Risk factors and survival associated with lung cancer recurrence after curative-intent surgery: beyond TNM pathological staging

Introduction

The care of patients with lung cancer continues to evolve. Rates of screening are increasing as early detection programs expand (1). Recent years have seen numerous emerging perioperative therapies that have resulted in decreased recurrence and improved survival (2-5). The use of minimally invasive surgical modalities especially robotic surgical platforms continues to rise (6). Despite these advances, lung cancer has been predicted to be the third most common cancer and the continued leading cause of cancer death until 2040 (6). Further attention to under investigated facets of the disease is certainly warranted. An improved understanding of recurrence rates after operations with curative intent may help make further progress in the treatment of non-small cell lung cancer (NSCLC).

Previous literature has suggested NSCLC recurrence rates range from 20–55% and may be improving with advancements in screening (7-10). Yet, the 3-year overall survival after recurrence has been reported as an abysmal 24% (11). The tumor, node, metastasis (TNM) staging system has proven to be an accurate predictor of survival and recurrence in NSCLC (12). However, there are additional risk factors and predictors of recurrence beyond those included in the TNM staging system that have not been studied extensively.

The objective of this study was to evaluate recurrence rates after surgical treatment of NSCLC, identify risk factors associated with recurrence emphasizing the assessment of factors not currently part of the TNM staging system, and to investigate risk factors associated with overall survival after recurrence. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1404/rc).

Methods

Data sources

The data obtained for this study were collected retrospectively from the electronic medical record and maintained in a database using REDCap (Research Electronic Data Capture) tools hosted at Mayo Clinic. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Institutional Review Board of Mayo Clinic (IRB # PR17-010802-05). A waiver of consent was provided given the retrospective nature of the study. Collected data included, but was not limited to patient characteristics, diagnosis, treatment details, and outcomes. The data represent patients from a single academic institution evaluated as a cohort.

Population

Patients 18 years of age and older diagnosed with NSCLC between 2004 and 2014 who underwent surgery with curative intent in the Division of Thoracic Surgery at Mayo Clinic in Rochester, Minnesota and were declared disease free in follow-up were considered for inclusion. Staging was according to the 7^th edition classification of the American Joint Committee on Cancer (AJCC). Patients with incomplete records or immediately lost to follow up were excluded. Post-resection surveillance followed national guideline recommendations at the time of treatment but consisted of clinical examination and CT scans of the chest at a minimum of 6-month intervals during the first 2–3 years, and yearly thereafter. Additional imaging was obtained as clinically indicated.

Variables

The associations of patient demographics [age, sex, race, body mass index (BMI), Zubrod functionality score, and smoking status], operative descriptors (type of surgical resection, surgical modality, number of lymph node stations sampled), and pathology findings on recurrence of disease were evaluated. Continuous quantitative variables were divided into quartiles. Variables were investigated in a categorical fashion and chosen prior to statistical analysis in order to limit bias.

Outcomes

Rates of NSCLC recurrence were calculated. Time to recurrence was calculated from the date of surgery to the date of first evidence of recurrence. Risk factors associated with cancer recurrence were identified and explored. Overall survival was considered from the date of surgery to the date of death from any cause. Overall survival was analyzed and compared for patients with and without recurrent disease. Risk factors associated with overall survival following disease recurrence were identified and explored.

Statistical analysis

The primary goals of the study were to define the frequency of recurrence in NSCLC patients who underwent surgery with curative intext, explore risk factors for recurrence, and evaluate overall survival following recurrence. Covariates were compared between patients who experienced and did not experience recurrence after surgery. T-tests were performed for continuous variables and chi-squared tests were performed for categorical variables. Kaplan-Meier analysis was used to evaluate 5-year recurrence rates. Risk factors of recurrence were identified using a time to event model and investigated with Kaplan-Meier analysis with log rank tests.

A secondary analysis of the association of positron emission tomography (PET) maximal standardized uptake value (SUVmax) with recurrence was performed using univariate analysis and Kaplan-Meier methodology.

Next, the study cohort was redefined to only those patients who had recurrence. Overall survival and predictors of survival were identified and investigated with individual Kaplan-Meier analyses and proportional hazard models. The software used to perform the statistical analysis was STATA (version 10.1, StataCorp, College Station, TX, USA). Statistical significance was defined by two-tailed P value <0.05.

Results

NSCLC recurrence after curative-intent pulmonary resection

There were 1,195 patients included in the study who underwent surgery with curative intent for NSCLC during the study period. From those patients, 394 or 33% were found to have recurrence of disease in follow-up. Table 1 compares patient demographics, tumor characteristics, and operative descriptors in patients with and without recurrence. Patients with recurrence were slightly older (69 vs. 68 years, P=0.02) and more frequently had a history of smoking (83% vs. 77.3%, P=0.01). There was no difference in gender, race, Zubrod score, histology, type or modality of surgical resections. There were further differences in extent of disease. Patients without recurrence were more likely to have pT1 tumors (61% vs. 44.2%, P<0.0001) and pN0 tumors (83.1% vs. 72.1%, P<0.0001). Patients with recurrence had higher rates of lymphovascular invasion (LVI) (11.7% vs. 5.9%, P<0.0001) and visceral pleural invasion (VPI) (32.2% vs. 19.2%, P<0.0001). The average follow up for patients was 3.8 years. The median was 4.5 years.

The overall trend in 5-year recurrence by pathologic staging is depicted in Figure 1. Rates were as follows: stage Ia 29%, stage Ib 39%, stage IIa 47%, stage IIb 59%, and stage III 57%. Of the 394 patients with recurrence, 147 (37.3%) had locoregional recurrence and 247 (62.7%) had distant recurrence. The distribution of location of distant recurrence is shown in Figure 2. The most common sites of distant recurrence were the contralateral lung (47.2%), bone (14.9%), and brain (12.8%).

Figure 1 Kaplan-Meier analysis of recurrence of lung cancer over 5 years by pathologic staging.

Figure 2 Locations of distant recurrence by frequency.

Risk factors for recurrence: impact of pathologic features and tumor metabolism

Analysis of risk factors for disease recurrence is shown with a time to event model in Table 2. Risk factors associated with recurrence included age >70 years [hazard ratio (HR) 1.56, P=0.003], wedge resection at the initial operation (HR 1.36, P=0.03), increasing T stage (HR >1.41, P<0.034 for all), LVI (HR 1.55, P=0.01), and VPI (HR 1.43, P=0.008). Recurrence rates associated with LVI and VPI were further investigated with Kaplan-Meier analysis in Figure 3. The 5-year recurrence rate with LVI was 63.2% compared to 36.4% without LVI (P<0.001). The 5-year recurrence rate with VPI was 55.2% compared to 33.6% without VPI (P<0.001).

Figure 3 Kaplan-Meier analysis depicting comparative 5-year recurrence stratified by left, LVI and right, VPI. LVI, lymphovascular invasion; VPI, visceral pleura invasion.

A subset analysis of 627 (52.5%) patients with available PET SUVmax values of the primary tumor prior to surgery is shown in Table 3, of which 232 (37%) developed recurrences. Initial primary tumor PET SUVmax was higher in patients who experienced recurrence (7.45 vs. 6.52, P=0.003). This trend is reflected by Kaplan-Meier analysis in Figure 4 where initial SUVmax scores are divided in quartiles, showing that higher SUVmax values were associated with higher rates of recurrence (P<0.001).

Figure 4 Kaplan-Meier analysis depicting comparative 5-year recurrence stratified by SUV maximums. SUV, standardized uptake value.

Impact of recurrence on overall survival

Patients without recurrence had a 5-year overall survival of 72.2% compared to 47.4% in those patients with recurrence (P<0.001). The subset of patients with recurrence was then analyzed. The median survival after recurrence was 12 months. Risk factors associated with survival after recurrence are shown in Table 4. Worse survival was identified in patients older than 76 years (HR 2.52, P<0.001), operations that included bilobectomy/sleeve resections (HR >2.92, P<0.039 for both), squamous cell carcinoma histology (HR 1.54, P=0.02) and distant recurrence (HR 1.45, P=0.02). Interestingly, patients who underwent a minimally invasive operation had improved survival (HR 0.57, P=0.001). Kaplan-Meier curves demonstrate survival in patients who initially underwent MIS resection and then recurred in Figure S1. MIS resection was associated with a survival of 71.1% compared to 56.7% in patients with an initial open operation (P=0.001). A comparison of survival between patients with locoregional versus distant disease recurrence is shown in Figure S2. The overall 5-year survival rate with locoregional disease was 56.2% compared to 42.7% with distant recurrence (P=0.01).

Finally, survival after recurrence was investigated in the subset of patients with a PET SUVmax recorded prior to surgery. This analysis is depicted in Figure S3. Higher tumor metabolic activity determined by increasing SUVmax was associated with worse long-term overall survival after recurrence. SUVmax of 0–2.9 had a survival of 59.7%, SUVmax of 3–4.9 had a survival of 58.7%, SUVmax of 5–9.9 had a survival of 43.7%, and SUVmax of 10+ had a survival of 34.8% at 5 years (P=0.02).

Discussion

Rates of cancer recurrence and the subsequent associated mortality remain a primary target of research as therapies for lung cancer continue to advance rapidly. Our study examined a large cohort of lung cancer patients that were followed closely at a single institution during a period of continued and prevalent advancement of minimally invasive operative techniques (13) but prior to many recent advancements in the perioperative use of immunotherapy and targeted therapies.

Recurrence

The recurrence rate in this study was found to be 33% which coincides with current literature describing rates between 20% to 55% (7-10). Increasing stage of disease was unsurprisingly associated with higher rates of 5-year recurrence. In our cohort, disease recurrence was most commonly distant as compared to locoregional. This rate and location suggest there is room for improvement with possible earlier identification of recurrence or improved identification of those patients most at risk for recurrence. Interestingly, Bille and colleagues studied patients who were screened following surgery and found higher rates of local as compared to distant disease at the time of identified recurrence (14). Comparing our studies one might hypothesize that an improved emphasis on ensuring compliance with postoperative surveillance protocols may help identify recurrence earlier and lead to improved outcomes. With regard to distant recurrences, locations were varied in our analysis. It would be difficult to conclude that more specific surveillance of a particular location would be warranted. However, further research is warranted to better understand the role of newer surveillance techniques, such as the monitoring of circulating tumor deoxyribonucleic acid (DNA), that may prove usefully in helping to improve risk stratification, prognostication, and early detection of recurrences (15).

Our study was able to identify several factors associated with disease recurrence beyond those included in the TNM staging classification. Wedge resections, LVI and VPI were shown to significantly increase risk of recurrence. In subset analysis, higher PET SUVmax was also directly associated with a higher risk of recurrence. Contemporary studies by Fick and colleagues similarly identified LVI, VPI, and PET SUV max as risk factors for recurrence and importantly risk factors of late recurrence (16,17).

Wedge resections for lung cancer have been an area of recent interest. In the CALGB140503 trial, Altorki and colleagues found that sub-lobar resections, including wedge resection, were non-inferior to lobectomy in peripheral NSCLC less than 2 cm (18). Specifically, no difference in survival or recurrence was noted. Our findings should be taken cautiously, as our patient population predates the publication of the CALGB140503 trial. Therefore, it is safe to assume that most patients that underwent a wedge resection in our cohort were not candidates for lobectomy due to limited pulmonary function, comorbidities, or multifocal disease, which might have resulted in wedge resections in cases with tumors >2 cm. Certainly, all of these factors impact long-term outcomes in this subgroup.

LVI has been shown to be a poor prognostic factor in varied cancers including gastric, colorectal, thyroid, and others (19-21). In our study, LVI increased odds of recurrence by 55%. Kaplan-Meier analysis at five-years demonstrated a recurrence rate increase from 36% to 63%. In comparative literature, Mollberg and colleagues combined 20 studies in a meta-analysis and found LVI was associated with significantly decreased recurrence free survival even after accounting for confounders (22). Despite the increasing evidence that LVI has prognostic value for poor outcomes, there remains room for novel research and innovation identifying how pathologic findings of LVI can be used to guide management.

Importantly, the recent editions of the TNM classification increases a tumor from T1 to T2 in the presence of VPI and upstages it to a minimum of stage IB (23). This change in part undersells the impact of VPI on outcomes. Maeda and colleagues demonstrated that overall survival for patients with VPI and LVI was less than that of patients with stage II disease and without these risk factors (24). Wang and colleagues found VPI to be an independent risk factor for worse disease-free survival (25). Our analysis expands those findings; odds of recurrence increased by 43% with the presence of LVI and Kaplan-Meier analysis of recurrence at five-years demonstrated a rate increase from 33% to 55%. Despite the inclusion of VPI in the TNM staging system, VPI merits additional consideration in following and treating lung cancer patients post-resection. Indeed, others have suggested similarly with Wightman and colleagues suggesting adjuvant chemotherapy should be considered in these patients due to an increase in rates of overall survival identified in their analysis (26).

Several studies have suggested that PET SUVmax may help to predict recurrence not only after surgical treatment but additionally after percutaneous ablation and radiotherapy (27-30). Our analysis adds credence to these findings as increased SUVmax was associated with higher recurrence in univariable and Kaplan-Meier analysis.

Overall, LVI, VPI and PET SUVmax might play a role in identifying higher risk sub-populations to evaluate the potential role of adjuvant therapies in patients with resected NSCLC <4 cm, N0, M0 who currently are not candidates for them.

Survival following recurrence

While recurrence rates have been reported in the literature, the impact of recurrence on survival and more specifically the risk factors associated with survival following recurrence after surgery have not been well analyzed. Fedor and colleagues compiled the data from limited studies and suggested overall survival varied from 7–26 months following recurrence (31). Our study shows 5-year survival rates drop from 72% to 47% in patients with recurrent disease and even more specifically, patients with locoregional recurrence have a 5-year survival of 56% which drops to 42% if recurrence is identified in a distant location. These differences highlight the importance of ongoing vigilance and surveillance after surgical resection of NSCLC, but also corroborate the need for improved perioperative therapies that can tackle the issue of distant recurrence. Novel methods such as measurement of circulating tumor deoxyribonucleic acid (ctDNA) might prove helpful in earlier identification of recurrence and need for further systemic therapy, independent of results of imaging studies. In our analysis, there were multiple non-modifiable risk factors for worse survival including age greater than 76, squamous cell histology, and more complex operations such as sleeve resection or bilobectomy. Interestingly, in our risk factor models for improved survival, patients who initially underwent a minimally invasive operation had improved survival following recurrence. It is difficult to interpret this finding. Perhaps, minimally operations lead to less scarring and an ability to identify recurrence sooner. Perhaps, it relates to selection bias, as patients who had non-minimally invasive operations may have been sicker or had larger tumors. In any case, our findings are in line with recent observations from a meta-analysis that showed a 21% reduction in the risk of death after VATS when compared to thoracotomy (32).

SUVmax levels were not only associated with disease recurrence but our study demonstrates a direct correlation with survival following recurrence after surgery. The more intense the SUVmax of the original primary tumor, the higher the rate of mortality after recurrence. SUVmax may prove to be useful in survival prediction models and may be useful in tailoring surveillance strategies or adjuvant therapies.

Limitations

Our study provides significant insight into disease recurrence and associated mortality but has a number of limitations. First, data were obtained retrospectively after outcomes had been determined. Second, the data were obtained from a single, large academic institution with data from multiple surgeons working with large teams of support staff who helped to care for the patients and keep close follow-up. This model is difficult and costly for other institutions to replicate which may lead to some degree of poor external validity. Third, our study required long term follow-up and results represent outcomes from operations and imaging modalities performed several years prior. Since the time the operations and images were performed, surgeons have had more experience with minimally invasive operations, imaging modalities have continued to improve, and treatment of cancer patients has changed with increasingly available immunotherapies and targeted therapies. These changes might have resulted in improved outcomes that are not captured by the present study.

Conclusions

Our study shows that NSCLC recurrence rates remain high following surgery with curative intent and that these recurrences have a significant impact on mortality. Recurrences most often are identified after disease has spread in a distant fashion. Risk factors such as LVI, VPI, and SUVmax may prove useful in predicting recurrence and identifying patients who deserve additional vigilance in surveillance. Lastly, there may be survival advantages in patients with recurrence who initially underwent minimally invasive surgery. Future research should be directed at recurrence rates in the era of expanding perioperative treatments including immune checkpoint inhibitors and targeted tyrosine kinase inhibitors, the role of LVI, VPI and tumor metabolic activity (SUVmax) in recurrence, and better ways to predict recurrence and improve survival after recurrence.

Acknowledgments

The abstract and data in this manuscript were first presented at the 2023 annual Chest meeting in Hawaii.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1404/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1404/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1404/prf

Funding: This work was supported by Medtronic.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1404/coif). All authors report that funding was provided by Medtronics. C.A.P. reports receiving lecture fees for the topic of lung cancer. J.S.R. reports receiving grant money from Intuitive for research on robotic bronchoscopy. The authors have no other 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. The study was approved by the Institutional Review Board of Mayo Clinic (IRB # PR17-010802-05). A waiver of consent was provided given the retrospective nature of the study.

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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