4L lymph node dissection in non-small cell lung cancer: an updated systematic review and subgroup meta-analysis

Introduction

Non-small cell lung cancer (NSCLC) remains one of the leading causes of cancer-related mortality worldwide, accounting for more deaths than prostate, breast, brain, and colorectal cancers combined (1). It is a heterogeneous disease characterized by various histological subtypes, with adenocarcinoma and squamous cell carcinoma being the most common (2). Lymph node involvement is a critical prognostic factor, and systemic nodal dissection has long been recognized as a key component of surgical treatment in patients with NSCLC (3).

Specifically, left lower paratracheal (4L) lymph nodes are of significant interest due to their association with potential complications during dissection and survival outcomes. They are located between the left margin of the trachea, the superior margin of the aorta, the superior margin of the left pulmonary artery, and medially to the ligamentum arteriosum. Their proximity to these vessels and the left recurrent laryngeal nerve arouses dilemmas during surgeries (4).

Although multiple studies have evaluated the prognostic impact of mediastinal lymph node dissection, the specific role of 4L lymph node dissection (4LND+) remains less clearly defined. Early evidence suggests a potential association between 4LND+ and survival benefit, yet with more adverse outcomes. Hence, the exact effect of its surgical removal on overall survival (OS) and complication rate between studies remains inconsistent (5-7).

Current guidelines lack consensus regarding 4L and its routine removal during NSCLC surgery. Organizations such as the European Society of Thoracic Surgeons (ESTS) focus primarily on the total number of lymph nodes removed (minimum of six) or their general anatomical location (N1 or N2 stations) rather than specifying individual stations like 4L (8). With the new 9th edition of TNM classification, it is even more significant than ever, as inadequate lymphadenectomy should be marked as R-uncertain(un) resection (9). Moreover, due to the anatomical complexity and technical challenges associated with 4LND+, as well as the risk of postoperative complications, many thoracic surgeons decide not to perform this resection routinely (10). The lack of high-quality, large-scale evidence on this issue highlights the need for further research.

Several previous meta-analyses have assessed the impact of 4LND+ (11-13). However, the available data on specific outcomes was limited, the results were inconsistence, and subgroup analyses were not feasible. Therefore, we conducted a systematic review and updated meta-analysis comparing outcomes in patients undergoing 4LND+ vs. the lack of left paratracheal lymph node dissection (4LND−). To our knowledge, this is the first meta-analysis to conduct a subgroup comparison of OS in patients undergoing 4LND+ in stage I NSCLC and based on the primary tumor location in the left upper lobe (LUL) or the left lower lobe (LLL). The systematic review and meta-analysis were conducted in accordance with the Cochrane Collaboration Handbook for Systematic Review of Interventions (14). We present this article in accordance with the MOOSE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-593/rc) (15).

Methods

Study selection

The review protocol was registered with the International Prospective Register of Systematic Reviews (PROSPERO) (registration No. CRD42025642958).

Search strategy

A comprehensive literature search was performed on the following databases: PubMed, Scopus, and Wiley from inception until February 10, 2025. In PubMed, the search string used was: “lung cancer AND 4L”. For Scopus and Wiley, we used a combination of the following terms: “4L lymph node”, “left lower paratracheal node”, “non-small cell lung cancer”, “NSCLC”, “lung cancer”, and “lung carcinoma”. The references from all included studies, previous systematic reviews and meta-analyses were also searched manually for any additional studies. Two authors (G.M.G. and M.M.C.) independently extracted the data following predefined search criteria and quality assessment. All searches were conducted directly through each database’s native interface without the use of external reference management or search software.

Eligibility criteria

Inclusion in this meta-analysis was restricted to studies that met all the following eligibility criteria: (I) prospective or retrospective observational studies; (II) comparing 4LND+ with 4LND−; (III) with data on any of the outcomes of interest, which consisted of OS, total complication, pneumonia, chylothorax, prolonged air leak, hemorrhage, and vocal cord palsy; and (IV) studies published in English. The exclusion criteria were: (I) overlapping patient populations (only the study with highest number of patients was retained); (II) studies without a report on the outcomes of interest; and (III) abstract-only or unpublished studies.

Subgroup analyses

Prespecified sub-analyses included data restricted to (I) propensity score matching (PSM) and propensity score weighting (PSW) studies; (II) patients with LUL tumor resection; (III) patients with LLL tumor resection; and (IV) patients with stage I NSCLC. Stage I NSCLC was defined based on clinical staging in three studies (7,16,17), and pathological staging in one study (18).

Statistical analysis

For each binary endpoint, risk ratios (RR) with 95% confidence intervals (CI) were computed. Statistical significance was defined as P<0.05. Continuous outcomes were compared with hazard ratios (HR). The Cochran Q test and I² statistics were used to examine heterogeneity; P values inferior to 0.10 and I² >40% were considered significant for heterogeneity. We used the DerSimonian and Laird random effects model in outcomes with significant heterogeneity. Otherwise, a fixed effect model was applied. Review Manager 5.4 (Cochrane Center, The Cochrane Collaboration) was used for statistical analysis.

If the primary studies did not report HR and 95% CI directly, we derived them from Kaplan-Meier survival curves using a previously validated method (19). Kaplan-Meier curves of the included studies were analyzed with Web Plot Digitizer version 5.2 (free tool https://automeris.io/wpd/?v=5_2). The HR was calculated using the spreadsheet downloaded from https://static-content.springer.com/esm/art%3A10.1186%2F1745-6215-8-16/MediaObjects/13063_2006_188_MOESM1_ESM.xls.

Quality assessment

The risk of bias and quality assessment of individual studies were analyzed with the Newcastle-Ottawa scale (NOS). In the NOS, each of the studies is scored on a 0–9 scale according to the quality of participant selection, comparability of groups, and outcome assessment (20). If the score was >6, the study was defined as a high-quality study consistent with previous literature (11). The risk of bias was assessed independently by two investigators (M.M.C. and S.A.K.). Disagreements were resolved through a consensus and discussion. A leave-one-out sensitivity analysis of the main outcome was performed.

Results

Study selection and characteristics

The initial search strategy identified 434 results from the following databases: PubMed (n=180), Scopus (n=203), and Wiley (n=51). After removing 120 duplicates, 314 studies were screened, of which 304 were excluded based on titles and abstracts. Ten studies were fully reviewed for inclusion and exclusion criteria (Figure 1). Of these, an additional 2 studies lacked an outcome of interest (21,22). As a result, 8 retrospective studies were included in the meta-analysis (5-7,16-18,23,24). A total of 13,314 patients with left-sided NSCLC who underwent surgery were included, of whom 3,695 (27.8%) had a 4LND+.

Figure 1 PRISMA flow diagram of study screening and selection. The updated search identified 10 records assessed for eligibility, of which 2 were excluded after full-text screening. 6 records corresponded to studies already included in the previous version of the review, and 2 new studies met the eligibility criteria and were included, bringing the total number of included studies to 8.

Study characteristics are reported in Table 1. Six studies applied PSM, and another was conducted with a PSW, the remaining was an observational study without any method to address confounding. Metastasis rate to 4L differs from 5.1% to 20.9% between studies. Follow-up was reported to range between 40 and 99 months. Most of the studies originated from China, while the remaining were from South Korea, Poland, and Japan (Table 1).

Pooled analysis of all studies

Patients in the 4LND+ group showed improved OS compared to the 4LND− group (HR 0.77; 95% CI: 0.62–0.96; P=0.02; I² =84%; Figure 2). However, there was no significant difference between the groups when only PSM and PSW studies were analyzed (HR 0.82; 95% CI: 0.66–1.02; P=0.07; I² =83%). The OS effect between these two subgroups was significantly different (P=0.02; I² =81.1%). Although differences in specific complications such as chylothorax (1.1% vs. 0.8%; RR 1.41; 95% CI: 0.76–2.61; P=0.28; I² =0%; Figure 3A), hemorrhage (0.9% vs. 0.6%; RR 1.46; 95% CI: 0.65–3.28; P=0.36; I² =46%; Figure 3B), and pneumonia (2.1% vs. 1.7%; RR 1.21; 95% CI: 0.79–1.85; P=0.38; I² =0; Figure 3C) were not statistically significant, prolonged air leak (2.7% vs. 1.7%; RR 1.62; 95% CI: 1.00–2.60; P=0.05; I² =7%; Figure 3D) reached a marginally significant difference, the incidence of vocal cord palsy (2.9% vs. 0.77%; RR 3.64; 95% CI: 1.96–6.78; P<0.001; I²=0; Figure 4A), and total complication rate (11.5% vs. 8.0%; RR 1.45; 95% CI: 1.20–1.74; P<0.001; I² =0; Figure 4B) were significantly higher in 4LND+ patients.

Figure 2 4LND+ group was associated with a significantly better OS. However, pooled analysis of only PSM and PSW studies did not show a difference between the groups. Studies using PSM or PSW, as well as those without these adjustment methods, are indicated and were further evaluated in subgroup analyses. 4LND−, lack of left paratracheal lymph node dissection; 4LND+, left paratracheal lymph node dissection; CI, confidence interval; HR, hazard ratio; IV, inverse variance; OS, overall survival; PSM, propensity score matching; PSW, propensity score weighting; SE, standard error.

Figure 3 Forest plot comparing various complications between the groups. (A) Chylothorax rate was not significantly higher in the 4LND+ group. (B) Hemorrhage rate was not significantly higher in the 4LND+ group. (C) Pneumonia rate was not significantly different between the groups. (D) Prolonged air leak rate was not significantly different between the groups. 4LND−, lack of left paratracheal lymph node dissection; 4LND+, left paratracheal lymph node dissection; CI, confidence interval; M-H, Mantel-Haenszel.

Figure 4 Forest plots comparing vocal cord palsy risk and overall complication risk between the groups. (A) 4LND+ group had a significantly higher risk of vocal cord palsy as compared with the 4LND− group. (B) 4LND+ group had a significantly higher risk of complications as compared with the 4LND− group. 4LND−, lack of left paratracheal lymph node dissection; 4LND+, left paratracheal lymph node dissection; CI, confidence interval; M-H, Mantel-Haenszel.

Sub-analysis in selected population analysis

Subgroup analysis indicated that there were no significant differences between groups in OS in patients with LLL (HR 0.91; 95% CI: 0.44–1.88; P=0.80; I² =84%; Figure 5A), and LUL (HR 0.71; 95% CI: 0.51–1.01; P=0.05; I² =58%; Figure 5B) tumors. No significant difference in treatment effect was observed between LUL and LLL subgroups (P=0.54, I² =0). Similarly, in patients with stage I NSCLC, no statistically significant difference in OS was observed (HR 0.99; 95% CI: 0.79–1.26; P=0.96; I² =15%; Figure 5C).

Figure 5 Forest plot comparing OS between the subgroups. (A) There was no statistical difference when OS was compared in patients with LLL resection between the groups. (B) There was no statistical difference when OS was compared in patients with LUL resection between the groups. (C) There was no statistical difference when OS was compared in Stage I between the groups. 4LND−, lack of left paratracheal lymph node dissection; 4LND+, left paratracheal lymph node dissection; CI, confidence interval; HR, hazard ratio; IV, inverse variance; LLL, left lower lobe; LUL, left upper lobe; OS, overall survival; SE, standard error.

Quality assessment

The NOS tool was used for quality assessment. All of the 8 nonrandomized studies achieved ≥7 points in the NOS (Table 1).

A leave-one-out sensitivity analysis of the OS outcome revealed that removing the only PSW study from the PSM + PSW subgroup resulted in the most substantial reduction in heterogeneity. Additionally, the pooled OS benefit in the 4LND+ group was no longer statistically significant (HR 0.82; 95% CI: 0.67–1.02; P=0.07; I² =80%; Figure 6).

Figure 6 A leave-one-out analysis of the OS outcome revealed that removing the only PSW study from the PSM + PSW subgroup resulted in the most substantial reduction in heterogeneity. Additionally, the pooled analysis of OS benefit in the 4LND+ group was no longer statistically significant. Studies using PSM or PSW, as well as those without these adjustment methods, are indicated and were further evaluated in subgroup analyses. The “×” symbol represents a study that was excluded from this particular analysis. 4LND−, lack of left paratracheal lymph node dissection; 4LND+, left paratracheal lymph node dissection; CI, confidence interval; HR, hazard ratio; IV, inverse variance; OS, overall survival; PSM, propensity score matching; PSW, propensity score weighting; SE, standard error.

Discussion

In this systematic review and meta-analysis of 8 studies and 13,314 patients, we compared 4LND+ vs. 4LND− in patients undergoing NSCLC resection. The main findings were as follows: (I) patients undergoing 4LND+ had significantly improved OS compared to 4LND− group, suggesting a potential survival benefit; (II) this survival advantage was not observed when the analysis was restricted to PSM and PSW studies; (III) while 4LND+ was associated with a potential survival benefit, it was also linked to a higher overall complication rate; (IV) specific complications, such as chylothorax, prolonged air leak, hemorrhage, and pneumonia, were more frequently observed in the 4LND+ group, although none of these differences reached statistical significance; (V) incidence of vocal cord palsy was significantly more frequent in the 4LND+ group, highlighting the risk of nerve injury associated with the procedure; (VI) in the subgroup analysis of LUL and LLL patients, we found no significant difference in OS; (VII) in patients with stage I NSCLC, no statistically significant difference in OS between the groups was observed.

4LND+ in left-sided NSCLC is a surgical dilemma. Their adjacency to aortic arch, left pulmonary artery, and left recurrent laryngeal nerve discourages many thoracic surgeons. These are sites of potential complications. While vascular complications might be repaired, nerve injuries are usually permanent. It is prominent especially in LLL tumors, where exposure to these anatomical landmarks is limited. In the case of left pneumonectomy, when the left mainstem bronchus is divided, access to these lymph nodes is easier (10). However, data regarding complication rate and impact of 4LND+ in pneumonectomy are limited. Due to a lack of data, this particular subgroup analysis of OS with or without 4LND+ was impossible. For example, in our institution, 4L are not usually resected by us and our colleagues unless it is a pneumonectomy.

The impact of specific lymph node station resection on survival is not clear. International guidelines (e.g., ESTS) only indicate subcarinal lymph nodes (station 7) as mandatory during the radical (anatomical) resection (8). Similarly. Other stations are chosen by thoracic surgeons based on their technique or intraoperative findings. Both sampling and complete resection of lymph nodes are comparable regarding their impact on survival in patients with clinical stage I NSCLC (25). Current guidelines remain inconsistent regarding the optimal extent of lymph node dissection, with some recommending SLND or systematic lymph node sampling, while others highlight the importance of station-specific dissection, including 4L (26).

Given that the 9th edition of TNM introduced uncertain R resection (R0-un) in case of inadequate lymphadenectomy, surgeons should approach their lymphadenectomy meticulously. But, still relatively “safer” and more accessible lymph nodes in the mediastinum are usually preferred by surgeons (e.g., stations 5, 6, 7, 8, and 9) (8).

The surgical approach to 4LND+ includes open thoracotomy and video-assisted thoracoscopic surgery (VATS), which has gained popularity due to its minimally invasive nature and enhanced visualization of the surgical field (24). According to European Society for Medical Oncology (ESMO) guidelines, VATS is recommended as the preferred approach for stage I lung cancer (27). The choice of 4LND+ technique is often based on the surgeon’s experience and tumor characteristics. Moreover, robotic-assisted thoracic surgery is an emerging, innovative approach with potential advantages in dexterity and visualization; however, based on the studies reviewed, no definitive conclusions can be drawn, and further studies are needed.

Previous studies have reported conflicting results regarding the prognostic value of 4LND+. Some studies indicated a significant survival benefit, while others found 4LND+ to significantly worsen the OS (11-13). Notably, our meta-analysis included the recent study by Park et al., the only one conducted in South Korea, with a large group of patients, which was not part of previous meta-analyses that primarily included studies only from China and one from Poland (7). Before PSM, patients who did not undergo 4LND had significantly higher OS (P=0.002). However, after PSM, there were no significant differences in OS (P=0.12) between the groups. Subgroup analysis revealed that OS rates in LUL tumors were unaffected by 4LND+ (P=0.70), while OS rates were significantly lower in LLL tumors undergoing 4LND (P=0.003) (7).

Due to proximity of LUL tumors to the 4L station, the metastases are more common, as opposed to tumors originating in the LLL, which follow a different lymphatic drainage pattern (7). Previous studies have demonstrated that while metastases to 4L are approximately three times more frequent in LUL tumors compared to LLL tumors, this difference was not statistically significant (28). This highlights the need for cautious interpretation of subgroup analyses. Although the difference in OS between LUL subgroups in our study was not statistically significant, the HR for LUL tumors was weighted toward the 4LND+ group (P=0.05). This suggests a potential clinical benefit of 4LND+ in patients with LUL tumors, potentially due to earlier lymphatic spread, making nodal staging more impactful in this group. However, this finding requires validation in future studies with larger sample sizes and detailed subgroup analyses.

Peng et al. demonstrated that 4LND+ was associated with a significant improvement in OS for patients with operable left-sided NSCLC (11). However, most of the studies included in the meta-analysis focused on patients with advanced-stage disease (pathological stage II or higher), where lymph node involvement is more common, potentially explaining the observed survival benefit. In contrast, recent Japanese study included in our meta-analysis showed no significant difference in OS between patients with stage I NSCLC who underwent 4LND+ vs. 4LND− (17). These findings are consistent with our OS subgroup analysis for stage I. Recommendations regarding lymph node dissection do not differ between early and late stages of NSCLC. However, metastases to lymph nodes, especially N2 stations, are less probable in early stages. Based on our subgroup analysis of stage I, 4LND+ could be disregarded to avoid potentially fatal or terrible complications. Hence, the benefit of 4LND+ may be limited to cases with more advanced disease.

In our study, OS was significantly improved in the 4LND+ group when all studies were analyzed. However, a leave-one-out analysis showed that removing the only PSW study from the PSM + PSW subgroup resulted in the most pronounced reduction in heterogeneity (23). Furthermore, the pooled OS benefit in the 4LND+ group was no longer statistically significant, suggesting that this study contributed substantially to the variability in effect estimates. The observed heterogeneity reduction after excluding the PSW study may be explained by its methodological limitations. This study had a small sample size in the 4LND+ group, increasing the likelihood of selection bias. Moreover, a large proportion of patients were lost to follow-up. Patients lost to follow-up in the 4LND– group were older, had a smoking history, and had more comorbidities, which could have led to an underestimation of mortality in this group and an overestimation of the survival benefit in the 4LND+ group. These factors may explain its considerable contribution to heterogeneity and the loss of statistical significance in OS improvement after its exclusion. This indicates that the observed OS benefit in the pooled analysis may be influenced by the methodological characteristics of the Wang et al.’s study and should therefore be interpreted with caution (23).

Similar to prior research, our analysis confirms that patients undergoing 4LND+ experience a higher overall complication rate (11). Moreover, we observed a significant increase in the incidence of vocal cord palsy, highlighting the vulnerability of the recurrent laryngeal nerve to surgical damage. This complication is clinically important, as it can lead to aspiration pneumonia and difficulty clearing respiratory secretions, which may significantly impact patient quality of life and, in severe cases, be even life-threatening (29). Moreover, complications such as chronic hoarseness, dysphonia decrease patients’ ability to communicate. Some laryngological interventions might alleviate patients’ symptoms, but sometimes they persist lifelong (30). For example, in thyroidectomies, recurrent laryngeal nerve palsy is one of the most common reasons for suing and prosecuting doctors (31). Given that the impact of 4LND+ on survival is not clear, such a terrible complication should be strictly avoided. Especially because recurrent laryngeal nerve neuromonitoring during thoracic surgery is not used routinely and not studied well enough (32). The lack of statistical significance in other complications may be due to the limited sample size, emphasizing the need for further prospective studies to better define the risks and benefits of 4LND+ and refine patient selection criteria.

Our study has several strengths. It represents the most comprehensive meta-analysis to date on this topic, including a larger number of studies and patients compared to previous analyses. Notably, while the previous meta-analysis by Peng et al. primarily relied on only two studies to assess individual complications, our analysis includes data from a broader range of studies, providing a more reliable estimation of complication risks (11). Furthermore, it is the first meta-analysis to perform a subgroup comparison of survival outcomes based on tumor location and stage I NSCLC, providing novel insights that could guide clinical decision-making.

Our study has important limitations. First, we only included non-randomized studies, which may introduce bias given the confounding factors. However, PSM or PSW was applied in the majority of studies to minimize such limitations, and subgroup analysis of PSM + PSW data was performed. Secondly, we utilized the estimation of HRs from Kaplan-Meier curves using Web Plot Digitizer, as some studies did not provide HRs directly. This method, while commonly used, introduces significant variability due to differences in follow-up times across studies—further contributing to potential inconsistencies in the results. Third, there was significant heterogeneity in OS outcome. However, we performed a sensitivity analysis to address this finding. Moreover, we were unable to perform further subgroup analyses stratified by clinical nodal status due to incomplete or inconsistent reporting in the included studies. The studies included in this meta-analysis provided data from before the 9th TNM edition, and R(uncertain) status. Given its clinical importance, this aspect should be further investigated in future studies. Finally, most of the included studies originated from Asia, with a significant portion from China, limiting the generalizability of our findings to other populations.

Conclusions

In conclusion, this meta-analysis provides limited evidence that 4LND+ may offer a survival benefit in patients with left-sided NSCLC. However, the significant heterogeneity observed in the primary analysis and the lack of statistical significance in the PSM/PSW subgroup suggest cautious interpretation of the observed survival benefit. Contrary, it is associated with increased overall complication rates, including vocal cord palsy, which underscores the need for careful patient selection. Given the lack of OS benefit in stage I disease, 4LND+ may be more appropriate for patients with more advanced NSCLC. However, further prospective studies are needed to better define its role.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the MOOSE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-593/rc

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-593/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-593/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.

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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