndrome may last from 6 months to 1 year. Those symptoms usually do not interfere with eating or sleeping in most patients.

There were several limitations to this study. This was a single-center retrospective study. The effectiveness of the two methods of GGNs treatment could not be accurately assessed because of the lack of long-term follow-up results. Furthermore, in order for the prime the data for comparison, we only selected patients in whom one ablation antenna was used and for whom the direction of the antenna was not shifted in any session. This may have led to some bias in the complication rate. Therefore, a prospective, multicenter, randomized controlled trial is needed to further clarify the safety of synchronous MWA and biopsy for the treatment of pulmonary GGNs.

Conclusions

In conclusion, synchronous MWA and biopsy for the treatment of pulmonary GGNs did not increase the risk of major complications, which could be easily managed when they did occur. However, there were also some minor complications. Thus, synchronously performing MWA and biopsy is safe for treating pulmonary GGNs.

Acknowledgments

Funding: This study was supported by the National Natural Science Foundation of China (No. 82072028) and Shandong Provincial Nature Foundation (No. ZR2020MH294).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-906/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-906/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Institutional Ethics Committee of The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital (No. QX-C010-01). The requirement for 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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