A structural dose-response relationship between lymph node yield and survival after anatomical segmentectomy for early-stage NSCLC: a SEER-based retrospective cohort study

Introduction

Anatomical segmentectomy is now an accepted option for selected early-stage non-small cell lung cancer (NSCLC), supported by randomized trials showing superior overall survival (OS) versus lobectomy in JCOG0802/WJOG4607L and noninferior disease-free survival (DFS) with similar OS versus lobectomy in Cancer and Leukemia Group B (CALGB)/Alliance 140503 for peripheral stage IA tumors ≤2 cm with confirmed node-negative status (1,2). Nevertheless, the “optimal” extent of nodal evaluation during segmentectomy remains unsettled (3). Current guidelines and expert consensus statements emphasize that systematic hilar and mediastinal lymph node dissection or evaluation should be performed during segmentectomy (4,5). Segmental anatomy and lymphatic drainage patterns can be heterogeneous, and the procedure may be performed in older or more comorbid patients in whom operative goals and competing mortality risks differ from lobectomy populations (6). Although consensus has been reached that lymph node dissection or evaluation should be performed, the quantitative dimension of lymph node management in patients undergoing segmentectomy remains insufficiently defined. The European Society of Thoracic Surgeons (ESTS) has proposed technical standards regarding the number of stations required for systematic lymph node dissection. In real-world practice, variation in nodal sampling persists, and multiple retrospective studies have explored whether a higher number of examined nodes is associated with better outcomes after sublobar resection (7-9). For example, an analysis by Yendamuri et al. (10) reported that many sublobar resections had no nodes examined and that greater lymph node examination was associated with improved survival, consistent with reduced under-staging. Other population-based work has suggested threshold effects (11) (e.g., poorer cancer-specific outcomes with low examined node counts) and has proposed procedure- and size-specific target ranges for nodes examined (12). However, more recent institutional series have reported no clear association between dissected node count and recurrence or OS after thoracoscopic segmentectomy (13), and the necessity of mediastinal lymph node dissection for peripheral stage IA tumors undergoing segmentectomy remains debated (14). Age and tumor size may also shape the observed relationship between lymph node evaluation and survival after segmentectomy (15). Older patients are more frequently selected for segmentectomy and may undergo less extensive nodal assessment, yet they face substantially higher non-cancer-related mortality (16); as a result, any association between lymph node yield and OS could be partly driven by competing risks rather than differences in cancer control. Tumor size, a key determinant of occult nodal metastasis, may further modify the prognostic value of a higher lymph node yield (17,18), but this potential effect modification has not been well characterized within a single segmentectomy-only cohort.

Against this background, large-scale evidence describing the shape of the association between lymph node yield and survival after anatomical segmentectomy, particularly using flexible dose–response modeling and accounting for competing risks, remains limited (5,7,17,19,20).

The aim of our study was to evaluate the quantitative relationship between regional lymph node yield (“regional nodes examined”) and OS after segmentectomy for clinical T1a–cN0M0 NSCLC ≤30 mm, using the Surveillance, Epidemiology, and End Results (SEER) database and to model dose-response relationship, assessing lung cancer-specific death using a competing-risk framework, including subgroup analyses by age and tumor size. We present this article in accordance with the STROBE reporting checklist (21) (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2026-0850/rc).

Methods

Data source and study design

This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. We conducted a population-based retrospective cohort study using the SEER database maintained by the U.S. National Cancer Institute. We used the SEERStat Database: Incidence—SEER Research Data, 17 Registries, Nov 2024 Submission (2000–2022).

Study population

We included patients diagnosed between 2000 and 2022 with pathologically confirmed NSCLC who underwent anatomical segmentectomy as the primary surgical procedure (SEER surgery code B220). To harmonize staging across calendar periods, we applied the American Joint Committee on Cancer (AJCC) 8th edition tumor-size cutoffs to reconstruct T1 subcategories using the recorded maximum tumor diameter (mm): T1a (1–10 mm), T1b (11–20 mm), and T1c (21–30 mm). The cohort was restricted to tumors 1–30 mm (T1). Clinical nodal status in SEER was used to select N0M0 disease, yielding a clinical T1a–cN0M0 cohort. Only patients with a single primary tumor were included.

Exclusion criteria were: (I) nodal or distant metastasis (N1–3/M1); (II) small cell lung cancer or neuroendocrine tumors; (III) diagnosis by autopsy or death certificate only; and (IV) missing data for regional lymph node yield (including regional nodes examined codes 95–98), survival time, or cause of death. Patients receiving perioperative radiotherapy and/or chemotherapy were retained and adjusted for in multivariable models. Among the 4,042 patients evaluated before application of the nodal-status exclusion criterion, 338 were classified as N1–2, including 123 with N1 and 215 with N2 disease, and were excluded from the final N0 analytic cohort. Because separate clinical and pathological nodal categories were not consistently available throughout the study period, the number of patients with confirmed cN0-to-pN1/2 upstaging could not be determined. The selection process is shown in Figure 1.

Figure 1 Flowchart. AJCC, American Joint Committee on Cancer; CS, collaborative stage; EOD, extent of disease; M, metastasis; N, node; SEER, Surveillance, Epidemiology, and End Results; T, tumor; TNM, tumor-node-metastasis.

Variables

Histology was classified using International Classification of Diseases for Oncology, Third Edition (ICD-O-3) codes into adenocarcinoma, squamous cell carcinoma, and other NSCLC types (codes listed in Appendix 1).

Regional lymph node yield was defined using the SEER variable “Regional nodes examined.” This variable reflects the number of nodes evaluated but does not distinguish systematic lymph node dissection from sampling. Lymph node yield was analyzed categorically as 0, 1–5, 6–10, and >10 nodes and continuously using restricted cubic splines. The 0-node group was considered separately because the absence of any recorded nodal evaluation is clinically distinct from limited sampling. Among patients with examined nodes, adjacent five-node intervals were used to represent limited and intermediate yields, while >10 nodes represented a higher-yield category. These pragmatic categories were selected a priori to provide clinically interpretable ordered groups while retaining adequate sample sizes and were not intended to define an optimal or biologically validated cut-off. The dose-response relationship was additionally evaluated using a test for trend across the ordered groups and by modeling lymph node yield continuously.

Age and tumor size were modeled as continuous variables; for interaction analyses, age was stratified at the cohort median (70 years).

Endpoints

The primary endpoint was OS, defined from surgery to death from any cause or last follow-up. The secondary endpoint was lung cancer-specific death, analyzed using a competing-risk framework with death from other causes treated as the competing event. OS was selected as the primary endpoint because SEER does not capture tumour recurrence, including the timing or site of relapse, and therefore does not permit reliable estimation of relapse-free survival (RFS) or DFS.

Statistical analysis

Baseline characteristics were compared using chi-square tests for categorical variables and parametric or non-parametric tests for continuous variables as appropriate. OS was estimated using Kaplan-Meier methods and compared by log-rank test. Associations between lymph node yield and OS were evaluated using multivariable Cox proportional hazards models adjusting for age, sex, race, tumor size, histology, grade, radiotherapy, chemotherapy, laterality and primary tumor lobe. Trend across ordered lymph node yield groups was assessed within Cox models. Proportional hazards assumptions were evaluated using Schoenfeld residuals.

To characterize the continuous dose-response association, restricted cubic spline models (four knots at Harrell-recommended percentiles) were fitted; P overall and P for non-linearity were reported. Effect modification by age and tumor size was assessed by including interaction terms in Cox models.

Competing-risk analyses for lung cancer-specific death and other-cause death were performed using Fine-Gray sub-distribution hazard models, reporting sub-distribution hazard ratios (sdHRs) with 95% confidence intervals (CIs).

Sensitivity analyses included: (I) additional adjustment for year of diagnosis (2000–2010 vs. 2011–2022); and (II) repeating the primary analysis among patients who did not receive radiotherapy or chemotherapy. Analyses were conducted using R Statistical Software (Version 4.2.2, http://www.R-project.org, The R Foundation) and the Free Statistics analysis platform (Version 2.3, Beijing, China). Two-sided P<0.05 was considered statistically significant. Additional model details, proportional hazards testing, sensitivity analyses, competing-risk models, and pairwise log-rank comparisons are provided in Tables S1–S7.

Results

Baseline characteristics

We included 2,217 patients with clinical T1a–cN0M0 NSCLC who underwent anatomical segmentectomy. Lymph node yield categories were: 0 nodes (n=351, 15.8%), 1–5 (n=793, 35.8%), 6–10 (n=538, 24.3%), and >10 (n=535, 24.1%). Median age was 70 years [interquartile range (IQR), 63–76 years]. Baseline characteristics differed across node-yield groups for age, sex, tumor size, grade, histology, and radiotherapy use (all P<0.001), while marital status and chemotherapy use did not. With increasing lymph node yield, mean tumor size decreased and the proportion of adenocarcinoma increased (Table 1).

OS

During a median follow-up of 58 months, 783 deaths occurred (35.3%). OS differed by lymph node yield (log-rank P<0.001) (Figure 2). Five-year OS increased stepwise across groups: 52.5%, 65.9%, 77.4%, and 83.9% for 0, 1–5, 6–10, and >10 nodes, respectively; corresponding 10-year OS rates were 26.8%, 38.3%, 53.6%, and 59.6%. In additional pairwise log-rank analyses, all six comparisons remained statistically significant after Holm adjustment for multiple testing; the adjusted P values were <0.001 for five comparisons and 0.012 for Group 3 versus Group 4 (Table S7). In multivariable Cox models (Table 2), higher lymph node yield remained independently associated with lower mortality: hazard ratio (HR) =0.79 (95% CI: 0.67–0.94; P=0.006) for 1–5 nodes, HR =0.55 (95% CI: 0.44–0.70; P<0.001) for 6–10 nodes, and HR =0.40 (95% CI: 0.30–0.52; P<0.001) for >10 nodes (trend P<0.001). The proportional hazards assumption was not violated (global P=0.15) (Table S2, Figure S1). Age (per year), male sex, larger tumor size, higher grade, and receipt of radiotherapy/chemotherapy were associated with increased mortality (Table 2).

Figure 2 Kaplan-Meier curves of overall survival stratified by LNY: Group 1, Group 2, Group 3, Group 4. The displayed P value corresponds to the overall log-rank comparison across all four lymph node yield groups and does not represent pairwise comparisons. Pairwise log-rank comparisons with Holm adjustment for multiple testing are reported in Table S7. The number at risk is shown below. P values were calculated using the log-rank test. The proportional hazards assumption was assessed and was not violated (global test P=0.15). Group 1: 0 nodes; Group 2: 1–5 nodes; Group 3: 6–10 nodes; Group 4: >10 nodes. LNY, regional lymph node yield.

Dose-response and subgroup analyses

Restricted cubic splines showed a significant association between node yield and mortality (P overall <0.001) with no evidence of non-linearity (P non-linearity =0.27), consistent with a graded dose-response pattern (Figure 3). In subgroup analyses, the association between higher node yield and OS was directionally consistent across age (<70 vs. ≥70 years) and tumor-size strata (≤10, 11–20, 21–30 mm), with no significant interaction (P for interaction =0.69 for age; =0.30 for tumor size) (Table 3, Figure S2).

Figure 3 Restricted cubic spline analysis of the association between regional lymph node yield and overall survival in the multivariable Cox model. The reference value was set at 6 nodes. Shaded areas represent 95% confidence intervals. Values above the 99.5th percentile were truncated for visualization. Group 1: 0 nodes; Group 2: 1–5 nodes; Group 3: 6–10 nodes; Group 4: >10 nodes.

Competing-risk and sensitivity analyses

In competing-risk analyses, lung cancer-specific death differed modestly by age (5-year: 15.6% vs. 19.6%; 10-year: 25.6% vs. 29.9% for <70 vs. ≥70 years; Gray’s test P=0.045), whereas other-cause death differed substantially (5-year: 8.7% vs. 18.5%; 10-year: 21.1% vs. 40.3%; Gray’s test P<0.001) (Table 4, Figure 4). In multivariable Fine-Gray models, age was not associated with lung cancer-specific death (sdHR 1.01, 95% CI: 1.00–1.02; P=0.13) but was associated with other-cause death (sdHR 1.05, 95% CI: 1.03–1.06; P<0.001). Higher lymph node yield was associated with lower lung cancer-specific death (vs. 0 nodes: sdHR 0.74, 0.58, 0.43 for 1–5, 6–10, and >10 nodes; all P≤0.02), and Group 3–4 also trended toward lower other-cause death (Tables S5,S6).

Figure 4 Cumulative incidence functions of lung cancer-specific death and other-cause death stratified by age group. CIFs for lung cancer-specific death (solid lines) and other-cause death (dashed lines) are shown for patients aged <70 and ≥70 years. Shaded areas indicate 95% confidence intervals. Gray’s test was used to compare CIFs between age groups for each endpoint (lung cancer-specific death: P=0.045; other-cause death: P<0.001). Age was modeled as a continuous variable in multivariable Fine-Gray regression analyses (see Tables S5,S6). CIF, cumulative incidence function.

After additional adjustment for year of diagnosis (2000–2010 vs. 2011–2022), and in the subgroup without radiotherapy/chemotherapy (n=2,148), the stepwise association between higher node yield and OS persisted (both trend P<0.001; Tables S3,S4).

Discussion

In this population-based cohort of 2,217 patients with clinical T1 (≤30 mm) N0M0 NSCLC treated by anatomical segmentectomy, regional lymph node yield showed a graded, stepwise association with long-term outcomes. OS was progressively higher across increasing lymph node yield categories, and the association remained significant after multivariable adjustment (trend P<0.001). Higher yields were associated with lower all-cause mortality (adjusted HRs were 0.79 for 1–5 nodes, 0.55 for 6–10 nodes, and 0.40 for >10 nodes). Importantly, restricted cubic spline modeling supported a continuous dose-response pattern (P overall <0.001) without evidence of a clear non-linear inflection (P non-linearity =0.27), arguing against a single “minimum threshold” explanation.

The association was directionally consistent across age and tumor-size strata (no significant interactions), and competing-risk analyses suggested that the adverse effect of increasing age on OS was driven primarily by non-cancer-related death, whereas the association between lymph node yield and lung cancer-specific death remained stable. Together with sensitivity analyses addressing calendar period and adjuvant therapy receipt, these findings indicate that lymph node yield functions as a robust prognostic marker in contemporary segmentectomy practice as captured by SEER. The oncologic role of segmentectomy has been reshaped by randomized evidence, but both pivotal trials also underscored the importance of nodal evaluation. JCOG0802/WJOG4607L (1,22) demonstrated OS superiority for segmentectomy compared with lobectomy in small peripheral NSCLC, while CALGB/Alliance 140503 (22,23) showed noninferiority of sublobar resection (segmentectomy or wedge) versus lobectomy for DFS with similar OS in peripheral stage IA tumors ≤2 cm after confirmation of node-negative status. These trials strengthen the premise that parenchyma-sparing resection can be oncologically sound when accompanied by appropriate staging, but they do not define the optimal quantity of nodal evaluation during segmentectomy.

Quality initiatives and guidelines (8,24-28) increasingly emphasize station-based nodal assessment rather than a single node-count cut-off. The American College of Surgeons Commission on Cancer (CoC) implemented Operative Standard 5.8 in 2021, requiring sampling from ≥1 hilar and ≥3 mediastinal lymph node stations, reflecting a consensus that systematic nodal evaluation should accompany curative-intent lung resections (29). Similarly, established surgical guidance has long advocated systematic intraoperative nodal staging as a core component of resection for NSCLC. However, large registries such as SEER do not capture nodal stations, and the available variable (“regional nodes examined”) is inherently count-based and cannot distinguish systematic dissection from sampling.

Within that constraint, our findings provide complementary evidence that, in real-world practice, higher nodal yield is associated with better outcomes in a manner consistent with a graded rather than binary effect.

Prior observational work has reported a correlation between the number of examined lymph nodes and survival after sublobar resection, while highlighting substantial variability in nodal evaluation. In a notable analysis focused on sublobar resections, Yendamuri and colleagues (10) found that a substantial proportion of patients, particularly those undergoing wedge resection and, to a lesser extent, segmentectomy, had no nodes examined, and that greater lymph node examination correlated with higher survival. Our results extend this literature in two key ways. First, by restricting to a segmentectomy-only cohort and modeling node yield both categorically and continuously, we provide evidence for a dose–response association rather than dependence on an arbitrarily chosen cut-off. Second, by applying competing-risk methods, we clarify the role of age-related competing mortality, showing that age materially increases other-cause death while its association with lung cancer-specific death is attenuated, helping interpret why OS gradients may differ by age even when cancer-related effects persist (15).

Mechanistically, several non-mutually exclusive explanations may underpin the observed gradient. Higher lymph node yield may reduce under-staging (stage migration) by detecting occult nodal disease, thereby aligning prognosis and subsequent therapy more appropriately. It may also reflect a therapeutic contribution of removing microscopic nodal metastases (30). Alternatively, node yield may function as a surrogate for care quality—including surgical thoroughness, institutional volume, and pathological processing rigor. SEER cannot disentangle these pathways, but the consistent monotonic pattern in the spline analysis supports the concept that “more complete nodal evaluation”, however operationalized, tracks with improved outcomes.

Limitations

This study has important limitations inherent to registry-based analyses. First, SEER records the number of “regional nodes examined”, but cannot distinguish systematic nodal dissection from sampling, does not provide station-level information, and lacks granular operative details (approach, extent of nodal dissection, intraoperative staging strategy).

Second, key confounders—comorbidity burden, pulmonary function, smoking history, frailty, surgeon/hospital factors, and recurrence patterns—are unavailable, leaving potential for residual confounding and “healthy patient/center” effects. SEER also lacks recurrence data; therefore, RFS and DFS could not be evaluated. Third, treatment variables in SEER are limited; while we adjusted for radiotherapy/chemotherapy sensitivity analyses, unmeasured treatment selection remains possible. Finally, the spline reference point was selected for visualization and should not be interpreted as establishing an optimal node-count target.

Conclusions

Among SEER patients undergoing anatomical segmentectomy for clinical T1a–cN0M0 NSCLC (≤30 mm), higher regional lymph node yield was associated with higher OS and lower lung cancer–specific mortality in a graded, dose-response pattern that was not materially modified by age or tumor size and persisted in sensitivity analyses.

While these findings are associative and limited by the inability to measure nodal stations and surgical technique, they support lymph node yield as a pragmatic marker of nodal evaluation adequacy in segmentectomy and provide population-based justification for prospective studies and quality initiatives focused on optimizing management.

Acknowledgments

We thank Free Statistics team for providing the valuable tools for data analysis and visualization (Version 2.3, Beijing, China).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2026-0850/rc

Peer Review File: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2026-0850/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2026-0850/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. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

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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