Examined lymph node counts ≤6 are correlated with an unfavorable prognosis in stage IA NSCLC patients following sublobar resection: a retrospective study employing propensity score matching analysis

Introduction

Lung cancer stands as the predominant cause of cancer-related mortality globally, with approximately 85% of cases attributed to non-small cell lung cancer (NSCLC) (1). In the realm of early-stage resectable NSCLC, radical surgical resection maintains its position as the gold standard of care. Nonetheless, the 5-year survival rate post-surgery lingers at a mere 50% to 60%. Individuals presenting with positive lymph node metastases face an augmented risk of disease recurrence.

Complete lymph node dissection, involving the excision of all ipsilateral lymph nodes visualized during surgery, represents a surgical approach that provides more precise pathologic staging for all patients and may offer improved clinical outcomes for select patients (2). It is considered the standard of care for individuals with a preoperative diagnosis of lymph node metastasis. However, for patients with intraoperative diagnosis of stage I NSCLC, complete lymph node dissection is not universally recommended as a routine surgical procedure. Several studies have indicated that there is no significant difference in outcomes between selective lymph node sampling and complete lymph node dissection for patients with early-stage lung cancer (3-5). More recent evidence, including the ACOSOG Z0030 randomized trial, demonstrated no survival difference between mediastinal lymph node sampling and complete dissection in early-stage NSCLC patients with negative clinical mediastinal staging (5).

An earlier analysis of a comprehensive cancer database revealed a noteworthy correlation: an increase in the number of lymph nodes removed during definitive surgery for stage I NSCLC was linked to a substantial enhancement in survival rates (6). Ludwig et al. (6), in their study using the Surveillance, Epidemiology, and End Results (SEER) database, reported that the survival advantage reached its pinnacle when approximately 13–16 lymph nodes were removed. More recently, Gulack et al. (7), in an analysis of the National Cancer Database (NCDB), demonstrated that the removal of 11 lymph nodes significantly enhanced survival in patients with NSCLC undergoing lobectomy.

The survival outcomes of stage IA NSCLC patients undergoing lobectomy may be enhanced by increasing the number of examined lymph nodes (ELNs) (8). However, these recommendations and potential benefits are predominantly derived from studies involving lobectomy, rather than sublobar resection.

Speicher et al. (9) reported an improved prognosis in patients with stage IA NSCLC who underwent sublobar resection with lymph node sampling. However, the authors did not explicitly emphasize the importance of ELN counts. The impact of ELN counts on survival following sublobar resection in patients with stage IA NSCLC remains undetermined. Here, we aimed to explore the relationship between ELN counts and lung cancer-specific survival (CSS) rates after propensity score matching (PSM) in stage IA NSCLC patients who underwent sublobar resection. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-aw-2137/rc).

Methods

Data source and patient selection

We retrieved data from the latest SEER 17 registry study database, which encompasses information from 2010 to 2019. The SEER 17 database captures data from 17 distinct and geographically diverse populations, encompassing rural, urban, and regional settings. Our inclusion criteria were as follows: (I) patients diagnosed with NSCLC who underwent sublobar (wedge or segmental) resection; (II) patients with pathological stage IA (pT1N0M0) NSCLC according to the 8th edition of the American Joint Committee on Cancer (AJCC) staging system; (III) patients with an ELN count of at least 1. We acknowledge that lymph node dissection practices during sublobar resection vary considerably among institutions and surgeons, both within the United States and globally. Unlike lobectomy, for which systematic mediastinal lymph node dissection or sampling is standard, there is no universally accepted protocol for lymph node examination during sublobar resection. Our study cohort reflects the heterogeneity of real-world clinical practice in the United States during the study period (2010–2019), where lymph node examination practices ranged from no nodal assessment to systematic mediastinal dissection. This heterogeneity, while representing a limitation in terms of standardization, also provides insight into the prognostic implications of varying degrees of lymph node examination in routine practice. ELN was defined as records the total number of regional lymph nodes that were removed and examined by the pathologist. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

To determine the optimal ELN cutoff, we systematically evaluated various thresholds (from 1 to 12) using Cox regression analysis. The cutoff value of 6 was selected based on the following criteria: (I) it demonstrated the strongest prognostic discrimination with the lowest hazard ratio (HR =0.7, P<0.001); (II) it provided balanced distribution of patients (66.0% vs. 34.0%), ensuring adequate sample size in both groups for robust statistical analysis; and (III) this threshold is clinically feasible, as it aligns with the number of lymph node stations typically sampled during sublobar resection according to NCCN guidelines.

Statistical analysis

CSS was utilized as the metric for survival outcomes. We employed COX proportional risk regression modeling to ascertain the impact of ELN count on CSS, adjusting for age, sex, race, primary site, grade, histology recoded, and operation type. Patients were stratified based on their ELN count. Subsequently, we identified cut-off points using the maximum HR and the minimum P value, with these structural breakpoints serving as thresholds for ELN. The comprehensive analysis of ELN counts on CSS is presented in Table 1, where patients were categorized into two groups: ELN ≤6 and ELN >6 (Table 1).

To compare survival between these groups, we employed PSM analyses. Propensity scores for the cohort were established using logistic regression based on potentially confounding variables, including age, sex, race, primary site, grade, histology recoded, and operation type.

Survival curves were plotted using the Kaplan-Meier method. Additionally, univariate and multivariate analyses were conducted using the Cox proportional risk model to calculate adjusted HRs and their corresponding 95% confidence intervals (CIs) for the specified variables. For all analyses, we utilized Empower (R) (www.empowerstats.com, X&Ysolutions, Inc., Boston, MA, USA) and R version 3.6.3 (http://www.R-project.org). Empower Stats is a statistical software based on the R language, renowned for its robust data processing and comprehensive analysis functions. The predetermined threshold for statistical significance was set at P<0.05.

Results

Baseline characteristics of the study participants

A total of 5,851 patients diagnosed with NSCLC and pathologic stage IA (T1N0M0) were included in this study based on the selection criteria (Table 2). The distribution of the ELN counts in this study cohort is illustrated in Figure 1. Baseline characteristics were generally comparable between the two ELN groups (Table 2). No statistically significant differences were observed in age distribution, sex, race, primary tumor site, tumor grade, or histologic type between patients with ELN ≤6 and those with ELN >6 (all P>0.05). However, patients with ELN ≤6 were significantly more likely to undergo wedge resection compared to those with ELN >6 (74.17% vs. 56.79%, P<0.001), which likely reflects the technical challenges of performing extensive lymph node dissection during wedge resection procedures. Overall, there were no significant disparities between the groups with ELN counts above and below 6 in terms of age, gender, race, primary tumor site, grade, and histologic type (P>0.05). However, patients with ELN counts below 6 were more inclined to undergo lung wedge resection compared to those with ELN counts above 6. Following PSM, the discrepancies between the two groups were effectively balanced (available online: https://cdn.amegroups.cn/static/public/jtd-2025-aw-2137-1.pdf).

Figure 1 Distribution of ELN in the population. ELN, examined lymph node.

Univariate analysis of the association between ELN and CSS

We did a univariate analysis before and after the PSM respectively. Prior to PSM, univariate analysis revealed superior survival outcomes in the cohort with an ELN count exceeding six, compared to those with six or fewer ELNs, yielding an HR of 0.75 (95% CI: 0.64–0.88, P=0.0004). Females exhibited markedly better survival rates than males, with an HR of 0.6 (95% CI: 0.5–0.7, P<0.001). Additionally, other races demonstrated significantly enhanced survival compared to white individuals, with an HR of 0.5 (95% CI: 0.3–0.7, P<0.001). Age, sex, race, primary site, grade, histology, and type of operation all correlated significantly with CSS (Table 3).

Post-PSM, the group with more than six ELNs continued to exhibit superior survival relative to those with six or fewer ELNs, with an HR of 0.6 (95% CI: 0.5–0.8, P<0.001). Females maintained a significant survival advantage over males, with an HR of 0.6 (95% CI: 0.5–0.7, P<0.001). However, no significant survival difference was observed between racial groups post-PSM, with other races having an HR of 0.6 (95% CI: 0.4–1.0, P=0.053) (Table 3).

Multivariate analysis of the association between ELN and CSS

We conducted multifactorial analyses both prior to and following PSM. Before PSM, in adjusted model I, controlling for age, sex, and race, the group with an ELN count exceeding six demonstrated significantly improved survival compared to the group with six or fewer ELNs, with a HR of 0.74 (95% CI: 0.63–0.87, P=0.0003). In adjusted model II, which included further adjustments for primary site, grade, histology, and type of surgery, the ELN >6 group continued to show a better survival prognosis relative to the ELN ≤6 group, with an HR of 0.76 (95% CI: 0.64–0.89, P=0.0008). Notably, there were no significant differences in the HRs across any of the three modeled groups, suggesting that other covariates had minimal impact on survival (Table 4).

Following PSM, in adjusted model I, which controlled for age and sex, the ELN >6 group again exhibited significantly superior survival compared to the ELN ≤6 group, with an HR of 0.70 (95% CI: 0.59–0.84, P<0.001). In adjusted model II, which included additional adjustments for grade, histology, and type of surgery, the ELN >6 group maintained a better survival prognosis relative to the ELN ≤6 group, with an HR of 0.80 (95% CI: 0.67–0.96, P=0.017) (Table 4).

Comparison of survival rates between the ELN >6 and ELN ≤6 groups in the KM curve

To conduct a more thorough comparison of the survival rates between the two groups, Kaplan-Meier (KM) survival curves were constructed. Across the entire population, the ELN >6 group exhibited a notably superior survival rate compared to the ELN ≤6 group in both the pre- and post-PSM cohorts (Figure 2). Furthermore, Kaplan-Meier curves were generated for subgroups comprising patients who underwent wedge resection and segmental resection. The subgroup analyses yielded consistent outcomes, demonstrating better survival rates in the ELN >6 group compared to the ELN ≤6 group for both wedge resection and segmental resection patients, with these findings persisting in the post-PSM model (Figures 3,4). Notably, despite the inherent technical challenges of performing systematic lymph node dissection during wedge resection compared to segmental resection, the survival benefit associated with higher ELN counts remained significant in both surgical subgroups.

Figure 2 Kaplan-Meier survival curves for all patients. (A) KM curves before PSM; (B) KM curves after PSM. ELN, examined lymph node; KM, Kaplan-Meier; PSM, propensity score matching.

Figure 3 Kaplan-Meier survival curves for the wedge resection cohort subgroup. (A) KM curves before PSM; (B) KM curves after PSM. ELN, examined lymph node; KM, Kaplan-Meier; PSM, propensity score matching.

Figure 4 Kaplan-Meier survival curves for the segmental resection cohort subgroup. (A) KM curves before PSM; (B) KM curves after PSM. ELN, examined lymph node; KM, Kaplan-Meier; PSM, propensity score matching.

Discussion

The findings of this study revealed that individuals with stage IA NSCLC who underwent sublobar resection exhibited inferior CSS outcomes when the ELN count was 6 or fewer, as opposed to those with ELN counts exceeding 6. Consistent results were obtained in the subgroup analysis involving patients who underwent wedge resection and segmental resection. These outcomes were validated through Cox modeling and PSM analysis.

The rationale behind the relationship between ELN counts and survival may be attributed to more accurate staging (10). Previous research has demonstrated that not all patients with negative lymph nodes are truly free of lymph node metastases (11,12). Inadequate lymph node examination may result in pathologic understaging, where occult nodal metastases remain undetected. Patients who are clinically staged as T1-2N0M0 but harbor occult lymph node metastases would be inappropriately classified as node-negative and consequently would not receive guideline-recommended adjuvant therapy, potentially compromising their long-term outcomes. A higher ELN count increases the probability of detecting positive lymph nodes when present, thereby enabling more accurate staging and appropriate selection of candidates for adjuvant therapy. This improved detection of nodal disease helps ensure that patients who would benefit from adjuvant treatment receive it, while confirming true node-negative status in those with higher ELN counts suggests a genuinely favorable prognosis (1).

For several types of cancers, such as gastrointestinal and breast cancers, extensive research has elucidated the connection between more thorough ELNs and enhanced patient survival. Consequently, the National Comprehensive Cancer Network (NCCN) guidelines advocate for resection or sampling of a minimum number of lymph nodes to achieve comprehensive nodal staging (13-16). However, the current NCCN guidelines recommend that surgeons only sample at the lymph node station and stipulate that one or more nodules be sampled from all mediastinal stations (2R, 4R, 7, 8, and 9 for right-sided cancers) (17), in order to accurately stage or identify patients at high risk for disease recurrence. Nonetheless, the optimal number of lymph nodes to be examined has not been definitively established or underscored in the context of NSCLC. While the ACOSOG Z0030 trial demonstrated no survival difference between systematic lymph node sampling and complete mediastinal lymph node dissection in early-stage NSCLC (5), that trial focused on patients undergoing lobectomy rather than sublobar resection. In the complete dissection arm of that study, the median number of lymph nodes harvested was 18, with 99% of patients having ≥6 nodes examined (5), reflecting the extent of nodal evaluation achievable during lobectomy. However, whether similar principles apply to sublobar resection, where anatomic access to nodal stations is more limited, remained unclear. Our findings suggest that even in the context of sublobar resection, examining more than 6 lymph nodes in patients with stage IA NSCLC is associated with improved CSS, potentially through more accurate pathologic staging. Prior studies have demonstrated that lymph node ratio (LNR) is a valuable metric for assessing the prognosis of surgically resected NSCLC patients, with a higher LNR correlating with a poorer prognosis (18).

LNR, which involves lymph node dissection and sampling, is the main adjunct to lung cancer surgery. Accurate pathologic staging is the ultimate goal of LNR, which permits better selection of candidates for adjuvant therapy. In addition, LNR can improve survival through better local control (19). The relationship between LNR and survival in NSCLC has been demonstrated in previous studies. In addition to guiding adjuvant chemotherapy and achieving local control, pathologic characterization of intraoperative lymph nodes is helpful in determining whether to perform standard sublobar resection in patients with adequate cardiopulmonary reserve. Patients with positive lymph nodes will undergo extended resection and may have better outcomes. Several previous studies have determined the relationship between the number of lymph nodes examined and survival by evaluating the prognostic impact of lymph node-negative NSCLC (1,6,20,21). These studies were based on the consideration that the more lymph nodes assessed, the more accurate the staging and the greater the probability of benefit from adjuvant chemotherapy.

However, alternative research groups have posited that a higher count of ELNs does not necessarily equate to improved survival outcomes for patients with stage I NSCLC. Liang’s comprehensive study, involving 9,603 NSCLC patients diagnosed with IA1 and IA2 from 2004 to 2014 using the SEER database, revealed that a greater number of ELNs in resected pT1bN0M0 NSCLC was linked to a heightened survival rate (22). Nevertheless, this finding did not extend to pT1aN0M0 NSCLC.

In a separate study, Ding et al. examined NSCLC patients with tumors ≤2 cm in size from 2004 to 2014 using the SEER database (19). Their findings suggested that for lesions equal to or smaller than 1 cm, wedge resection should involve the examination of 4 to 9 lymph nodes, and for lesions between 1 and 2 cm, 10 to 16 lymph nodes should be examined. However, in cases where the lesion measures 2 cm or smaller, segmental resection did not confer a survival benefit from lymph node dissection.

Our study population was predominantly composed of patients who underwent wedge resection (68.3%), which presents unique challenges for lymph node assessment. Wedge resection, by its nature as a limited parenchymal-sparing procedure, provides less anatomic access to mediastinal and hilar lymph node stations compared to segmental resection. Consequently, systematic lymph node dissection is more technically demanding during wedge resection, and the lymph nodes examined may represent a combination of systematically sampled nodes and those incidentally included in the resection specimen. Despite these technical limitations, our subgroup analyses demonstrated that the survival benefit associated with examining more than 6 lymph nodes was consistent across both wedge resection and segmental resection cohorts (Figures 3,4), suggesting that the prognostic value of more thorough nodal assessment is not confined to one surgical approach. However, we acknowledge that our study cannot distinguish between intentional systematic lymph node sampling and incidental nodal examination, nor can we account for surgeon-specific technical proficiency, surgical approach (video-assisted thoracoscopic surgery versus open), operative time, or intraoperative complications—all of which may influence both the extent of lymph node examination and overall survival outcomes.

Our study is subject to several limitations. Firstly, the retrospective nature of this study introduces inherent biases that are difficult to eliminate. There is no standardized protocol across institutions for the management and examination of lymph node dissection, leading to variability in practices. Furthermore, the SEER database does not capture detailed surgical technical factors that may confound the relationship between ELN count and survival. These unmeasured variables include surgeon experience and volume, surgical approach (video-assisted thoracoscopic surgery versus open thoracotomy), operative time, intraoperative complications, blood loss, and the specific intent of lymph node examination (systematic sampling versus incidental inclusion). The predominance of wedge resections (68.3%) in our cohort introduces additional complexity, as this procedure provides limited anatomic access for systematic mediastinal lymph node dissection compared to segmental resection. Therefore, higher ELN counts in wedge resection patients may reflect not only more thorough nodal assessment but also greater surgical complexity, more experienced surgeons, or patient selection factors—all of which could independently influence survival outcomes. In practices both within the United States and globally. This heterogeneity in surgical technique and lymph node assessment strategies represents a significant limitation, as we cannot determine whether lymph nodes were systematically sampled according to standardized stations, opportunistically removed, or represented incidental findings in the resection specimen. The decision to perform lymph node dissection and the extent of dissection likely varied based on surgeon preference, institutional practice patterns, intraoperative findings, and patient factors. Furthermore, our findings are based on US practice patterns captured in the SEER database and may not be directly generalizable to other healthcare systems with different surgical traditions and lymphadenectomy protocols. Complete removal of all lymph nodes in their entirety is often unattainable, and ELN counts may include partial lymph nodes. Consequently, ELN counts may fluctuate depending on the pathologic process, with some institutions recording counts based on intact lymph nodes and others including only lymph node fragments. Furthermore, while ELN counts are documented in the SEER database, the specific location of the lymph nodes (station N1 or N2) retrieved is not recorded (23). Therefore, it is challenging to determine the number and location of node stations that were removed or sampled. We can only infer that a higher number of ELNs indicates a broader examination of lymph node stations, potentially including more mediastinal (N2) nodes in addition to hilar/intrapulmonary (N1) nodes. Lastly, the SEER database lacks detailed information on several important clinical, radiologic, and pathologic variables. Specifically, data on patients’ comorbidities, lung function, functional status, and recurrence rates are not available. Most importantly, the database does not capture radiologic characteristics of the nodules, including the proportion of ground-glass opacity (GGO) components, solid component size, or nodule density, which represents a critical limitation. Recent evidence, including a randomized controlled trial presented at the World NSCLC Congress, has demonstrated that the risk of lymph node metastasis and the benefit of lymphadenectomy differ substantially among pure GGOs, part-solid lesions, and solid nodules. Pure GGOs, which typically represent adenocarcinoma in situ (AIS) or minimally invasive adenocarcinoma (MIA), have an extremely low risk of lymph node metastasis (often <1%) and may not require extensive lymph node examination. In contrast, solid nodules and part-solid lesions with larger solid components carry higher nodal metastasis risk and are more likely to benefit from thorough lymph node assessment. Our cohort likely includes a heterogeneous mixture of these radiologic subtypes, though the majority are expected to be solid or predominantly solid lesions given the clinical context of stage IA disease treated with sublobar resection. Therefore, our findings should be interpreted primarily in the context of solid or predominantly solid stage IA NSCLC and may not be applicable to pure GGOs.

Additionally, the SEER database does not systematically record important pathologic variables including surgical margin status, spread through air spaces (STAS), pleural invasion, and lymphovascular invasion—all of which are critical prognostic factors in sublobar resection. The absence of these data may confound the observed associations between ELN count and survival. Future prospective studies incorporating detailed radiologic imaging characteristics and comprehensive pathologic data are needed to establish nodule subtype-specific and risk-stratified recommendations for optimal ELN thresholds during sublobar resection.

Conclusions

In conclusion, our findings indicate that an ELN count of ≤6 following sublobar resection in patients with stage IA NSCLC is linked to an unfavorable prognosis. We recommend dissecting more than 6 nodes during sublobar resections in stage 1A NSCLC patients.

Acknowledgments

We would like to gratefully acknowledge to the patients who participated in the cohort for their contribution to data collection.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-aw-2137/rc

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-aw-2137/prf

Funding: None.

Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-aw-2137/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.

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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