Changes in pulmonary function of CT-guided microwave ablation for patients with pulmonary ground-glass nodules after lobectomy: a retrospective, observation study

Abstract

Purpose

This retrospective study aimed to investigate changes in pulmonary function among patients undergoing computed tomography (CT)-guided microwave ablation (MWA) for the treatment of pulmonary ground-glass nodules following lobectomy.

Materials and methods

Fifty-two patients with pulmonary ground-glass nodules (GGN) who underwent lobectomy and were subsequently diagnosed with non-small cell lung cancer (NSCLC) were included in the study. Pulmonary function tests (PFTs) were conducted at baseline and again 1 month after microwave ablation (MWA). The assessed parameters included vital capacity (VC), forced vital capacity (FVC), forced expiratory volume in 1 s (FEV1), FEV1 percentage (FEV1%), peak expiratory flow (PEF), maximal voluntary ventilation (MVV), and maximum mid-expiratory flow (MMEF). The measurements obtained 1-month post-MWA were compared to the baseline values.

Results

The mean values for VC, FVC, FEV1, FEV1%, MMEF, PEF, and MVV at baseline and 1-month post-MWA for all patients were as follows: VC (3.01 ± 0.68vs. 2.88 ± 0.67, P = 0.348), FVC (3.07 ± 0.75 vs. 2.95 ± 0.69, P = 0.430), FEV1 (2.29 ± 0.61 vs. 2.14 ± 0.55, P = 0.228), FEV1% (74.26 ± 7.70 vs. 72.41 ± 9.40, P = 0.316), MMEF (1.88 ± 0.81 vs. 1.74 ± 0.72, P = 0.410), PEF (5.03 ± 1.62 vs. 4.54 ± 1.53, P = 0.179), and MVV (77.69 ± 22.21 vs. 73.15 ± 17.63, P = 0.286). For the eight patients who underwent ablation of two or more lesions simultaneously, the mean values for VC, FVC, FEV1, FEV1%, MMEF, PEF, and MVV at baseline and 1 month post-MWA were as follows: VC (2.67 ± 0.90vs. 3.05 ± 0.97, P = 0.341), FVC (2.82 ± 0.94vs. 3.10 ± 0.92, P = 0.430), FEV1 (1.97 ± 0.69vs. 2.07 ± 0.69, P = 0.709), FEV1% (70.01 ± 7.24 vs. 66.27 ± 4.47, P = 0.082), MMEF (1.28 ± 0.80 vs. 1.35 ± 0.58, P = 0.777), PEF (4.43 ± 1.44 vs. 3.87 ± 1.40, P = 0.074), and MVV (65.22 ± 16.50 vs. 72.26 ± 12.28, P = 0.222). No significant differences were observed in the PFT results before and 1 month after MWA.

Conclusions

MWA is a localized treatment that spares lung parenchyma. The pulmonary function 1 month after MWA did not statistically differ from baseline levels, suggesting that MWA may not adversely affect pulmonary function.

Introduction

Lung cancer remains the leading cause of cancer-related mortality worldwide [1]. Historically, lobectomy has been considered the preferred surgical approach for the oncologic resection of early-stage non-small cell lung cancer (NSCLC) lesions [2]. Previous studies indicate that patients with synchronous multiple pulmonary ground glass nodules (GGN) comprise ~ 20–30% of all individuals diagnosed with pulmonary GGN [3]. When patients undergo pulmonary lobectomy accompanied by simultaneous lymph node dissection targeting the lesions, the presence of residual nodules may increase the risks associated with anesthesia and significantly impair postoperative lung function. Currently, there is no standardized approach for managing residual pulmonary nodules in patients who have undergone pulmonary lobectomy. Furthermore, the optimal management of newly appearing GGN in other lung lobes after surgery remains uncertain.

Evidence suggests that non-surgical treatments for pulmonary GGN, such as stereotactic body radiotherapy and image-guided thermal ablation (IGTA), are both safe and effective, particularly IGTA [4–6]. IGTA is one of the methods for treating pulmonary metastases. Among IGTA methods, microwave ablation (MWA) is a widely utilized approach that demonstrates a favorable local tumor control rate for both primary and secondary lung tumors. However, to date, no studies have assessed the impact of pulmonary function tests (PFT) on the treatment of pulmonary GGN following lobectomy with MWA.

This retrospective study involved 52 patients with postoperative pulmonary GGN who underwent MWA following lobectomy. The study aims to provide preliminary evidence regarding changes in pulmonary function after this treatment. By assessing PFTs after the procedure, this research seeks to offer insights into the safety of MWA concerning pulmonary function, thereby guiding clinical decision-making for the management of postoperative pulmonary GGN.

Materials and methods

Patients

This study retrospectively analyzed data from patients with NSCLC who underwent MWA at our institution from October 2021 to December 2023. Patients were included in this study if they met the following criteria: (1) a history of one or more lobectomies performed more than 6 months prior, along with a histopathological diagnosis of NSCLC; (2) a single lesion or multiple pulmonary lesions with a maximum diameter ranging from 8 to 30 mm, or imaging findings consistent with malignancies, such as vacuole or burr signs, pleural depression, and vascular clusters; (3) availability of PFT results obtained before and 1 month after MWA. The exclusion criteria were as follows: (1) evidence of distant metastasis or local lymph node metastasis as revealed by enhanced (computed tomography) CT or positron emission tomography/CT; (2) a single lesion measuring less than 8 mm or greater than 30 mm; (3) poor cardiopulmonary function and inability to perform self-care; irreversible coagulopathy and severe bleeding tendency. Clinical and demographic data collected from patients included age, sex, medical history, body mass index, smoking status, chemotherapy, pulmonary condition, histology, as well as surgical blood loss and postoperative drainage. A total of 52 patients with pulmonary GGN who underwent CT-guided MWA were included in the study (Fig. 1). The baseline characteristics of these 52 patients and their lesions are shown in Table 1. This study has been approved by the Ethics Committee of Qujing First People's Hospital (Ethics Number: 2024-043-01), and written consent was obtained from all patients.

Fig. 1.

Patient collection flow of study design

Table 1.

60 cases of pulmonary GGN in patients, detailing the characteristics for the nodules

Characteristics	Number	Percent (%)
Total GGNs ablated	60	100%
Age range median ± SD(years)	43–84	59.7 ± 8.8
Gender
Male	26	50.00%
Female	26	50%
Lesion location
Left lung	41	68.30%
Right lung	19	31.70%
Type of GGN
Pure GGN	15	25%
Solid nodules	15	25%
Mixed GGN	30	30%
Number of ablated lesion
1	44	84.60%
2	8	15.40%
Maximum diameter (mm)
8–10	26	43.30%
11–15	24	40%
16–20	7	11.70%
21–25	1	1.70%
26–30	2	3.30%
Maximum diameter (median ± SD) [mm]	8.0–30.0 (11.3 ± 6.1)
Pathology
Invasive adenocarcinoma	15	28.80%
Squamous cell carcinoma	4	7.70%
Others	33	63.50%
Comorbidities
Yes	33	63.50%
No	19	36.50%

Type of pulmonary GGN

Pulmonary GGN are classified into three types based on the solid component: pure GGN (pGGN), part‑solid nodules or mixed GGN (mGGN), and solid nodules, where pGGN and mGGN are also known as sub‑solid nodules [7]. Among them, solid pulmonary nodules refer to circular or quasi circular density increased shadows in the lungs, with lesion density sufficient to mask the blood vessels and bronchial shadows that run through them. GGN lesions refer to CT images of increased lung density with clear or unclear boundaries, but the lesion density is not sufficient to mask the vascular and bronchial shadows that run through it. If the ground glass lesion does not contain solid components, it is called pGGN; If it contains solid components, it is called mGGN.

MWA procedure

For each patient, the surgical route and the extent of ablation were discussed by the entire surgical team prior to the performance of MWA. Percutaneous MWA was performed under CT guidance using a 16-row large-bore helical CT simulator (Brilliance CT Big Bore, Philips). A layer thickness of 1.8 mm was routinely employed during CT scanning. For pulmonary nodule treated with MWA (ECO-100A1, ECO Medical Instrument Co., Ltd., China), preoperative localization was confirmed with CT images, and the patient was positioned appropriately. The puncture site was marked and disinfected, a sterile towel was spread, and local anesthesia (lidocaine) and preemptive analgesia (hydromorphone) were administered. Puncture biopsy needle (CA1811, MAIRUITONG Medical Inc, China) and the microwave ablation antenna (ECO-100AL5, ECO Medical Instrument Co., Ltd, China) were advanced to the predetermined position. The ablation probe was connected to a 250-mL syringe containing normal saline and to a generator through a peristaltic pump and a cooling circulating water pipe. Firstly, one or two strips of pathological tissue were obtained. Subsequently, the generator was activated (ablation power: 30–60 W, ablation time: 2–8 min). During the procedure, CT was performed again to confirm the ablation range and monitor for any complications. After a sufficient ablative zone was achieved, the antenna was pulled out, and a sterile bandage was applied to the skin.

Evaluation indexes and postoperative follow-up

The technical success was indicated by observation that the post-ablation ground-glass nodules (GGO) were generally 0.5–1.0 cm larger than the tumor sites. If the patient developed massive pneumothorax or pleural effusion, catheter drainage was performed. In addition, antibiotics were administered if any signs of infection arose. A non-contrast chest CT was performed 24–48 h post-ablation for all patients to identify potential complications. Subsequently, chest CT was performed at 1 month and 3 months post -ablation to confirm the achievement of complete ablation. Thereafter, chest CT was scheduled every 6 months to monitor for local progression or development of new lesions. Subsequently, chest CT was performed every 1 year. The basis for CT follow-up after ablation is expert consensus on the multidisciplinary diagnosis and treatment of multiple ground-glass nodule-like lung cancer (2024 Edition). PFTs were performed via spirometry both preoperatively and at the 1 month follow-up. PFTs were based on the American Thoracic Society recommendations and included vital capacity (VC), forced vital capacity (FVC), forced expiratory volume in 1 s (FEV1), FEV1%, peak expiratory flow (PEF), maximal voluntary ventilation (MVV), and maximum mid-expiratory flow (MMEF).

Statistical analysis

All analyses were performed using SPSS (version 25). The variables are presented as means and standard deviations (SDs). Differences between pre- and post-MWA PFT findings were evaluated using the paired t-test. A single-sample Kolmogorov–Smirnov (K–S) test was used to assess the normality of the data. Data that did not conform to a normal distribution were analyzed using the Wilcoxon test. Statistical significance was established at P < 0.05.

Results

A total of 60 lesions underwent simultaneous percutaneous core needle biopsy and MWA in 52 patients with pulmonary GGNs, including 3 patients with 2 nodules in a single pulmonary lobe and 5 patients with 2 nodules in different pulmonary lobes (Fig. 2). The remaining cases presented with a single pulmonary nodule (Fig. 3). The technical success rate was 100%.

1. The pre and 1-month post-MWA PFT results of the 52 patients.

   The mean values for VC, FVC, FEV1, FEV1%, MMEF, PEF, and MVV at baseline and 1 month post MWA for all patients were as follows: VC (3.01 ± 0.68vs. 2.88 ± 0.67, P = 0.348), FVC(3.07 ± 0.75 vs. 2.95 ± 0.69, P = 0.430), FEV1(2.29 ± 0.61 vs. 2.14 ± 0.55, P = 0.228), FEV1%(74.26 ± 7.70 vs. 72.41 ± 9.40, P = 0.316), MMEF (1.88 ± 0.81 vs. 1.74 ± 0.72, P = 0.410),PEF(5.03 ± 1.62 vs. 4.54 ± 1.53, P = 0.179), and MVV (77.69 ± 22.21 vs. 73.15 ± 17.63, P = 0.286). No significant differences were observed in the PFT results before and 1 month after MWA. The pre and 1-month post-MWA PFT results of the 52 patients are presented in Table 2.

2. The pre and 1-month post-recovery PFT results of the 8 patients who underwent ablation of ≥ 2 lesions simultaneously

   The mean values for VC, FVC, FEV1, FEV1%, MMEF, PEF, and MVV at baseline and 1 month post MWA for 8 patients who underwent ablation of ≥ 2 lesions simultaneously are as follows: VC (2.67 ± 0.90 vs. 3.05 ± 0.97, P = 0.341), FVC (2.82 ± 0.94 vs. 3.10 ± 0.92, P = 0.430), FEV1 (1.97 ± 0.69 vs. 2.07 ± 0.69, P = 0.709), FEV1% (70.01 ± 7.24 vs. 66.27 ± 4.47, P = 0.082), MMEF (1.28 ± 0.80 vs. 1.35 ± 0.58, P = 0.777),PEF (4.43 ± 1.44 vs. 3.87 ± 1.40, P = 0.074), and MVV (65.22 ± 16.50 vs. 72.26 ± 12.28, P = 0.222). No significant differences were observed in the PFT results before and 1 month after MWA. The pre and 1-month post-recovery PFT results of the 8 patients who underwent ablation of ≥ 2 lesions simultaneously are presented in Table 3.

3. Complications

   No MWA-associated deaths were observed during the procedure or within 30 days after the procedure. 17 patients developed major complications, including pneumothorax that does not require catheter drainage (n = 12), pneumothorax requiring catheter drainage (n = 2), pleural effusion requiring catheter drainage (n = 1), and the incidence of intrapulmonary hemorrhage requiring treatment with hemostatic drugs was observed in two patients (n = 2). None of the patients developed air embolism or bronchopleural fistula. In these patients, PFTs were performed 1 month after recovery from complications. Figure 4 shows a 69- year- old male patient who underwent MWA treatment for GGN located in the upper lobe of the left lung, one year after lobectomy for right lung cancer. During the surgery, a large amount of pneumothorax occurred, and a chest drainage tube was implanted for continuous negative pressure drainage (Fig. 4c). The pneumothorax subsided 24 h after MWA, and the drainage tube was subsequently removed. Continuous regression of lesions was observed 36 months after MWA (Fig. 4f).

4. CT follow-up

   A total of 52 patients underwent evaluations at 1 month and 3 months post-ablation to confirm the achievement of complete ablation. No local progression or development of new lesions was observed in these patients at the 6 months follow-up post -ablation. After 1 year of CT follow-up, none of the 52 patients exhibit local progression at the ablation site, however, 2 patients developed new lesions in the lungs.

Fig. 2.

A 50-year- old female patient underwent MWA treatment for GGN in the upper lobe of the right lung 3 years after lobectomy for left lung cancer. The red arrows indicate the locations of the nodules. a A solid nodule, located in the upper lobe of the right lung, measuring18 mm in diameter. b An antenna was inserted into the lesion. c The lesion was covered by ground-glass opacity and a small amount of pneumothorax was observed immediately post-MWA. d The lesion involuted 3 months post-MWA. e The lesion gradually involuted 12 months post-MWA. f The lesion involuted to a band 24 months post-MWA

Fig. 3.

A 61-year- old male underwent MWA treatment for two GGNs in the lower lobe of the right lung two years after lobectomy for left lung cancer. The red arrows indicate the locations of the nodules. a Two mixed GGNs located in the inferior lobe of the right lung, with diameter of 14 mm and 9 mm. b1 An antenna was inserted into the lesions. b2 An antenna was inserted into the lesions. c Both lesions were covered by ground-glass opacity and a small amount of pneumothorax was observed immediately post-MWA. d The lesions involuted 3 months post-MWA. e The lesions gradually involuted 12 months post-MWA. f The lesions involuted to bands 24 months post-MWA

Table 2.

The pre- and post-PFT results for all the patients

PFT	pre-MWA	post-MWA	t	p
VC	3.01 ± 0.68	2.88 ± 0.67	0.948	0.348
FVC	3.07 ± 0.75	2.95 ± 0.69	0.796	0.43
FEV1	2.29 ± 0.61	2.14 ± 0.55	1.219	0.228
FEV1%	74.26 ± 7.70	72.41 ± 9.40	1.013	0.316
MMEF	1.88 ± 0.81	1.74 ± 0.72	0.830	0.41
PEF	5.03 ± 1.62	4.54 ± 1.53	1.363	0.179
MVV	77.69 ± 22.21	73.15 ± 17.63	1.077	0.286

Table 3.

The pre- and post-PFT results for 8 patients who underwent ablation of ≥ 2 lesions simultaneously

PFT	pre-MWA	post-MWA	t	p
VC	2.67 ± 0.90	3.05 ± 0.97	− 1.022	0.341
FVC	2.82 ± 0.94	3.10 ± 0.92	− 0.838	0.43
FEV1	1.97 ± 0.69	2.07 ± 0.69	− 0.389	0.709
FEV1%	70.01 ± 7.24	66.27 ± 4.47	2.207	0.082
MMEF	1.28 ± 0.80	1.35 ± 0.58	− 0.294	0.777
PEF	4.43 ± 1.44	3.87 ± 1.40	2.094	0.074
MVV	65.22 ± 16.50	72.26 ± 12.28	− 1.342	0.222

Fig. 4.

A 69-year-old male patient underwent MWA treatment for GGN in the upper lobe of the left lung one year after lobectomy for right lung cancer. a A tumor located in the lower lobe of the left lung measuring 14 mm in diameter. classified as a mixed GGN. bAn antenna was inserted into the lesion. c A large amount of pneumothorax occurred during the procedure. A chest drain tube was implanted for continuous negative pressure drainage. d The pneumothorax resolved 24 h post-MWA, and the drainage tube was subsequently removed. The lesion was observed to be covered by ground-glass opacity. e The lesion showed involution 12 months post-MWA. f Continued involution of the lesion was noted 36 months post-MWA

Discussion

Preliminary data showed acceptable safety profile and efficacy for percutaneous radiofrequency ablation (RFA) and MWA in early-stage lung cancer [4, 5]. More than that, MWA is becoming increasingly recognized as a therapeutic option, and it has the advantages of a shorter operation time, a larger volume of necrosis in the ablation area, and less "heat sink" effect, making more patients with malignant tumors accept MWA as an alternative [8]. Huang et al. [4] retrospectively evaluated the feasibility, safety, and short‑term efficacy of MWA in the treatment of multiple simultaneous GGNs of the lung. 33 patients (9 males and 24 females, mean age: 59.6 ± 10.0 years) with multiple GGOs (103 GGOs with mean size 12.3 ± 6.3 mm) were enrolled in this study. Patients underwent 66 procedures of CT-guided percutaneous MWA. The technical success rate was 100%, and there were no deaths related to the MWA procedure. The median follow‑up period was 18.1 months (range: 6.8–37.7 months). The 3‑year overall survival and local progression-free survival rates were both 100%. Therefore, they believed that CT‑guided percutaneous MWA treatment of multiple synchronized lung GGNs is feasible, safe, and effective. In this study, all patients with pulmonary GGNs were treated with CT-guided MWA, performed under local anesthesia. The technical success rate was 100%.

There is a limited number of studies investigating changes in pulmonary function following image-guided thermal ablation. Li et al. [9] demonstrated an impairment of pulmonary function post MWA in 133 patients diagnosed with malignant lung tumors, confirming that there was a significant difference in PFT results before and 1 month after MWA. Wu et al. [10] studied the changes in pulmonary function before and after MWA in 35 patients, identifying significant differences in the PFT findings on day 3, but not at 6 months. Additionally, several studies have examined the changes in pulmonary function impairment following radiofrequency ablation, with results indicating that pulmonary function can be restored within 1–3 months [11, 12]. This study aims to examine the differences in pre- and post-MWA pulmonary function in patients with GGN after lobectomy. To evaluate changes in pulmonary function, we analyzed PFT results at baseline and 1 month post‑MWA. To our knowledge, there is currently no research on pulmonary function changes after MWA of residual or newly developed pulmonary nodules following lobectomy. Our study results demonstrate that the mean VC, FVC, FEV1, FEV1%, MMEF, PEF and MVV of the 52 patients were not significantly different between the baseline and 1 month post MAW (Table 2). Kim et al. [13] explored pulmonary function changes over one year after lobectomy in lung cancer patients, finding that actual pulmonary function improved over time over when compared with predicted postoperative values, with significant increase observed at 6 months. Therefore, in this study, the relationship between baseline pulmonary function and surgical procedures was not significant. It is interesting that in this study, three patients diagnosed with SMGNs as target lesions underwent two lobectomy treatments, with pathology findings revealing lung invasive adenocarcinoma. Patients with residual GGNs suggestive of malignant transformation underwent MWA more than 12 months later. And the patient's postoperative pulmonary function gradually recovers within 1 month, and there have been no fatalities.

In this study, we also reviewed the impact of simultaneous ablation of multiple nodules on pulmonary function. Among the eight patients, five had two nodules located in different lung lobes, while three had two nodules within the same lung lobe. Both nodules were successfully ablated during a single surgery. Of these patients, two developed pneumothorax, two experienced slight bleeding, and no life-threatening conditions were observed. Although the FEV1% and PEF decreased 1 month post-surgery compared to pre-operative levels, the P-value was not significant, and the patient's pulmonary function gradually improved during subsequent follow-ups. Wu et al. [10] suggests that up to three GGNs present in the same lobe may be ablated in a single procedure. However, GGNs located in different lobes should be approached separately to ensure patient safety. This is also consistent with our perspective, and we suggest that target lesions are determined based on PFT findings.

Pneumothorax is the most common complication that occurs after ablation, with an incidence rate ranging from 10 to 60% [14, 15]. In this study, the incidence of pneumothorax was approximately 26.9%. Most cases of pneumothorax are self-limiting. However, two patients required drainage due to lung compression exceeding 30%. A small amount of pleural effusion is often observed after ablation, with an incidence rate of 1–60% [16, 17]. In this study, only one patient developed a small amount of pleural effusion. The occurrence of pleural effusion appears to be associated with increased pleural temperatures during the procedure, suggesting a potential link to pleural effusion induced by thermal injury. The incidence of hemorrhage during ablation is reported to be between 3 and 8% [18, 19]. In our study, the incidence of hemorrhage was approximately 3.8%. CT may assist in identifying the ablation range covered affected by hemorrhage. While a significant large amount of pneumothorax and pleural effusion may have a negative impact on the performance of PFT, in this study, only one patient required drainage for pleural effusion, and recovery did not affect pulmonary function.

Conclusions

In conclusion, our study provides valuable insights into the effects of CT-guided MWA on pulmonary function in patients with GGN. Our results show that there is no significant difference in pulmonary function at 1-month post-MWA compared to baseline, suggesting that MWA may not affect pulmonary function. However, it is important to acknowledge several limitations of this study. Firstly, it is a retrospective observational study without randomization, which may lead to imbalances among the included patients, potentially influencing the results. Future prospective studies with randomized controlled designs would provide stronger evidence regarding the impact of MWA on pulmonary function. Second, the short follow-up period of only 1-month post-procedure limits our ability to assess the longer-term effects of MWA on pulmonary function. Although our results suggest no immediate changes, we acknowledge that the long-term impact of MWA on pulmonary function may differ. A longer follow-up period would offer a more comprehensive understanding of the sustained effects of MWA. We strongly advocate for the importance of long-term follow-up data, and in future studies, we plan to extend the follow-up period to evaluate ongoing changes in pulmonary function. Additionally, a larger sample size should be considered to gain deeper insights into the long-term effects of MWA on pulmonary function. Finally, we recognize that diffusion capacity of the lung for carbon monoxide (DLCO) is a crucial aspect of assessing pulmonary function, and we regret DLCO measurements were not included in this study. The majority of physicians involved in this study did not routinely utilize DLCO in clinical practice, which accounts for the absence of this data. However, we acknowledge the significance of TLCO as part of a comprehensive pulmonary function assessment and plan to incorporate it into future studies to provide a more thorough evaluation of the pulmonary function changes following MWA.

Author contributions

ZC and ZW designed this study and directed the research group in all aspects, including planning, execution, and analysis of the study. DRY drafted the manuscript. LH and LJL collected the data. FYD and WL provided the statistical software, performed the data analysis, LFN and ZTF arranged the Figures and Tables. LCY and WZP revised the manuscript. All authors read and approved the final manuscript.

Funding

This work was supported by an internal project of Qujing First People's Hospital (No. 2022YJKTY18, 2022YJKTF01, 2023YJKTY04), and The Basic Research Program of Yunnan Provincial Department of Education (2023Y0699).

Data availability

The original data presented in the study are included in the article/Supplementary Table, and further inquiries can be directed to the corresponding author.

Declarations

Ethics approval and consent to participate

The study was conducted in accordance with the Declaration of Helsinki and Good Clinical Practice guidelines. The study was approved by the ethics committee of Qujing First People’s Hospital (Ethics Number: 2024-043-01). Written informed consent was obtained from all patients.

Competing interests

The authors declare no competing interests.