Compared with assessment via endoscopic examination, assessment through the examination of resected regional lymph nodes can significantly reduce the mortality rate of lung cancer patients: a retrospective study of 222,563 participants from the SEER database

Introduction

The 2022 Global Cancer Statistics released by the International Agency for Research on Cancer (IARC) identified lung cancer as the most commonly diagnosed cancer worldwide (1), with nearly 2.5 million new cases, accounting for one-eighth (12.4%) of all global cancer cases. Lung cancer is also the leading cause of cancer-related mortality, being responsible for an estimated 1.8 million deaths (18.7% of all cancer deaths). Moreover, it is the most prevalent type of cancer, with approximately 1.06 million new cases and 733,300 deaths in 2022, the highest number in the world among malignancies according to the National Cancer Registry of China (2). These statistics highlight the critical need for improving the survival of patients with lung cancer.

Regular nodes evaluation plays a crucial role in predicting outcomes in patients with lung cancer (3). A variety of methods for preoperatively evaluating the lymph nodes of patients with lung cancer have been devised, including fluorodeoxyglucose positron emission tomography (FDG-PET) (4), clinical bioradiomics (CBR) (5), anti-carcinoembryonic antigen (CEA) immunoscintigraphy (6), virtual monoenergetic low-kiloelectron volt imaging (7), surgical removal of lymph nodes (8), endobronchial ultrasound guided transbronchial needle aspiration (EBUS-TBNA) (9-11).

Despite variety of techniques available, surgically removal of lymph nodes and endoscopic puncture biopsy remain the most extensively used and accurate methods for obtaining preoperative lymph node samples. However, controversy persists regarding whether detection via surgical removal of lymph nodes or endoscopic puncture biopsy is more beneficial. Some argue that surgical removal of lymph nodes has more advantages, although the specific impact of these methods on patient survival remains unclear.

The Surveillance, Epidemiology, and End Results (SEER) database, an authoritative source of cancer statistics (https://seer.cancer.gov/) supported by the Surveillance Research Program (SRP) of the National Cancer Institute Division of Cancer Control and Population Sciences (DCCPS) (12), provides vital cancer statistics to help reduce the cancer burden in the U.S. population. The SEER database is distinguished among many open-access databases, being extensively used in the medical field and contributing substantially to its advancement. The SEER database acts as a spur in driving the progress in precision medicine and facilitates the expansion of individualized therapies.

On a broader scale, SEER helps improve healthcare, reduces unnecessary medical expenses, and enables more targeted and efficient preventive measures. It also encourages the public to adopt healthier lifestyles, enhances health literacy, and contributes significantly to the overall health of the society (13-15).

This study conducted an in-depth and comprehensive analysis based on sample data from 222,563 lung cancer patients, comparing the differences in patient prognosis between the assessment via the examination of resected regional lymph nodes and the assessment through endoscopic examination. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-821/rc).

Methods

Data sources

The data for this study were obtained from SEER databases, specifically the Incidence SEER Research Plus Data, 17 registries, and the November 2021 Sub [2000–2019]. This dataset represents approximately 26.5% of the U.S. population (based on the 2020 census) and covers regions including San Francisco (SF)-Oakland Standard Metropolitan Statistical Area, Connecticut, Hawaii, Iowa, New Mexico, Seattle (Puget Sound), Utah, Atlanta (Metro), San Jose-Monterey (SJM), Los Angeles (LA), Alaska Native, Rural Georgia, California (excluding SF, SJM, and LA), Kentucky, Louisiana, New Jersey, and Greater Georgia. The specific sites of focus were the lung and bronchus (site recode: IOD .0.3/ World Health Organization 2008).

Regarding the patient follow-up methods, The Tumor Registry Department follows all cancer patients on a yearly basis after they have been diagnosed and given first course of treatment. For details, see (https://training.seer.cancer.gov/followup/requirements.html).

Based on the regional nodes evaluation method, we categorized patients into three groups for screening: endoscopic examination/diagnostic biopsy, assessment through the examination of resected regional lymph nodes, and assessment based on physical examination, imaging studies, or other non-invasive clinical evidence. In the end, a total of 222,563 participants were included in this study. The patient inclusion and exclusion process are detailed in Figure 1.

Figure 1 Flowchart of participant inclusion. CS, Collaborative Stage; SEER, Surveillance, Epidemiology, and End Results.

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study received approval from the Ethics Review Committee of the First Affiliated Hospital of Zhejiang University School of Medicine (approval No. IIT20241665A).

Variables and study design

The outcome variables of this study were the survival of patients with lung cancer, including overall survival (OS) and lung cancer-specific mortality (CSS). The independent variable was the regional nodes evaluation method. Fifteen covariates were included: age; sex; race; total number of malignant tumors; histology; tumor size; regional nodes positive; grade; primary site; laterality; stage; median household income; surgery; radiation; chemotherapy. Model I was adjusted for: none. Model II was adjusted for: age; sex; race. Model III was adjusted for: age; sex; race; total number of malignant tumors; histology; tumor size; regional nodes positive; grade; primary site; laterality; stage; median household income; surgery; radiation; chemotherapy.

Collaborative Stage (CS) Regular Nodes Evaluation: variable 0 represents no regional lymph nodes removed for examination; evaluation based on physical examination, imaging, or other non-invasive clinical evidence; variable 1 represents no regional lymph nodes removed for examination; evaluation based on endoscopic examination, diagnostic biopsy including fine needle aspiration of lymph node(s) or other invasive techniques; variable 3 represents regional lymph nodes removed for examination (removal of at least 1 lymph node) without pre-surgical systemic treatment or radiation or lymph nodes removed for examination. For details, see (https://www.training.seer.cancer.gov/collaborative/system/evaluation/reg_nodes.html).

Statistical analysis

Statistical analysis was performed using frequency function statistics and SPSS v. 24 (IBM Corp., Armonk, NY, USA). Survival curves for different subgroups were drawn using GraphPad Prism 8 (Dotmatics, Boston, MA, USA). Life table analysis, Kaplan-Meier survival analysis, and univariate and multivariate Cox proportional hazard analyses were conducted on the patient data. The log-rank (Mantel-Cox), Breslow (generalized Wilcoxon), and Tarone-Ware tests were used to compare survival data distributions between the groups. Mean survival time and 1-, 2-, 3-, 5-, 10-, and 15-year survival rates of patients with lung cancer were calculated. Univariate and multivariate analyses were conducted using Empower Stats software (X&Y Solutions, Inc., Boston, MA, USA; www.empowerstats.net).

Results

Baseline characteristics

The baseline characteristics of the patients (N=222,563) showed significant differences across all evaluated variables (all P<0.001). The population was predominantly elderly, with 33.05% aged 70–79 years and 21.60% aged ≥80 years. Tumor size was ≥40 mm in 32.54% of cases. Lymph node evaluation was missing in 69.70% of cases, while 12.04% had positive regional nodes. Treatment-wise, only 24.01% underwent surgery, 34.87% received radiation, and 41.34% received chemotherapy. Median household income was distributed across four categories, with 33.68% of patients having an income ≥$75,000 (Table 1).

Kaplan-Meier survival curves (OS and CSS)

Figure 2A presents the OS curve of patients with lung cancer who underwent surgery. Figure 2B depicts the OS curves of surgical patients with lung cancer stratified by the regional lymph nodes evaluation method, which indicates significantly better survival for those who underwent lymph node biopsy resection as compared to those who underwent endoscopic lymph node biopsy. Figure 2C-2Q shows the Kaplan-Meier survival curves (OS) for patients with lung cancer, stratified by the covariates, including age; sex; race; total number of malignant tumors; histology; tumor size; regional nodes positive; grade; primary site; laterality; stage; median household income; surgery; receipt of radiotherapy; receipt of chemotherapy.

Figure 2 Kaplan-Meier survival curves of patient with lung cancer (OS). (A) Overall survival curve. (B) Prognosis of lung cancer patients with different regional lymph node evaluation methods, overall survival rate. (C) Age stratification: overall survival rate. (D) Sex stratification: overall survival rate. (E) Race stratification: overall survival rate. (F) Total number of malignant tumors stratification: overall survival rate. (G) Histology stratification: overall survival rate. (H) Tumor size stratification: overall survival rate. (I) Regional node-positive stratification: overall survival rate. (J) Stage stratification: overall survival rate. (K) Grade stratification: overall survival rate. (L) Primary site stratification: overall survival rate. (M) Laterality stratification: overall survival rate. (N) Median household income stratification: overall survival rate. (O) Surgery stratification: overall survival rate. (P) Radiation stratification: overall survival rate. (Q) Chemotherapy stratification: overall survival rate. OS, overall survival.

Figure 3A presents the CSS curve of the same group. Figure 3B presents the lung cancer-specific survival curves, similarly indicating superior outcomes for patients undergoing regional lymph nodes removed for examination. Figure 3C-3Q shows the Kaplan-Meier survival curves (lung cancer-specific death) for patients with lung cancer, stratified by the 15 covariates.

Figure 3 Kaplan-Meier survival curves of patient with lung cancer (lung cancer-specific mortality). (A) Cancer-specific death curve. (B) Prognosis of lung cancer patients with different regional lymph node evaluation methods, cancer-specific death rate. (C) Age stratification: cancer-specific death rate. (D) Sex stratification: cancer-specific death rate. (E) Race stratification: cancer-specific death rate. (F) Total number of malignant tumors stratification: cancer-specific death rate. (G) Histology stratification: cancer-specific death rate. (H) Tumor size stratification: cancer-specific death rate. (I) Regional node-positive stratification: cancer-specific death rate. (J) Stage stratification: cancer-specific death rate. (K) Grade stratification: cancer-specific death rate. (L) Primary site stratification: cancer-specific death rate. (M) Laterality stratification: cancer-specific death rate. (N) Median household income stratification: cancer-specific death rate. (O) Surgery stratification: cancer-specific death rate. (P) Radiation stratification: cancer-specific death rate. (Q) Chemotherapy stratification: cancer-specific death rate.

Kaplan-Meier survival curves (stratified by whether surgery was performed, OS and CSS)

Figure 4 (A1-B4) depicts the survival curves (surgical, OS, and CSS) of lung cancer patients stratified by lymph node assessment methods, staging, radiotherapy, and chemotherapy. Figure 4 (C1-4D4) shows the survival curves (Non-surgical, OS, and CSS) of lung cancer patients stratified in the same manner.

Figure 4 The prognosis of lung cancer patients (surgical patients and non-surgical patients) with different stratification variables (stratified by regional nodes evaluation methods, stage, radiotherapy and chemotherapy). (A1-A4) OS of surgical patients. (B1-B4) Lung cancer-specific death rate of surgical patients. (C1-C4) OS of nonsurgical patients. (D1-D4) Lung cancer-specific death rate of nonsurgical patients. Cause-specific mortality: lung cancer-specific mortality. OS, overall survival.

Among surgical patients, the survival curve for those who underwent “regional lymph nodes removed for examination” indicated a better survival prognosis compared to the other two assessment methods (Figure 4, A1,B1). In contrast, among non-surgical patients, the magnitude of survival differences among the three assessment methods was significantly reduced (Figure 4, C1,D1).

Regardless of whether they received surgery, the survival prognosis of lung cancer patients gradually deteriorated with advancing staging. However, the survival curves of patients with stage IIA and stage II lung cancer were relatively close. In surgical patients, those who did not receive radiotherapy had a better survival prognosis, whereas among non-surgical patients, those who received radiotherapy had a better survival prognosis. In surgical patients, those who did not receive chemotherapy had a better survival prognosis, while among non-surgical patients, the survival curves of those who did and did not receive chemotherapy were relatively close (Figure 4).

Univariate analysis results

Table 2 demonstrates the results of the univariate analysis of the independent variable (method of lymph node examination) and the 15 covariates. Compared with endoscopic lymph node biopsy, removal of regional lymph nodes for examination was associated with a 67.9% reduction in the risk of death [hazard ratio (HR) 0.321, 95% confidence interval (CI): 0.315, 0.327, P<0.001], and a 74.3% reduction in lung cancer-specific mortality (HR 0.257, 95% CI: 0.252, 0.263, P<0.001). Male patients undergoing lung cancer surgery had a 26.7% higher risk of death than female patients (HR 1.267, 95% CI: 1.256, 1.279, P<0.001) and a 25.4% higher risk of lung cancer-specific death (HR 1.254, 95% CI: 1.242, 1.267, P<0.001).

Asian or Pacific Islander patients had a 10.1% lower risk of death than white patients (HR 0.899, 95% CI: 0.886, 0.913, P<0.001), while the risk of lung cancer-specific death was 4.9% lower (HR 0.951, 95% CI: 0.935, 0.966, P<0.001). Compared with patients with middle lobe lung cancer, patients with upper lobe lung cancer had a 12.2% higher risk of death (HR 0.878, 95% CI: 0.858–0.898, P<0.001) and an 11.7% increased risk of lung cancer-specific death (HR 0.883, 95% CI: 0.861–0.905, P<0.001).

Multivariate analysis of lymph node examination methods

Table 3 presents the results of multivariate regression analysis on the impact of different lymph node examination methods on the prognosis of lung cancer patients. Three models were used: model I was unadjusted; model II was adjusted for age, sex, and race; model III was adjusted for age, sex, race, total number of malignant tumors, histology, tumor size, regional nodes positive, grade, primary site, laterality, stage, median household income, surgery, radiation, and chemotherapy. After adjusting for these 15 covariates, multivariate regression analyses showed that removal of regional lymph nodes for examination reduced the risk of death by 6.2% (HR 0.938, 95% CI: 0.914–0.962, P<0.001) and the cancer-specific mortality rate by 6.0% compared with endoscopic lymph node biopsy (HR 0.940, 95% CI: 0.914–0.968, P<0.001).

Stratified multivariate analysis

Table 4 demonstrates the results of multivariate regression analysis stratified by surgery. The results showed that among surgical patients, removal of regional lymph nodes for examination reduced the risk of death by 15.7% compared with endoscopic lymph node biopsy (HR 0.843, 95% CI: 0.781–0.910, P<0.001), and the risk of cancer-specific death by 15.5% (HR 0.845, 95% CI: 0.771–0.927, P<0.001).

In this study, multiple regression equations were analyzed for all surgical patients. The results of the multiple regression equation analysis stratified by stage, radiotherapy and chemotherapy (for all surgical patients) are presented in Tables 5-7, respectively. The results in Table 5 showed that in patients undergoing stage IA surgery, removal of regional lymph nodes for examination resulted in a 29.2% reduction in the risk of death compared with endoscopic lymph node biopsy (HR 0.708, 95% CI: 0.617–0.812, P<0.001) and a 35.6% reduction in the risk of cancer-specific death (HR 0.644, 95% CI: 0.535–0.775, P<0.001). In patients undergoing stage IIB surgery, removal of regional lymph nodes for examination led to a 25.8% reduction in the risk of death compared with endoscopic lymph node biopsy (HR 0.742, 95% CI: 0.594–0.928, P=0.009) and a 26.5% reduction in the risk of cancer-specific death (HR 0.735, 95% CI: 0.566–0.954, P=0.02).

The results in Table 6 showed that in surgical patients undergoing radiotherapy, removal of regional lymph nodes for examination resulted in a 16.8% reduction in the risk of death compared with endoscopic lymph node biopsy (HR 0.832, 95% CI: 0.716–0.965, P=0.02), and a 20.0% reduction in the risk of cancer-specific death (HR 0.800, 95% CI: 0.681–0.939, P=0.006). In surgical patients who did not receive radiotherapy, removal of regional lymph nodes for examination reduced the risk of death by 15.7% compared with endoscopic lymph node biopsy (HR 0.843, 95% CI: 0.769–0.923, P<0.001), and the risk of cancer-specific death by 15.9% (HR 0.841, 95% CI: 0.749–0.945, P=0.003).

The results in Table 7 showed that in surgical patients undergoing chemotherapy, removal of regional lymph nodes for examination resulted in a 16.0% reduction in overall mortality compared with endoscopic lymph node biopsy (HR 0.840, 95% CI: 0.741–0.952, P=0.006), and a 15.0% reduction in the risk of cancer-specific mortality (HR 0.850, 95% CI: 0.741–0.975, P=0.02). In surgical patients who did not receive chemotherapy, removal of regional lymph nodes for examination reduced the risk of death by 18.1% compared with endoscopic lymph node biopsy (HR 0.819, 95% CI: 0.743-0.902, P<0.001), and the risk of cancer-specific death by 20.5% (HR 0.795, 95% CI: 0.701-0.900, P<0.001).

Survival rates according to lymph node biopsy method

The 1-, 2-, 3-, 5-, 10-, and 15-year OS rates of lung cancer patients who underwent endoscopic lymph node biopsy were 38%, 23%, 17%, 11%, 5%, and 1%, respectively (see Table 8). In comparison, for lung cancer patients who had regional lymph nodes removed for examination, the OS rates were 82%, 72%, 64%, 53%, 33%, and 21%, respectively, representing increases of 44%, 49%, 47%, 42%, 28%, and 20%.

Among all surgical patients, the 1-, 2-, 3-, 5-, 10-, and 15-year OS rates of lung cancer patients who underwent endoscopic lymph node biopsy were 74%, 60%, 51%, 40%, 21%, and 12%, respectively (see Table 9). In contrast, for lung cancer patients who had regional lymph nodes removed for examination, the OS rates were 86%, 76%, 68%, 57%, 36%, and 23%, respectively, showing increases of 12%, 16%, 17%, 17%, 15%, and 11%.

Survival time and analysis according to patient characteristics

The mean OS period for patients who underwent endoscopic lymph node biopsy was 25.071 months, whereas for lung cancer patients who had regional lymph nodes removed for examination, the average OS was 87.403 months, which is 62.332 months longer than that of patients who underwent endoscopic lymph node biopsy (available online: https://cdn.amegroups.cn/static/public/jtd-2025-821-1.xlsx). Additionally, the average OS periods for lung cancer patients, categorized by age group, are as follows: 47.563 months for patients under 60 years old (excluding 60); 41.447 months for patients aged 60 to 69 years; 32.137 months for patients aged 70 to 79 years; and 18.735 months for patients aged 80 years and above. The detailed average survival analysis time and median survival analysis time are shown in table available online: https://cdn.amegroups.cn/static/public/jtd-2025-821-1.xlsx.

Survival analysis according to lymph node examination

The table available online: https://cdn.amegroups.cn/static/public/jtd-2025-821-2.xlsx presents the Chi-squared values from the log-rank test (Mantel-Cox), Breslow test (Generalized Wilcoxon), and Tarone-Ware test for the overall comparison and pairwise comparisons among groups in the Kaplan-Meier survival analysis (for OS rate and lung cancer-specific mortality rate). The Chi-squared values for the comparison between patients undergoing endoscopic examination and those having regional lymph nodes removed for examination were 19,258.272, 20,176.575, and 20,285.116 for the log-rank test, Breslow test, and Tarone-Ware test, respectively (P<0.001). For the comparison between male and female patients, the Chi-squared values were 2,878.43, 2,371.867, and 2,735.38 for the log-rank test, Breslow test, and Tarone-Ware test, respectively (P<0.001).

Discussion

Lung cancer has a high mortality rate and is the leading cause of cancer-related deaths (16,17). Although lung cancer surgeries such as open surgery, thoracoscope-assisted surgery, and robot-assisted surgery have improved the survival rate of patients with lung cancer (18-20), there remains an acute demand for improving the postoperative survival rate of patients with lung cancer. Chemotherapy, radiotherapy, immunotherapy, and targeted therapy have a degree of efficacy, but surgery remains an important treatment for lung cancer (21-24). Lymph node detection is the only basis for determining the treatment method and evaluating the scope of surgery and has an important impact on the prognosis of patient survival (3). The chief purpose of this study was to investigate the effects of regional lymph nodes removed for examination and endoscopic lymph node biopsy on the prognosis and survival of patients with lung cancer.

This study analyzed 222,563 patients with lung cancer from the SEER database to evaluate the effects of lymph node examination methods—regional lymph nodes removed for examination and endoscopic lymph node biopsy—on survival prognosis (12). After adjusting for 15 covariates, the results of multiple regression analysis indicated that the risk of death was significantly lower in surgical patients who underwent lymph node resection examination compared to those who received endoscopic biopsy. In non-surgical patients, however, the reduction in the risk of death associated with lymph node resection examination was less pronounced compared to that of the surgical patients.

No large-sample retrospective studies have been conducted to compare lymph node examination methods in patients with lung cancer. Specifically, comprehensive research on lymph node examination and endoscopic lymph node biopsy in this patient population is lacking. It has been reported that preoperative percutaneous and bronchoscopic biopsies do not increase the risk of recurrence in patients undergoing surgery for stage I non-small cell lung cancer (25). Moreover, Li et al. found that wedge resection was not inferior to anatomical resection in terms of OS in patients with early-stage lung cancer, while preoperative lymph node biopsy significantly improved survival in both multivariate and matched studies (26). However, their study did not perform the preoperative lymph node examination of patients with lung cancer. Xie et al. found that a positron emission tomography (PET)-computed tomography (CT) nomogram combining maximum standardize uptake value and CT radiomics for preoperative lymph node staging of non-small cell lung cancer could improve the diagnostic performance for lymph node metastasis (27). Bousema et al. indicated in a randomized controlled study involving 360 patients that for patients with negative lymph node assessments based on systematic endoscopic ultrasound, mediastinoscopy for lymph node examination could be omitted (28). Despite these findings, few studies have directly compared lymph node examination with endoscopic lymph node biopsy. Therefore, we conducted this retrospective study involving 222,563 cases to evaluate these preoperative lymph node examination methods.

Our findings suggested that patients with lung cancer who underwent surgical removal of lymph nodes had a superior prognosis to those who underwent endoscopic lymph node examination biopsy, which may be attributed to several factors. First, various lymph nodes are typically removed and examined during surgical removal, which is not the case with endoscopic examination. Second, surgically removed lymph nodes entail detailed pathological examination, which is generally more accurate than the puncture cytology often used in endoscopic methods. Third, surgical removal is not constrained by the limitations of endoscopic procedures, allowing sufficient time for thorough examination and ensuring better patient compliance. Fourth, the more accurate and comprehensive lymph node assessment and grading enable precise treatment planning, thereby improving patient prognosis.

Compared to prospective studies, although this study included a large volume of patient data, it remains a retrospective analysis. On the other hand, due to the large sample size included in the study, there is a certain degree of heterogeneity within the sample. Moreover, owing to the limitations of the SEER database, detailed information regarding the techniques used in endoscopic examinations is not available. Future prospective studies will further validate the reliability of our findings.

Conclusions

For patients undergoing lung cancer surgery, compared to endoscopic evaluation of lymph nodes, the removal of regional lymph nodes for examination can reduce the risk of death by 15.7%, thereby decreasing mortality rates and improving survival outcomes.

Acknowledgments

We would like to thank the participants for their time and effort during the data collection phase.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-821/rc

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-821/prf

Funding: This work received financial support from the National Key Research and Development Program of China (No. 2022YFC2407303) and the Zhejiang Provincial Research Center for Lung Tumor Diagnosis and Treatment Technology (No. JBZX-202007).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-821/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study received approval from the Ethics Review Committee of the First Affiliated Hospital of Zhejiang University School of Medicine (approval No. IIT20241665A).

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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