Abstract
Background
Minimally invasive surgery, including video-assisted thoracoscopic surgery (VATS) and robotic-assisted thoracoscopic surgery (RATS), has been widely performed for non-small cell lung cancer (NSCLC). Several studies have reported the clinical benefits of RATS for early-stage NSCLC. However, the application of RATS in the more advanced stage NSCLC remains controversial. This retrospective study aimed to compare the perioperative and survival outcomes of patients with pathological stage II–IIIB NSCLC who underwent lobectomy by VATS or RATS.
Methods
This retrospective study identified patients with pathological stage II–IIIB NSCLC who underwent lobectomy via VATS or RATS at Nagoya City University Hospital between 2017 and 2023. Perioperative outcomes, disease-free survival (DFS) and overall survival (OS) were assessed.
Results
In total, 145 patients (VATS, n=109; RATS, n=36) were included. After propensity score matching (PSM), there were 62 patients in the VATS group and 31 patients in the RATS group. In the PSM cohort analysis, blood loss was lower [109 mL, interquartile range (IQR), 67–168 vs. 52 mL, IQR, 25–102; P=0.003] and the length of postoperative hospital stay was shorter (5 days, IQR, 5–8 vs. 5 days, IQR, 4–5; P=0.01) in the RATS group. The 3-year DFS rates were 44.2% in the VATS group and 56.0% in the RATS group (P=0.12). The 3-year OS rates were 68.1% in the VATS group and 72.5% in the RATS group (P=0.30).
Conclusions
Even in cases of pathological stage II–IIIB NSCLC, RATS is feasible and is associated with comparable survival and perioperative outcomes to VATS. Additional multicenter studies are needed to ensure the representativeness of this study.
Keywords: Video-assisted thoracoscopic surgery (VATS), survival outcomes, robotic-assisted thoracoscopic surgery (RATS), non-small cell lung cancer (NSCLC)
Highlight box.
Key findings
• There was no significant difference in survival outcomes of pathological stage II–IIIB non-small cell lung cancer (NSCLC) patients between the robotic-assisted thoracoscopic surgery (RATS) and the video-assisted thoracoscopic surgery (VATS) groups after propensity score matching.
• In addition, RATS was associated with less blood loss and a shorter postoperative hospital stay than VATS.
What is known and what is new?
• Several studies comparing RATS and VATS have revealed that the surgical approach was not an independent predictor of the overall survival or disease-free survival. However, most of the included studies focused on early-stage NSCLC. In particular, only a few reports on locally advanced NSCLC have been published previously. Therefore, the application of RATS in patients with more advanced stage NSCLC remains controversial.
• We evaluated the perioperative and survival outcomes of patients with pathological stage II–IIIB NSCLC who underwent lobectomy by RATS or VATS.
What is the implication, and what should change now?
• Even in cases of pathological stage II–IIIB NSCLC, RATS is feasible and associated with a comparable survival and perioperative outcomes to that of VATS. RATS may be applied as minimally invasive surgery in stage II–IIIB NSCLC.
Introduction
In recent decades, video-assisted thoracoscopic surgery (VATS) has been widely performed as a minimally invasive surgery. VATS is associated with reduced postoperative pain, better postoperative quality of life, and fewer complications than thoracotomy (1-3). Moreover, the long-term prognosis of locally advanced non-small cell lung cancer (NSCLC) has been reported to be non-inferior to that of thoracotomy (4-7). On the other hand, robotic-assisted thoracoscopic surgery (RATS) has been widely performed for the treatment of early-stage NSCLC. RATS has several advantages over VATS, including three-dimensional visualization and articulated joint forceps with more degrees of freedom of motion (8,9). Several studies comparing RATS with VATS in early-stage NSCLC have demonstrated that RATS is superior in terms of the clinical advantages of fewer complications, fewer blood transfusions, length of hospital stay, and increased lymph node harvesting (3,10-13). Regarding survival outcomes, two meta-analyses have compared VATS and RATS. These studies revealed that the surgical approach was not an independent predictor of overall survival (OS) or disease-free survival (DFS) (11,13). However, most of the included studies focused on early-stage NSCLC. Therefore, the application of RATS in patients with more advanced stage NSCLC remains controversial. Regarding the survival outcomes for locally advanced NSCLC, only a few reports have been published previously (14-18).
The aim of this retrospective study was to evaluate the perioperative and survival outcomes of pathological stage II–IIIB NSCLC patients who underwent lobectomy by VATS or RATS. To assess these outcomes, we reviewed consecutive cases of VATS and RATS lobectomies at our institution. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-553/rc).
Methods
Patient selection and data collection
This retrospective study was approved by the institutional ethics committee of Nagoya City University (approval No. 60-24-0058). The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. Individual consent for this retrospective analysis was waived. We reviewed the databases of our institution between January 2017 and March 2023. Eligible cases included patients who underwent VATS or RATS lobectomy at Nagoya City University Hospital and who had pathological stage II–IIIB NSCLC. The following exclusion criteria were applied: (I) incomplete resection; (II) thoracotomy; (III) induction therapy; and (IV) wedge resection, segmentectomy, or pneumonectomy. Clinical and pathological staging were based on the 8th edition of the tumor-node-metastasis (TNM) classification of the International Association for the Study of Lung Cancer (19). The clinical TNM stage was diagnosed on contrast-enhanced chest and abdomen computed tomography (CT), enhanced brain magnetic resonance imaging (MRI), and positron emission tomography/CT (PET/CT) before surgery. Lymph nodes with a short diameter greater than 1.0 cm on CT and fluorodeoxyglucose uptake on PET/CT were clinically suspected to be positive for lymph node metastasis. Basically, in clinical N2 cases, mediastinal lymph node sampling by endobronchial ultrasound-transbronchial needle aspiration was considered. Adjuvant therapy was recommended for every patient depending on their individual status and was administered on the basis of a multidisciplinary discussion. Surveillance follow-up was performed to measure tumor makers, chest X-rays, and whole-body CT every 3 months during the first 2 years and every half-year thereafter, while contrast-enhanced head MRI was performed every year.
The following data of the included patients were recorded: (I) clinicopathological features such as age, sex, smoking status, Charlson comorbidity index (CCI), comorbidities, preoperative serum carcinoembryonic antigen (CEA), preoperative pulmonary functions, tumor size, location of tumor, histology, clinical and pathological TNM stage, occult lymph node metastases (defined as unexpected pathological N1–2 metastases in clinical N0 cases), and adjuvant therapy; (II) perioperative outcomes, such as operative time, intraoperative blood loss, conversion to thoracotomy, intraoperative and postoperative complications, duration of chest drainage, postoperative length of hospital stay, extent of lymph node dissection, number of dissected lymph nodes; (III) survival outcomes such as 3-year DFS, OS, relapse pattern, cause of death, and subsequent therapy. In this study, locoregional recurrence was defined as recurrence in the bronchial stump, cut end of the lung parenchyma, ipsilateral hilar or mediastinal lymph nodes, ipsilateral pleura, or ipsilateral chest wall.
To minimize potential bias in case selection, we performed two-to-one propensity score matching (PSM) using the nearest-neighbor matching method with a 0.20 caliper width. The included cases were matched according to 10 variables: age, sex, presence or absence of comorbidities, smoking status, percent vital capacity (%VC), forced expiratory volume in one second (FEV1%), laterality of tumor, histological type, pathological stage, and adjuvant therapy.
Surgical procedure
The surgical approach was decided by both the patients and surgeons before surgery. In our hospital, there was no difference in the indications between the VATS and RATS approaches. All patients underwent general epidural anesthesia contralateral one-lung ventilation using a double-lumen endotracheal tube. Patients were placed in the lateral decubitus position. VATS was performed in three incisions, including a 3–4 cm main incision in the 4th intercostal space at the site of the anterior axillary line and two ports in the 7th intercostal space. For RATS, 5 incisions, including a 3 cm main incision in the 4th intercostal space at the site of the anterior axillary line, 1 port at the 7th intercostal space, and 3 ports at the 9th intercostal space. The procedure was performed by complete portal lobectomy with 4 robotic arms and a carbon dioxide insufflation system under 8 mmHg of pressure. The da Vinci Xi system (Intuitive Surgical, Sunnyvale, CA, USA) was used. Patients generally underwent lobe-specific mediastinal lymph node dissection. However, cases with suspected clinical N2 lymph node metastases underwent systematic mediastinal lymph node dissection.
Statistical analysis
Patient characteristics are summarized as numbers and percentages for categorical variables and median and interquartile range (IQR) for continuous variables. Fisher’s exact test was used for categorical variables, and the Mann-Whitney U test was used for continuous variables when comparing the two groups. The standardized mean difference (SMD) was used to evaluate PSM performance. DFS and OS were evaluated using a Kaplan-Meier survival analysis. Differences between the two groups were examined using the log-rank test. Univariate and multivariate analyses using Cox regression models were performed to assess the potential independent effects on DFS and OS. Two-sided P values of <0.05 were considered to indicate statistical significance. Data were analyzed using EZR (ver. 1.65, Saitama Medical Center, Jichi Medical University, Saitama, Japan).
Results
Patient characteristics
In total, 145 patients met our inclusion criteria, including 109 patients who underwent VATS lobectomy and 36 patients who underwent RATS lobectomy. After PMS, 62 and 31 patients were included in the VATS and RATS groups, respectively. Demographic data are presented in Table 1. The distribution of age, sex, smoking status, comorbidities, CEA, pulmonary function, and tumor size was comparable between the two groups. Pathological data, such as pathological N stage, occult lymph node metastases, pathological stage, histology, and adjuvant therapy were well balanced between the two groups (Table 2). The details of adjuvant therapy are shown in Table S1.
Table 1. Baseline characteristics, before and after propensity score matching.
| Variables | Overall cohort | PSM cohort | |||||
|---|---|---|---|---|---|---|---|
| VATS (n=109) | RATS (n=36) | SMD | VATS (n=62) | RATS (n=31) | SMD | ||
| Age, years | 71 [67–77] | 71 [62–75] | 0.15 | 71 [66–75] | 72 [62–76] | 0.06 | |
| Sex: male | 81 (74.3) | 27 (75.0) | 0.02 | 48 (77.4) | 23 (74.2) | 0.08 | |
| Smoking status | 0.06 | 0.04 | |||||
| Ever | 85 (78.0) | 29 (80.6) | 51 (82.3) | 25 (80.6) | |||
| Never | 24 (22.0) | 7 (19.4) | 11 (17.7) | 6 (19.4) | |||
| CCI | 1 [0–2] | 1 [0–2] | 0.01 | 1 [0–2] | 1 [0–1] | 0.21 | |
| No comorbidity | 31 (28.4) | 9 (25.0) | 0.08 | 14 (22.6) | 7 (22.6) | <0.001 | |
| Hypertension | 40 (36.7) | 10 (27.8) | 0.19 | 25 (40.3) | 9 (29.0) | 0.24 | |
| Diabetes mellitus | 17 (15.6) | 3 (8.3) | 0.23 | 12 (19.4) | 3 (9.7) | 0.28 | |
| COPD | 13 (11.9) | 6 (16.7) | 0.14 | 8 (12.9) | 5 (16.1) | 0.09 | |
| Coronary artery disease | 6 (5.5) | 1 (2.8) | 0.14 | 5 (8.1) | 1 (3.2) | 0.21 | |
| Interstitial pneumonia | 14 (12.8) | 4 (11.1) | 0.05 | 9 (14.5) | 3 (9.7) | 0.15 | |
| History of cancer | 21 (19.3) | 10 (27.8) | 0.20 | 14 (22.6) | 8 (25.8) | 0.08 | |
| Renal dysfunction | 24 (22.0) | 8 (22.2) | 0.005 | 17 (27.4) | 8 (25.8) | 0.04 | |
| CEA, ng/mL | 4.1 [2.3–7.6] | 4.1 [2.4–6.3] | 0.04 | 3.9 [2.3–8.0] | 4.0 [2.4–5.9] | 0.11 | |
| FEV1% | 74 [66–79] | 70 [65–79] | 0.04 | 73 [65–79] | 69 [65–77] | 0.006 | |
| %VC | 100 [91–109] | 102 [92–111] | 0.17 | 104 [93–110] | 101 [91–110] | 0.14 | |
| Tumor size, mm | 39 [23–50] | 32 [25–42] | 0.28 | 32 [20–47] | 32 [22–41] | 0.11 | |
| Primary tumor lobe | 0.41 | 0.25 | |||||
| Right upper | 32 (29.4) | 10 (27.8) | 23 (37.1) | 9 (29.0) | |||
| Right middle | 4 (3.7) | 2 (5.6) | 2 (3.2) | 2 (6.5) | |||
| Right lower | 28 (25.7) | 15 (41.7) | 18 (29.0) | 11 (35.5) | |||
| Left upper | 25 (22.9) | 5 (13.9) | 12 (19.4) | 5 (16.1) | |||
| Left lower | 20 (18.3) | 4 (11.1) | 7 (11.3) | 4 (12.9) | |||
| Clinical T stage | 0.55 | 0.38 | |||||
| T1 | 35 (32.1) | 17 (47.2) | 24 (38.7) | 14 (45.2) | |||
| T2 | 39 (35.8) | 12 (33.3) | 21 (33.9) | 11 (35.5) | |||
| T3 | 23 (21.1) | 7 (19.4) | 13 (21.0) | 6 (19.4) | |||
| T4 | 12 (11.0) | 0 (0.0) | 4 (6.5) | 0 (0.0) | |||
| Clinical N stage | 0.43 | 0.37 | |||||
| 0 | 64 (58.7) | 27 (75.0) | 39 (62.9) | 24 (77.4) | |||
| 1 | 30 (27.5) | 4 (11.1) | 14 (22.6) | 3 (9.7) | |||
| 2 | 15 (13.8) | 5 (13.9) | 9 (14.5) | 4 (12.9) | |||
| Clinical stage | 0.52 | 0.48 | |||||
| IA | 21 (19.2) | 12 (33.3) | 15 (24.2) | 10 (32.3) | |||
| IB | 12 (11.0) | 5 (13.9) | 8 (12.9) | 5 (16.1) | |||
| IIA | 10 (9.2) | 4 (11.1) | 4 (6.5) | 4 (12.9) | |||
| IIB | 32 (29.4) | 10 (27.8) | 19 (30.6) | 8 (25.8) | |||
| IIIA | 32 (29.4) | 4 (11.1) | 15 (24.2) | 3 (9.7) | |||
| IIIB | 2 (1.8) | 1 (2.8) | 1 (1.6) | 1 (3.2) | |||
Categorical variables are expressed as the number (percentage), and continuous variables are expressed as the median [interquartile range]. CCI, Charlson comorbidity index; CEA, carcinoembryonic antigen; COPD, chronic obstructive pulmonary disease; FEV1, forced expiratory volume in 1 second; N, node; PSM, propensity score matching; RATS, robotic-assisted thoracoscopic surgery; SMD, standardized mean difference; T, tumor; VATS, video-assisted thoracoscopic surgery; VC, vital capacity.
Table 2. Pathologic details before and after propensity score matching.
| Variables | Overall cohort | PSM cohort | |||||
|---|---|---|---|---|---|---|---|
| VATS (n=109) | RATS (n=36) | SMD | VATS (n=62) | RATS (n=31) | SMD | ||
| Pathological T stage | 0.32 | 0.16 | |||||
| T1 | 16 (14.7) | 8 (22.2) | 11 (17.7) | 7 (22.6) | |||
| T2 | 37 (33.9) | 14 (38.9) | 23 (37.1) | 12 (38.7) | |||
| T3 | 33 (30.3) | 10 (27.8) | 20 (32.3) | 8 (25.8) | |||
| T4 | 23 (21.1) | 4 (11.1) | 8 (12.9) | 4 (12.9) | |||
| Pathological N stage | 0.02 | 0.08 | |||||
| 0 | 48 (44.0) | 16 (44.4) | 23 (37.1) | 13 (41.9) | |||
| 1 | 36 (33.0) | 12 (33.3) | 22 (35.5) | 11 (35.5) | |||
| 2 | 25 (22.9) | 8 (22.2) | 17 (27.4) | 7 (22.6) | |||
| Occult lymph node metastases | 33 (30.3) | 13 (36.1) | 0.12 | 24 (38.7) | 12 (38.7) | <0.001 | |
| Pathological stage | 0.29 | 0.13 | |||||
| IIA | 9 (8.3) | 5 (13.9) | 5 (8.1) | 3 (9.7) | |||
| IIB | 52 (47.7) | 19 (52.8) | 33 (53.2) | 17 (54.8) | |||
| IIIA | 40 (36.7) | 9 (25.0) | 17 (27.4) | 9 (29.0) | |||
| IIIB | 8 (7.3) | 3 (8.3) | 7 (11.3) | 2 (6.5) | |||
| Histology | 0.20 | 0.104 | |||||
| Adenocarcinoma | 70 (64.2) | 26 (72.2) | 42 (67.7) | 22 (71.0) | |||
| Squamous cell | 27 (24.8) | 6 (16.7) | 12 (19.4) | 6 (19.4) | |||
| LCNEC | 6 (5.5) | 2 (5.6) | 4 (6.5) | 1 (3.2) | |||
| Other† | 6 (5.5) | 2 (5.6) | 4 (6.5) | 2 (6.5) | |||
| Adjuvant therapy | 0.102 | 0.097 | |||||
| Yes | 52 (47.7) | 19 (52.8) | 29 (46.8) | 16 (51.6) | |||
| No | 57 (52.3) | 17 (47.2) | 33 (53.2) | 15 (48.4) | |||
Categorical variables are expressed as the number (percentage). †, adenosquamous cell carcinoma (one case in the RATS group and three cases in the VATS group), large cell carcinoma (one case in the RATS group and one case in the VATS group), and pleomorphic carcinoma (two cases in the VATS group). LCNEC, large cell neuroendocrine carcinoma; PSM, propensity score matching; RATS, robotic-assisted thoracoscopic surgery; SMD, standardized mean difference; VATS, video-assisted thoracoscopic surgery.
Perioperative outcomes
Table 3 shows the perioperative outcomes and lymph node dissections in the two groups. No 30-day mortality was observed in either group. In the PSM analysis, the amount of blood loss was significantly lower in the RATS group than in the VATS group (52 mL, IQR, 25–102 vs. 109 mL, IQR, 67–168; P=0.003). Additionally, the postoperative length of hospital stay was significantly shorter in the RATS group (5 days, IQR, 4–5 vs. 5 days, IQR, 5–8; P=0.01). The operative time was longer in the RATS group than in the VATS group (255 min, IQR, 195–286 vs. 219 min, IQR, 173–254), but the difference was not statistically significant (P=0.08). The duration of chest drainage, prevalence of intraoperative and postoperative complications, and rate of conversion to thoracotomy were comparable between the two groups. The distribution of the extent of lymph node dissection was similar between the groups. Regarding the number of dissected lymph nodes, the median number at the N1 level was 8 (IQR, 6–11) in the VATS group and 10 (IQR, 6–12) in the RATS group (P=0.41). At the N2 level, the median number of dissected lymph nodes was 8 (IQR, 3–11) in the VATS group and 7 (IQR, 4–9) in the RATS group (P=0.56). There was no significant difference in N1 and N2 levels between the two groups either before or after PSM.
Table 3. Perioperative outcomes.
| Variables | Overall cohort | PSM cohort | |||||
|---|---|---|---|---|---|---|---|
| VATS (n=109) | RATS (n=36) | P | VATS (n=62) | RATS (n=31) | P | ||
| Operative time, min | 220 [172–270] | 252 [194–285] | 0.18 | 219 [173–254] | 255 [195–286] | 0.08 | |
| Blood loss, mL | 120 [66–185] | 44 [18–99] | <0.001 | 109 [67–168] | 52 [25–102] | 0.003 | |
| Mediastinal lymph node dissection | 0.88 | >0.99 | |||||
| Sampling | 17 (15.6) | 6 (16.7) | 7 (11.3) | 4 (12.9) | |||
| Lobe-specific | 74 (67.9) | 23 (63.9) | 46 (74.2) | 22 (71.0) | |||
| Systematic | 18 (16.5) | 7 (19.4) | 9 (14.5) | 5 (16.1) | |||
| Number of dissected lymph nodes | |||||||
| N1 level | 7 [5–11] | 10 [6–12] | 0.21 | 8 [6–11] | 10 [6–12] | 0.41 | |
| N2 level | 7 [3–10] | 7 [4–9] | >0.99 | 8 [3–11] | 7 [4–9] | 0.56 | |
| Intraoperative complications | 7 (6.4) | 1 (2.8) | 0.68 | 4 (6.5) | 1 (3.2) | 0.66 | |
| Conversion to thoracotomy | 1 (0.9) | 0 (0.0) | >0.99 | 0 (0.0) | 0 (0.0) | >0.99 | |
| Duration of chest drainage, days | 1 [1–2] | 1 [1–2] | 0.56 | 1 [1–2] | 1 [1–2] | 0.34 | |
| Postoperative LOS, days | 5 [5–8] | 5 [4–5] | 0.003 | 5 [5–8] | 5 [4–5] | 0.01 | |
| Postoperative complications | 21 (19.3) | 2 (5.6) | 0.06 | 12 (19.4) | 2 (6.5) | 0.13 | |
| Prolonged air leak ≥7 days | 10 | 5 | |||||
| Chest tube reinsertion† | 2 | 1 | |||||
| Pneumonia requiring antibiotics | 2 | ||||||
| Acute exacerbation of IPF | 2 | 2 | |||||
| Pleural effusion requiring intervention | 1 | 1 | 1 | ||||
| Bronchopleural fistula | 1 | 1 | |||||
| Chylothorax | 1 | 1 | |||||
| Subglottic stenosis | 1 | 1 | |||||
| Recurrent nerve palsy | 1 | 1 | |||||
| Respiratory failure | 1 | 1 | |||||
Categorical variables are expressed as the number (percentage) and continuous variables are presented as the median (interquartile range). †, all patients requiring chest tube reinsertion had late-onset alveolopleural fistula. IPF, idiopathic pulmonary fibrosis; LOS, length of hospital stay; PSM, propensity score matching; RATS, robotic-assisted thoracoscopic surgery; VATS, video-assisted thoracoscopic surgery.
Survival analysis
The median follow-up period for censored cases was 40.5 months (IQR, 27.4–59.2 months) before PSM and 42.8 months (IQR, 31.5–60.3 months) after PSM. In the VATS group, the median follow-up period was 48.5 months (IQR, 27.1–61.3 months) before PSM and 51.4 months (IQR, 33.8–66.9 months) after PSM. In the RATS group, the median follow-up period was 34.6 months (IQR, 27.9–42.3 months) before PSM and 37.1 months (IQR, 27.9–43.6 months) after PSM. Table 4 shows the postoperative recurrence and mortality rates. The postoperative recurrence rate in the PSM cohort was 58.1% (n=36) in the VATS group and 38.7% (n=12) in the RATS group. The all-cause mortality rate was 35.5% (n=22) and 22.6% (n=7) in the VATS and RATS group, respectively. The lung cancer death rate was 54.5% (n=12) and 85.7% (n=6) in the VATS and RATS group, respectively.
Table 4. Postoperative recurrence and mortality.
| Variables | Overall cohort | PSM cohort | |||
|---|---|---|---|---|---|
| VATS (n=109) | RATS (n=36) | VATS (n=62) | RATS (n=31) | ||
| Postoperative recurrence | 58 (53.2) | 13 (36.1) | 36 (58.1) | 12 (38.7) | |
| Relapse pattern | |||||
| Locoregional | 31 (53.4) | 9 (69.2) | 17 (47.2) | 8 (66.7) | |
| Distant | 18 (31.0) | 3 (23.1) | 12 (33.3) | 3 (25.0) | |
| Locoregional + distant | 9 (15.5) | 1 (7.7) | 7 (19.5) | 1 (8.3) | |
| Death | 38 (34.9) | 8 (22.2) | 22 (35.5) | 7 (22.6) | |
| Cause of death | |||||
| Lung cancer | 22 (57.9) | 6 (75.0) | 12 (54.5) | 6 (85.7) | |
| Other cause | 14 (36.8) | 2 (25.0) | 8 (36.4) | 1 (14.3) | |
| Unknown | 2 (5.3) | 0 (0.0) | 2 (9.1) | 0 (0.0) | |
Categorical variables are expressed as the number (percentage). PSM, propensity score matching; RATS, robotic-assisted thoracoscopic surgery; VATS, video-assisted thoracoscopic surgery
Before PSM, the 3-year DFS rates in the VATS and RATS groups were 46.4% and 59.6%, respectively (P=0.09) (Figure 1A). The 3-year OS rates in the VATS and RATS groups were 68.1% and 73.1%, respectively, which did not amount to a statistically significant difference (P=0.24) (Figure 1B). After PSM, the 3-year DFS rates in the VATS and RATS groups were 44.2% and 56.0%, respectively (Figure 2A). The 3-year OS rates in the VATS and RATS groups were 68.1% and 72.5%, respectively (Figure 2B). There was also no significant difference in DFS or OS between the two groups in the PSM cohort (DFS: P=0.12, OS: P=0.30). The median DFS for the VATS and RATS groups was 24.5 months and was not reached, respectively. Post-recurrence treatment was administered to 33 patients (91.6%) in the VATS groups and 9 patients (75.0%) in the RATS group (Table S2). A univariate Cox regression analysis revealed that the surgical approach was not individually associated with DFS [hazard ratio (HR) =1.68; 95% confidence interval (CI): 0.92–3.06; P=0.09] and OS (HR =1.58, 95% CI: 0.73–3.40; P=0.25). A multivariate analysis showed similar results for DFS (HR =1.79, 95% CI: 0.97–3.31; P=0.06) and OS (HR =1.50, 95% CI: 0.69–3.29; P=0.31). Pathological stage was associated with DFS in the multivariate analysis (Table 5). Younger age, female sex, never smoker status, the absence of comorbidities, adenocarcinoma histology, and adjuvant therapy were associated with prolonged OS in the univariate analysis. Pathological stage, histology and the absence of comorbidities were independent predictors of prolonged OS in the multivariate analysis (Table 6).
Figure 1.
Survival outcomes of pathological II–IIIB NSCLC patients in the VATS group and RATS groups. Before propensity score matching: (A) DFS; (B) OS. CI, confidence interval; DFS, disease-free survival; NSCLC, non-small cell lung cancer; OS, overall survival; RATS, robotic-assisted thoracoscopic surgery; VATS, video-assisted thoracoscopic surgery.
Figure 2.
Survival outcomes of pathological II–IIIB NSCLC patients in the VATS group and RATS groups. After propensity score matching: (A) DFS; (B) OS. CI, confidence interval; DFS, disease-free survival; NSCLC, non-small cell lung cancer; OS, overall survival; RATS, robotic-assisted thoracoscopic surgery; VATS, video-assisted thoracoscopic surgery.
Table 5. Univariate and multivariate analyses for disease-free survival.
| Variables | Univariate | Multivariate | |||||
|---|---|---|---|---|---|---|---|
| HR | 95% CI | P | HR | 95% CI | P | ||
| Age | 1.00 | 0.97–1.03 | 0.91 | 0.99 | 0.96–1.02 | 0.43 | |
| Sex (male/female) | 0.93 | 0.55–1.56 | 0.78 | 1.05 | 0.50–2.20 | 0.89 | |
| Smoking history (yes/no) | 0.87 | 0.51–1.48 | 0.60 | 0.80 | 0.36–1.80 | 0.59 | |
| No comorbidities (yes/no) | 0.68 | 0.39–1.17 | 0.16 | 0.54 | 0.29–1.00 | 0.051 | |
| Histology (adenocarcinoma/others) | 1.04 | 0.63–1.73 | 0.86 | 1.01 | 0.60–1.72 | 0.96 | |
| Pathological stage (III/II) | 1.53 | 0.96–2.44 | 0.07 | 1.70 | 1.04–2.80 | 0.03 | |
| Surgical approach (VATS/RATS) | 1.68 | 0.92–3.06 | 0.09 | 1.79 | 0.97–3.31 | 0.06 | |
| Adjuvant chemotherapy (yes/no) | 0.80 | 0.50–1.28 | 0.35 | 0.82 | 0.48–1.41 | 0.47 | |
CI, confidence interval; HR, hazard ratio; RATS, robotic-assisted thoracoscopic surgery; VATS, video-assisted thoracoscopic surgery.
Table 6. Univariate and multivariate analyses for overall survival.
| Variables | Univariate | Multivariate | |||||
|---|---|---|---|---|---|---|---|
| HR | 95% CI | P | HR | 95% CI | P | ||
| Age | 1.05 | 1.01–1.09 | 0.02 | 1.03 | 0.99–1.08 | 0.18 | |
| Sex (male/female) | 2.30 | 1.03–5.14 | 0.04 | 1.55 | 0.55–4.43 | 0.41 | |
| Smoking history (yes/no) | 2.85 | 1.12–7.24 | 0.03 | 1.60 | 0.48–5.34 | 0.45 | |
| No comorbidities (yes/no) | 0.28 | 0.11–0.70 | 0.006 | 0.30 | 0.11–0.80 | 0.02 | |
| Histology (adenocarcinoma/others) | 0.44 | 0.25–0.79 | 0.006 | 0.52 | 0.29–0.94 | 0.03 | |
| Pathological stage (III/II) | 1.45 | 0.81–2.59 | 0.21 | 2.10 | 1.15–3.83 | 0.02 | |
| Surgical approach (VATS/RATS) | 1.58 | 0.73–3.40 | 0.25 | 1.50 | 0.69–3.29 | 0.31 | |
| Adjuvant chemotherapy (yes/no) | 0.43 | 0.23–0.79 | 0.007 | 0.77 | 0.39–1.52 | 0.45 | |
CI, confidence interval; HR, hazard ratio; RATS, robotic-assisted thoracoscopic surgery; VATS, video-assisted thoracoscopic surgery.
Discussion
RATS for early-stage NSCLC patients has proven to be safe and effective and is therefore widely applied. The National Comprehensive Cancer Network (NCCN) guidelines version 3.2024 for NSCLC suggest that minimally invasive surgery (VATS or RATS) should be strongly considered for patients with no anatomic or surgical contraindications, provided there is no compromise between the standard oncologic and dissection principles of thoracic surgery (20). However, its application to more advanced stage NSCLC remains controversial. The main reasons for the low adoption were the concern about the increased risk of intraoperative complications, and most importantly, doubts about the ability to perform radical oncologic resection (21). Therefore, we analyzed the feasibility of RATS in more advanced stage NSCLC. In this study, we found that RATS for pathological stage II–III NSCLC resulted in significantly less blood loss (P=0.003) and a shorter postoperative hospital stay (P=0.01) than VATS. Furthermore, we found no statistically significant differences in the survival outcomes between the RATS and VATS groups.
Regarding the perioperative outcomes of the more advanced stage NSCLC, Pan et al. recently published the study comparing RATS, VATS, and thoracotomy for patients with N1 metastatic NSCLC (14). They demonstrated that RATS resulted in the shortest operative time, the least intraoperative blood loss, and the lowest rate of postoperative complications. Li et al. reported that the robotic approach resulted in a shorter postoperative hospital stay and a greater number of dissected lymph nodes (15). In our study, we also found that RATS was associated with less blood loss and a shorter postoperative hospital stay. The good results are attributed to several advantages of RATS, including three-dimensional visualization, which makes the operation more delicate, allows for more thorough hemostasis, and causes less irritation to the surrounding lung tissues. The operative time was longer in the RATS group than in the VATS group, but the difference was not statistically significant (P=0.08). This might have affected the results, as this study included initial attempts to perform RATS for stage II–III NSCLC.
In this study, we compared survival and other outcomes in patients with pathological stage II–IIIB disease rather than clinical stage. There are two reasons for this: (I) to include occult lymph node metastases; and (II) the different selection tendencies of the surgical approach concerning the clinical N stage of patients may cause selection bias. In the analysis of the clinical N stage, “overstaging” (clinical > pathological) N cases were included. Yoshino et al. reported a retrospective study of 11,663 resected lung cancer cases, in which 271 (33.8%) of 800 patients with clinical N2 were confirmed as pathological N0 cases (22). On the other hand, in the analysis of pathological N stage, it was possible to assess occult lymph node metastases. In our cases, the rate of occult lymph node metastases was over 30% of pathological stage II–IIIB NSCLC. Therefore, among pathological stage II–III NSCLC cases, patients with occult lymph node metastases comprised a significant population. Navani et al. assessed the agreement between clinical and pathological TNM stage, and reported that 131 (37.4%) of 350 pathological N1–2 cases had been confirmed as clinical N0 cases (23). Similarly, Yun et al. reported that 308 (43.6%) of 706 patients with pN2 who underwent surgery had been clinical N0 cases (24). Previous studies reported that unexpected pathological N1–2 was associated with poor prognosis, similarly to expected pathological N1–2 cases (25,26). Therefore, we thought that occult lymph node metastases should be analyzed in the study of stage II–III NSCLC.
Lymph node dissection is an important factor in the treatment of NSCLC. It not only clears metastatic lymph nodes but also provides an accurate stage assessment, which is essential for deciding whether adjuvant therapy is needed. Liang et al. reported that a greater number of examined lymph nodes is associated with more accurate node staging and better long-term survival in resected NSCLC (27). Previous studies showed that a greater number of lymph nodes could be resected in RATS in comparison to VATS (10-13,28-30). Meanwhile, there were also studies that the number of dissected lymph nodes was the same or higher in the VATS approach than in the RATS approach (8,31-33). The results of this study showed that the median number of dissected lymph nodes at the N1 and N2 level was not statistically significant between the two groups. This study included initial attempts to perform RATS for stage II–III NSCLC and a small sample size, which might have affected the results. Postoperative lymph node upstaging can also be used as an indicator of surgical quality. In this study, the rate of occult lymph node metastasis in both groups was 38.7% after PSM. According to previous studies, there was no significant difference in the upstaging rates with the two surgical approaches (30,33,34). Nevertheless, these results might indicate that RATS is not inferior to VATS.
Regarding survival outcomes, two meta-analyses have compared VATS and RATS. These studies revealed that the surgical approach was not an independent predictor of OS or DFS (11,13). However, most of the included studies focused on early-stage NSCLC. In terms of more advanced stage NSCLC, Pan et al. retrospectively reviewed 855 NSCLC patients with pathological N1 lymph nodal involvement who were treated by thoracotomy (n=350), RATS (n=70) and VATS (n=435). After PSM, the three surgical approaches were associated with similar DFS (P=0.56) and OS (P=0.77). Furthermore, a multivariate Cox regression model analysis revealed that the surgical approach was not individually associated with DFS or OS (14). Moreover, Li et al. confirmed that the robotic approach had similar long-term outcomes to VATS in clinical stage IIB–IIIA NSCLC. In detail, the median DFS in the RATS and VATS groups was 31.1 and 33.8 months, respectively. The 3-year OS rates were 75.7% in the RATS group and 77.0% in the VATS group (15). In our study, a positive trend was observed in survival outcomes after RATS relative to VATS. However, no statistically significant differences were found between the RATS and VATS groups in terms of survival outcomes. Similarly, in the multivariate analysis, the surgical approach was not independently associated with survival outcomes.
The present study was associated with several limitations. First, it was a retrospective study. We tried to minimize selection bias by applying PSM, but there was a considerable selection bias that may have influenced the outcomes between the two groups. This study included initial attempts to perform RATS for lung cancer, which was started at our hospital in September 2018. Accordingly, there may have been a patient selection bias. Therefore, randomized control studies or larger matched case-control studies might be essential to validate the conclusions of this study further. Second, the sample size of the two groups was relatively small and could only reflect the experience of a single center. According to the annual report by the Japanese Association for Thoracic Surgery, 9,896 (21.1%) of 46,848 patients with pathological stage II–IIIB underwent surgery for primary lung cancer during 2022 (35). Considering that thoracotomy is often applied for stage II–III cases, it would be meaningful to report this study performed by VATS or RATS, despite the small sample size. However, the statistical power was low and the findings should not be generalized because the outcomes are reflective of the current practice at a single institution. Therefore, multicenter studies with larger sample sizes are required to ensure the representativeness of this study. Finally, surgeon bias was evident because this study included the initial attempts to perform RATS for lung cancer. Furthermore, relationships such as improved nodal harvest, estimated blood loss, or length of hospital stay may be related to the surgeon rather than to the surgical approach. However, it is difficult to determine the relationship between surgeon-specific outcomes and the surgical approach.
Conclusions
In conclusion, our findings suggest that the RATS approach is feasible and is associated with comparable survival and perioperative outcomes to the VATS approach in patients with pathological stage II–III NSCLC. Additional multicenter studies are needed to ensure the representativeness of this study.
Supplementary
The article’s supplementary files as
Acknowledgments
We thank Brian Quinn for providing excellent English language editing assistance.
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 and its subsequent amendments. The study was approved by the institutional ethics committee of Nagoya City University (approval No. 60-24-0058) and individual consent for this retrospective analysis was waived.
Footnotes
Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-553/rc
Funding: None.
Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-553/coif). The authors have no conflicts of interest to declare.
Data Sharing Statement
Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-553/dss
References
- 1.Bendixen M, Jørgensen OD, Kronborg C, et al. Postoperative pain and quality of life after lobectomy via video-assisted thoracoscopic surgery or anterolateral thoracotomy for early stage lung cancer: a randomised controlled trial. Lancet Oncol 2016;17:836-44. 10.1016/S1470-2045(16)00173-X [DOI] [PubMed] [Google Scholar]
- 2.Novellis P, Maisonneuve P, Dieci E, et al. Quality of Life, Postoperative Pain, and Lymph Node Dissection in a Robotic Approach Compared to VATS and OPEN for Early Stage Lung Cancer. J Clin Med 2021;10:1687. 10.3390/jcm10081687 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Kent MS, Hartwig MG, Vallières E, et al. Pulmonary Open, Robotic, and Thoracoscopic Lobectomy (PORTaL) Study: An Analysis of 5721 Cases. Ann Surg 2023;277:528-33. 10.1097/SLA.0000000000005115 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Park BJ, Yang HX, Woo KM, et al. Minimally invasive (robotic assisted thoracic surgery and video-assisted thoracic surgery) lobectomy for the treatment of locally advanced non-small cell lung cancer. J Thorac Dis 2016;8:S406-S413. 10.21037/jtd.2016.04.56 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Cao J, Zhang C, Zhang X, et al. The Clinical Outcomes of Thoracoscopic Versus Open Lobectomy for Non-Small-Cell Lung Cancer After Neoadjuvant Therapy: A Multi-Center Retrospective Cohort Study. Clin Lung Cancer 2024;25:e153-60. 10.1016/j.cllc.2023.12.008 [DOI] [PubMed] [Google Scholar]
- 6.Gonfiotti A, Bongiolatti S, Bertolaccini L, et al. Thoracoscopic lobectomy for locally advanced-stage non-small cell lung cancer is a feasible and safe approach: analysis from multi-institutional national database. J Vis Surg 2017;3:160. 10.21037/jovs.2017.09.06 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Chen K, Wang X, Yang F, et al. Propensity-matched comparison of video-assisted thoracoscopic with thoracotomy lobectomy for locally advanced non-small cell lung cancer. J Thorac Cardiovasc Surg 2017;153:967-976.e2. 10.1016/j.jtcvs.2016.12.008 [DOI] [PubMed] [Google Scholar]
- 8.Huang S, Huang X, Huang Z, et al. Comparison of robot-assisted thoracic surgery versus video-assisted thoracic surgery in the treatment of lung cancer: a systematic review and meta-analysis of prospective studies. Front Oncol 2023;13:1271709. 10.3389/fonc.2023.1271709 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Veronesi G, Novellis P, Voulaz E, et al. Robot-assisted surgery for lung cancer: State of the art and perspectives. Lung Cancer 2016;101:28-34. 10.1016/j.lungcan.2016.09.004 [DOI] [PubMed] [Google Scholar]
- 10.Wang P, Fu YH, Qi HF, et al. Evaluation of the efficacy and safety of robot-assisted and video assisted thoracic surgery for early non-small cell lung cancer: A meta-analysis. Technol Health Care 2024;32:511-23. 10.3233/THC-230201 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Zhang J, Feng Q, Huang Y, et al. Updated Evaluation of Robotic- and Video-Assisted Thoracoscopic Lobectomy or Segmentectomy for Lung Cancer: A Systematic Review and Meta-Analysis. Front Oncol 2022;12:853530. 10.3389/fonc.2022.853530 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Veronesi G, Abbas AE, Muriana P, et al. Perioperative Outcome of Robotic Approach Versus Manual Videothoracoscopic Major Resection in Patients Affected by Early Lung Cancer: Results of a Randomized Multicentric Study (ROMAN Study). Front Oncol 2021;11:726408. 10.3389/fonc.2021.726408 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Tasoudis PT, Diehl JN, Merlo A, et al. Long-term outcomes of robotic versus video-assisted pulmonary lobectomy for non-small cell lung cancer: systematic review and meta-analysis of reconstructed patient data. J Thorac Dis 2023;15:5700-13. 10.21037/jtd-23-582 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Pan H, Tian Y, Wang H, et al. Perioperative and Oncological Outcomes of Robotic-Assisted, Video-Assisted Thoracoscopic and Open Lobectomy for Patients with N1-Metastatic Non-Small Cell Lung Cancer: A Propensity Score-Matched Study. Cancers (Basel) 2022;14:5249. 10.3390/cancers14215249 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Li C, Hu Y, Huang J, et al. Comparison of robotic-assisted lobectomy with video-assisted thoracic surgery for stage IIB-IIIA non-small cell lung cancer. Transl Lung Cancer Res 2019;8:820-8. 10.21037/tlcr.2019.10.15 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Veronesi G, Park B, Cerfolio R, et al. Robotic resection of Stage III lung cancer: an international retrospective study. Eur J Cardiothorac Surg 2018;54:912-9. 10.1093/ejcts/ezy166 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Shahin GMM, Vos PWK, Hutteman M, et al. Robot-assisted thoracic surgery for stages IIB-IVA non-small cell lung cancer: retrospective study of feasibility and outcome. J Robot Surg 2023;17:1587-98. 10.1007/s11701-023-01549-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Zirafa CC, Romano G, Sicolo E, et al. Robotic versus Open Surgery in Locally Advanced Non-Small Cell Lung Cancer: Evaluation of Surgical and Oncological Outcomes. Curr Oncol 2023;30:9104-15. 10.3390/curroncol30100658 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Rami-Porta R, Bolejack V, Giroux DJ, et al. The IASLC lung cancer staging project: the new database to inform the eighth edition of the TNM classification of lung cancer. J Thorac Oncol 2014;9:1618-24. [DOI] [PubMed] [Google Scholar]
- 20.NCCN. NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines) Version 3.2024: Non-Small Cell Lung Cancer. Accessed on October 15, 2024. Available online: https://crain-platform-precisiononcologynews-prod.s3.amazonaws.com/2024-04/nscl_NCCN%20guidelines.pdf
- 21.Patané AK. Minimal invasive surgery in locally advanced N2 non-small cell lung cancer. Transl Lung Cancer Res 2021;10:519-28. 10.21037/tlcr.2020.03.27 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Yoshino I, Yoshida S, Miyaoka E, et al. Surgical outcome of stage IIIA- cN2/pN2 non-small-cell lung cancer patients in Japanese lung cancer registry study in 2004. J Thorac Oncol 2012;7:850-5. 10.1097/JTO.0b013e31824c945b [DOI] [PubMed] [Google Scholar]
- 23.Navani N, Fisher DJ, Tierney JF, et al. The Accuracy of Clinical Staging of Stage I-IIIa Non-Small Cell Lung Cancer: An Analysis Based on Individual Participant Data. Chest 2019;155:502-9. 10.1016/j.chest.2018.10.020 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Yun JK, Bok JS, Lee GD, et al. Long-term outcomes of upfront surgery in patients with resectable pathological N2 non-small-cell lung cancer. Eur J Cardiothorac Surg 2020;58:59-69. 10.1093/ejcts/ezaa042 [DOI] [PubMed] [Google Scholar]
- 25.Cai JS, Yang F, Wang X. Occult lymph node metastasis is not a favorable factor for resected NSCLC patients. BMC Cancer 2023;23:822. 10.1186/s12885-023-11189-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Kamigaichi A, Tsutani Y, Mimae T, et al. Prediction of Unexpected N2 Disease Associated With Clinical T1-2N0-1M0 Non-Small-Cell Lung Cancer. Clin Lung Cancer 2021;22:120-126.e3. 10.1016/j.cllc.2020.12.010 [DOI] [PubMed] [Google Scholar]
- 27.Liang W, He J, Shen Y, et al. Impact of Examined Lymph Node Count on Precise Staging and Long-Term Survival of Resected Non-Small-Cell Lung Cancer: A Population Study of the US SEER Database and a Chinese Multi-Institutional Registry. J Clin Oncol 2017;35:1162-70. 10.1200/JCO.2016.67.5140 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Li JT, Liu PY, Huang J, et al. Perioperative outcomes of radical lobectomies using robotic-assisted thoracoscopic technique vs. video-assisted thoracoscopic technique: retrospective study of 1,075 consecutive p-stage I non-small cell lung cancer cases. J Thorac Dis 2019;11:882-91. 10.21037/jtd.2019.01.78 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Merritt RE, Abdel-Rasoul M, D'Souza DM, et al. Comparison of the long-term oncologic outcomes of robotic-assisted and video-assisted thoracoscopic lobectomy for resectable non-small cell lung carcinoma. J Robot Surg 2022;16:1281-8. 10.1007/s11701-022-01368-y [DOI] [PubMed] [Google Scholar]
- 30.Nelson DB, Mehran RJ, Mitchell KG, et al. Robotic-Assisted Lobectomy for Non-Small Cell Lung Cancer: A Comprehensive Institutional Experience. Ann Thorac Surg 2019;108:370-6. 10.1016/j.athoracsur.2019.03.051 [DOI] [PubMed] [Google Scholar]
- 31.Rajaram R, Mohanty S, Bentrem DJ, et al. Nationwide Assessment of Robotic Lobectomy for Non-Small Cell Lung Cancer. Ann Thorac Surg 2017;103:1092-100. 10.1016/j.athoracsur.2016.09.108 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Huang J, Tian Y, Zhou QJ, et al. Comparison of perioperative outcomes of robotic-assisted versus video-assisted thoracoscopic right upper lobectomy in non-small cell lung cancer. Transl Lung Cancer Res 2021;10:4549-57. 10.21037/tlcr-21-960 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Kneuertz PJ, D'Souza DM, Richardson M, et al. Long-Term Oncologic Outcomes After Robotic Lobectomy for Early-stage Non-Small-cell Lung Cancer Versus Video-assisted Thoracoscopic and Open Thoracotomy Approach. Clin Lung Cancer 2020;21:214-224.e2. 10.1016/j.cllc.2019.10.004 [DOI] [PubMed] [Google Scholar]
- 34.Merritt RE, Abdel-Rasoul M, D'Souza DM, et al. Lymph Node Upstaging for Robotic, Thoracoscopic, and Open Lobectomy for Stage T2-3N0 Lung Cancer. Ann Thorac Surg 2023;115:175-82. 10.1016/j.athoracsur.2022.05.041 [DOI] [PubMed] [Google Scholar]
- 35.Committee for Scientific Affairs , The Japanese Association for Thoracic Surgery, Yoshimura N, Sato Y, et al. Thoracic and cardiovascular surgeries in Japan during 2022 : Annual report by the Japanese Association for Thoracic Surgery. Gen Thorac Cardiovasc Surg 2025;73:254-94. 10.1007/s11748-024-02106-x [DOI] [PMC free article] [PubMed] [Google Scholar]


