Ten-year survival outcomes of video-assisted thoracic surgery vs. open major lung resection for stage I–III non-small cell lung cancer: a large cohort study in China

Introduction

Since the introduction of video-assisted thoracic surgery (VATS) for the treatment of lung cancer, minimally invasive major lung resection has been recommended as the preferred method for early-stage lung cancer in numerous evidence-based guidelines (1-4). However, for oncologic surgery, the most important evaluation metric is long-term survival outcomes, and long-term survival after minimally invasive surgery is not necessarily superior to that of open surgery (5,6). In recent years, there has been substantial evidence confirming the advantages of VATS over open surgery for non-small cell lung cancer (NSCLC), but after years of widespread adoption of the VATS approach, only a few articles have comprehensively compared the prognostic differences between VATS and open surgery in the treatment of lung cancer beyond 5 years (7-14).

Evaluations of the efficacy of VATS and open surgery in patients with different stages of lung cancer have been inconsistent, and evaluations of 10-year survival outcomes are lacking (11-14). In a previous study, we concluded that VATS lobectomy provided better 5-year survival rates than did the open approach and should be the preferred surgical treatment for stage I–II NSCLC (11). The present large single-center cohort study evaluated the outcomes of VATS and open major lung resection performed by experienced surgeons and reported the 10-year survival outcomes of these patients. This study also analyzed the short-term results of surgery and total in-hospital costs of VATS vs. open major lung resection using data from the Western China Lung Cancer Database (WCLCD). The database collected data on lung cancer patients undergoing surgery at West China Hospital of Sichuan University. We present this article in accordance with the STROBE reporting checklist (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-24-150/rc).

Methods

Data source

The WCLCD was established in September 2005. Since then, all lung cancer patients who underwent surgery at the Department of Thoracic Surgery, West China Hospital, Sichuan University, have been registered in the database. The database is currently updated through May 2023. The study conformed to the provisions of the Declaration of Helsinki (as revised in 2013) and was approved by the Institutional Review Board (IRB) of West China Hospital (No. 2023-1406). Individual consent for this retrospective analysis was waived.

Patient and method

All patients who underwent VATS or open lung cancer resection at the Department of Thoracic Surgery, West China Hospital, Sichuan University, between May 2006 and June 2018 were recruited for this study. The inclusion criteria included VATS or open major lung resection (including lobectomy, bilobectomy, pneumonectomy and lobectomy combined with sublobectomy) for postoperative stage I–III NSCLC according to the 8^th edition of the tumor, node and metastasis (TNM) staging system after surgery. The exclusion criteria were as follows: VATS or open access (video-assisted mini-thoracoscopy was also considered VATS), non-lobectomy (segmental resection, wedge resection, sleeve resection, bilateral surgery, chest wall resection or other extended resection), stage IV NSCLC with pulmonary metastases, incomplete data, or positive surgical margins.

We adopted a propensity score matching (PSM) approach to minimize potential selection bias, balancing confounding factors between the two groups with a 1:1 nearest matching approach. Matching indicators included sex (male, female), age at the time of surgery (<60 years, ≥60 years), smoking history (never smoked, current or ever smoked), Charlson comorbidity index (CCI), side of surgery (right, left), histology (adenocarcinoma, squamous, adenosquamous carcinoma and other types of primary NSCLC), p-T status (8^th edition of TNM staging system: T1, T2, T3), p-N status (8^th edition of TNM staging system: N0, N1, N2) and adjuvant therapy. The patient inclusion process is shown in Figure 1.

Figure 1 Study subject selection (pathological stage I–III patients). NSCLC, non-small cell lung cancer; VATS, video-assisted thoracic surgery.

Outcomes

The primary outcomes were 10-year overall survival (OS), 5-year recurrence-free survival (RFS) and lung cancer-specific survival (LCSS). Patient follow-up began on the day of surgery, and patient status was determined based on periodic follow-up [including chest computed tomography (CT), brain magnetic resonance imaging or CT, and upper abdominal CT]. Follow-up was performed every 3–6 months for the first 3 years, every 6 months for the next 2 years, and once a year thereafter. In addition, patients should undergo a bone scan every year to detect bone metastases, and positron emission tomography (PET)-CT or biopsy may be performed if necessary. Patients who did not return to the outpatient clinic were followed up with regular telephone visits.

The secondary outcomes included VATS conversion rate, intraoperative blood loss volume, postoperative complications, chest tube duration, postoperative length of stay, and total hospital costs. Postoperative complications included prolonged air leakage (>5 days), pneumonia, bronchopleural fistula (BPF), empyema, chylothorax, reoperation, pulmonary embolism, arrhythmia, reintubation, and 30-day mortality.

Statistical analysis

All the statistical analyses were performed using R (version 4.2.1). Quantitative data were expressed as the mean ± standard deviation. Independent samples t tests were used to compare differences between groups. Enumerated data were expressed as percentages, and differences between groups were compared using Fisher’s exact test or the Chi-square test. Kaplan-Meier survival curves were used to describe the OS and RFS times before and after PSM in both groups, and survival outcomes were compared using log-rank tests. In addition, Cox regression models were used to determine independent prognostic factors for these patients. Missing data for each variable were assessed independently and evaluated if it was missing at random or systematically, potentially introducing selection bias. A P value <0.05 indicated statistical significance.

Results

Patient characteristics

A total of 10,167 patients underwent surgery for pulmonary malignancies in the Department of Thoracic Surgery, West China Hospital, Sichuan University, between May 2006 and June 2018. A total of 3,762 patients were excluded based on the exclusion criteria, while the remaining 6,405 patients were included in the study (including 4,224 patients who underwent major lung resection via VATS and 2,181 patients who underwent major lung resection via open surgery). The subsequent PSM identified 1,487 patients who underwent major lung resection via VATS and 1,487 patients who underwent open major lung resection based on patient demographics, CCI, tumor histology, and TNM stage.

Unmatched population

Patient characteristics are shown in Table 1. Patients who underwent major lung resection via VATS were older than those in the open group (47.6% vs. 42.5% of patients in the ≥60 years group, P<0.001). Compared with the open group, the VATS group had more female patients and more patients with comorbidities but fewer current or former smokers. The mean tumor size was smaller in the VATS group than in the open group (2.7±2.1 vs. 4.5±2.0 cm, P<0.001). The proportion of patients with adenocarcinoma was greater in the VATS group than in the open group (79.5% vs. 42.4%, P<0.001). More patients in the VATS group than in the open group had p-TNM stage I disease (70.7% vs. 31.9%, P<0.001).

In the VATS group, 190 (4.0%) patients were converted to open surgery (Table 2). Compared with open major lung resection, major lung resection via VATS resulted in less blood loss (median: 50 vs. 100 mL, P<0.001), shorter operation times (145 vs. 156 min, P<0.001) and more harvested lymph node stations (5.6±1.6 vs. 5.3±1.8, P<0.001) but fewer lymph nodes harvested (11.6±6.4 vs. 14.0±8.6, P<0.001).

The overall postoperative complication rate was significantly lower in the VATS group (18.4% vs. 23.0%, P<0.001). The VATS approach was associated with a lower incidence of postoperative pneumonia (3.0% vs. 5.4%, P<0.001), less frequent development of a BPF and/or empyema (0.2% vs. 0.5%, P<0.001) and a lower risk of mortality within 30 days (0.3% vs. 0.8%, P=0.009). Compared with the open group, the VATS group had shorter chest tube drainage times (4.2±3.3 vs. 4.5±2.8 days, P<0.001) and shorter postoperative hospital stays (7.1±5.9 vs. 8.8±4.9 days, P<0.001). However, the VATS group had a higher incidence of postoperative air leakage (6.0% vs. 4.6%, P=0.03) and a higher total hospitalization cost (53.8±17.0 vs. 43.6±16.5 kRMB, P<0.001).

Matched population

The baseline clinical characteristics and surgical outcomes of the PSM-matched patients are listed in Tables 3,4. The two groups were comparable in terms of age, sex, comorbidities, smoking status, tumor size, histology, and TNM stage. The blood loss volume was lower in matched VATS major lung resection patients than in open major lung resection patients (median blood loss: 50 vs. 100 mL, P<0.001). There was no significant difference in the overall incidence of postoperative complications between the matched VATS group and the open group (21.3% vs. 21.7%, P=0.39), and major lung resection via VATS was associated with a higher incidence of postoperative air leakage (7.2% vs. 4.6%, P=0.004). Patients who underwent open major lung resection still had longer postoperative hospital stays (7.6±6.0 vs. 8.6±4.9 days, P<0.001), but total hospital costs were higher in the VATS group than in the open major lung resection group (52.5±21.2 vs. 45.0±16.4 kRMB, P<0.001).

Long-term outcomes

In the 6,504 patients included in this study, the 5-year survival rate was 69.8%, the 10-year survival rate was 54.5%, and the 5-year RFS rate was 58.9%. Patients with stage I–III NSCLC who underwent major lung resection via VATS had significantly better 5-year and 10-year survival rates than did those who underwent major lung resection via open surgery (5-year survival rate: 77.1% vs. 55.9%; 10-year survival rate: 62.8% vs. 42.5%, P<0.001) (Figure 2). Moreover, patients with stage I–III NSCLC who underwent major lung resection via VATS had better RFS (5-year RFS: 66.2% vs. 45.0%, P<0.001) and LCSS (5-year LCSS rate: 82.2% vs. 63.0%; 10-year LCSS rate: 71.7% vs. 52.6%, P<0.001) (Figure 3, Figure S1). The descriptions of recurrence sites or metastatic patterns are shown in Table 3. Multivariate adjusted survival analysis revealed that the VATS approach was associated with superior long-term survival [hazard ratio (HR) =0.83; 95% confidence interval (CI): 0.74–0.94; P<0.001] (Table 4). Other independent predictors of OS included age at the time of surgery, sex, tumor size, and pT and pN stages (Table 4).

Figure 2 OS of p-stage I–III NSCLC patients stratified by VATS vs. open lobectomy. VATS, video-assisted thoracic surgery; OS, overall survival; NSCLC, non-small cell lung cancer.

Figure 3 Recurrence-free survival of p-stage I–III NSCLC patients stratified by surgery vs. open lobectomy. VATS, video-assisted thoracic surgery; NSCLC, non-small cell lung cancer.

After PSM analysis, compared with open major lung resection, major lung resection via VATS still had better OS, RFS and LCSS [5-year survival rate: 64.9% vs. 57.7%; 10-year survival rate: 47.8% vs. 42.6%, P<0.001; 5-year RFS: 50.3% vs. 45.3%, P=0.003; and LCSS (5-year LCSS rate: 71.2% vs. 63.0%; 10-year LCSS rate: 59.3% vs. 52.6%; P<0.001)] (Figures 4,5, Figure S2). According to our subgroup analysis, only stage II NSCLC patients who underwent major lung resection via VATS had better OS and RFS (OS: P<0.001; RFS: P=0.004), while the difference was not significant between stage I and stage III NSCLC patients.

Figure 4 Overall survival of p-stage I–III NSCLC patients stratified by VATS vs. open lobectomy after propensity score-matched analysis. NSCLC, non-small cell lung cancer; VATS, video-assisted thoracic surgery.

Figure 5 Recurrence free survival of p-stage I–III NSCLC patients stratified by VATS vs. open lobectomy after propensity score-matched analysis. NSCLC, non-small cell lung cancer; VATS, video-assisted thoracic surgery.

Discussion

Owing to advances in television imaging systems and endoscopic cutting and suturing instruments in the 2000s, thoracoscopic surgery has been developed rapidly, and an increasing number of complex surgeries have been performed through thoracoscopic surgery in recent years. However, despite the various benefits of minimally invasive surgery, it still needs to be proven that its perioperative outcomes and long-term survival are not inferior to those of conventional surgery before it can be called a more advanced surgical approach (15,16). VATS has long been validated worldwide for its safety and efficacy (17-25). The advantages of the VATS operation over the open operation are that it results in less trauma to the patient and faster postoperative recovery. However, the most worrying aspect of major lung resection in VATS is that it could have limited visibility and handling capabilities compared to open surgery. According to published results, major lung resection via VATS is not only noninferior but also has lower 90-day mortality rates, less pain, fewer complications and better quality of life without compromising oncologic outcomes (18,22,25). Previously reported outcomes have been dominated by perioperative outcomes and 5-year survival outcomes, with little mention of long-term survival outcomes beyond 10 years. The aim of this study was to report long-term follow-up data from a high-volume center and to analyze the differences in perioperative outcomes and long-term survival outcomes between VATS major lung resection and open major lung resection.

In this study, we enrolled stage III NSCLC patients to investigate whether VATS was suitable for this group of patients. To answer the question of whether this group of patients is suitable for VATS, the present study included patients who underwent extended major lung resection rather than solely lobectomy, which included pneumonectomy, bilobectomy and lobectomy combined with sublobectomy. Our results showed that patients who underwent bilobectomy or lobectomy combined with sublobectomy had better survival times than did patients who underwent VATS alone, and there was no significant difference in survival time between the two surgical approaches for patients who underwent pneumonectomy (Table 4).

The most important finding of this study was that patients with stage I–III NSCLC who underwent major lung resection via VATS had better 10-year OS and 5-year RFS times than did those who underwent open major lung resection in both the unmatched and matched cohorts. In terms of perioperative outcomes, the overall postoperative complication rate in the VATS group was not significantly different from that in the open group. Notably, prolonged air leakage (>5 days) was more common in the VATS group after matching. However, there was no significant difference in postoperative chest tube duration. The VATS group had less intraoperative bleeding and shorter operative times and postoperative hospital stays than did the open group, which is consistent with the findings of many retrospective studies (9,11,12,26,27). Therefore, we believe that VATS is a safer surgical procedure than open surgery.

In our study, we found that the VATS approach was more expensive than the open approach because of the higher cost of surgical consumables. Several previous reports have shown that the increased surgical costs of major lung resection via VATS are compensated for by lower postoperative costs, improved postoperative prognosis and shorter hospital stays (14,28-30). In China, VATS is not more cost-efficient than is open surgery because of the use of staplers and other cost-related sealants or developing instruments, despite their potential to shorten hospital stays. This is attributed to the health care insurance system in China, which significantly reduces hospitalization costs, making them far lower than the costs of consumables.

Regarding survival outcomes, many articles have concluded that there is no significant difference in survival between patients who underwent major lung resection via VATS and those who underwent open surgery (26,27,31-33), and even patients who underwent open surgery had better survival outcomes (13). To reduce bias, we performed PSM on the included patients and stratified the matched patients by p-TNM stage. After matching, we found that the advantages of major lung resection in terms of OS and RFS were associated with stage II NSCLC. This result differs from the data provided by other national databases, and the discrepancy may be due to differences in the development of VATS and open surgery for major lung resection (34-36). For stage I and III patients, the choice of surgical approach did not affect their survival outcomes, as confirmed in other articles (26,31,37). Overall, VATS is the preferred surgical option for patients with stage I–III NSCLC with better long-term survival outcomes and superior perioperative outcomes.

Limitations to this study should also be acknowledged. First, this was a retrospective study. Although the Cox regression model and PSM can help reduce bias, the retrospective nature of the study may have led to unobserved confounding and selection bias between the two groups. Second, this was a single-center study from a high-volume center in China. Whether this study is representative of the reality in China requires further confirmation in a larger multicenter study. Finally, the proportion of VATS lobectomies increased annually over the study period, from 6.6% in 2006 to 96.5% in 2018. As an increasing number of lung cancer resections are performed via VATS, comparative studies are somewhat biased over time, and this bias is difficult to eliminate by PSM analysis.

Conclusions

In summary, the present study confirmed that major lung resection via VATS provides better 5-year RFS and 10-year OS than does the open approach. VATS major lung resection could be considered the preferred surgical option for stage I–III NSCLC due to its better survival outcomes and advantages of less blood loss and shorter postoperative hospital stays.

Acknowledgments

Funding: This study was funded by the 1.3.5 Project for Disciplines of Excellent, West China Hospital, Sichuan University (No. ZYJC21002, to L.L.) and Science and Technology Project of the Health Planning Committee of Sichuan Province, China (No. 21PJ001 to C.G.).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-24-150/rc

Data Sharing Statement: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-24-150/dss

Peer Review File: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-24-150/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-24-150/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 conformed to the provisions of the Declaration of Helsinki (as revised in 2013) and was approved by the Institutional Review Board (IRB) of West China Hospital (No. 2023-1406). 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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