Preoperative pulmonary function and nutrition predict survival in lung cancer patients with previous operated malignancies

Introduction

Significant advances in cancer treatment have led to an increased the incidence of multiple primary cancers, with previous epidemiological reports indicating a range from 2% to 17% (1-4). This trend is primarily attributed to improvements in diagnostic tests, more sophisticated treatments, and enhanced screening and surveillance of cancer survivors (2,5-8). The number of patients with multiple primaries is projected to rise further, as a longer follow-up period after the diagnosis of a primary cancer increases the likelihood of developing a second malignancy (5).

The treatment strategies differ substantially between synchronous and metachronous multiple primaries (9). For metachronous multiple primaries, successful treatment of the initial cancer is a prerequisite for considering curative-intent therapy for the second cancer. However, previous treatments—surgical, chemotherapeutic, or radiotherapeutic—may impair organ function, alter immune responses, and reduce tolerance to subsequent therapies (5). As a result, some patients may require modified treatment strategies, yet there are no established screening or treatment guidelines specific to multiple primaries.

Lung cancer is among the most common second primary cancers, with an incidence ranging from 13.4% to 22% (3), depending on the type and treatment of the initial malignancy (9). While prior studies have described the epidemiology of lung cancer in patients with previous malignancy (10,11), data on patient characteristics, prognostic factors, and tailored management strategies remain scarce. Prior malignancy has been associated with impaired organ function and reduced treatment tolerance, and patients with such history are often older, have more comorbidities, and are frequently excluded from clinical trials (9,12). Nakao et al. identified a history of previous malignancy as a significant predictor of poor postoperative survival in surgically resected lung cancer (13), but the mechanisms underlying this disadvantage remain unclear.

Patients with previous malignancy often undergo regular follow up after initial treatment, which may facilitate earlier detection of a second cancer compared with those without such history (11,14). Indeed, previous report has shown a higher proportion of pathological stage I disease in surgically resected lung cancer among patients with previous malignancy (13). While annual computed tomography (CT) screening has been reported to detect curable lung cancer (15), it remains unclear whether this potential lead-time advantage translates into improved postoperative survival.

The prognostic nutritional index (PNI), calculated from serum albumin levels and peripheral lymphocyte counts (16), reflects immunonutritional status. Low preoperative PNI (pre-PNI) has been associated with poor survival in non-small cell lung cancer (NSCLC) (17-19), including stage I (20,21) and stage IV disease (22). Similarly, reduced percent predicted forced expiratory volume in one second (%FEV1) is a known risk factor for adverse outcomes after lung cancer surgery (23-25). However, few studies have evaluated the prognostic significance of these factors specifically in patients with a history of cancer surgery—hereafter referred to as previous operated malignancy—a group potentially more vulnerable to surgical stress and cancer progression.

Therefore, this study aimed to characterize patients with primary lung cancer and a history of previous operated malignancy, and to identify prognostic factors—particularly preoperative PNI and FEV1—that could guide treatment selection and perioperative management in this high-risk population. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-844/rc).

Methods

This was a single-center, retrospective cohort study utilizing a lung cancer surgery database in the Department of Thoracic Surgery, Tohoku University Hospital, between 2010 and 2016. During the study period, 562 patients underwent pulmonary resection for primary lung cancer. Among them, 34 had R1 or more residual disease and were excluded. The remaining 528 patients who achieved R0 resection (no residual tumor) were included in the final analysis. In this study, “previous operated malignancy” was defined as a malignancy surgically treated under general anesthesia with pathological confirmation, prior to the diagnosis of lung cancer, regardless of the time interval between the two cancers.

Data collection

Clinical variables collected included:

• Demographics and baseline status: age, sex, height, body weight, smoking history, and performance status (PS).
• Cancer history: history of previous operated malignancy, site of prior cancer, and method of detection of lung cancer (screening, follow-up imaging, or symptoms).
• Lung cancer characteristics: clinical and pathological stages of lung cancer according to the eighth edition of the Union for International Cancer Control/American Joint Committee on Cancer (AJCC) TNM (tumor-node-metastasis) staging, tumor size, consolidation size, and tumor markers [carcinoembryonic antigen (CEA), squamous cell carcinoma antigen (SCC), Krebs von den lungen-6 (KL-6)].
• Pulmonary function tests: percent predicted forced vital capacity (%FVC), %FEV1, and percent predicted diffusing capacity for carbon monoxide (%DLco).
• Treatment-related data: extent of resection, lymph node dissection, operation time, and intraoperative blood loss.
• Follow-up outcomes: recurrence status, cause of death, overall survival (OS), recurrence-free survival (RFS), and lung cancer-specific survival (LCSS).

Definition of multiple primaries

Multiple primaries were defined according to the IACR/IARC (International Association of Cancer Registries and International Agency for Research on Cancer), which is currently the most common definition (26,27). To distinguish a new primary lung cancer from recurrence, the classical Martini-Melamed criteria were applied: lesions in a different lobe or contralateral lung and/or with a different histologic type were considered new primaries; when histology was identical, additional criteria such as a disease‑free interval ≥2 years, origin from carcinoma in situ, and absence of shared nodal or extrathoracic metastases were used (28). Final diagnosis was adjudication was made by two pathologists, with immunohistochemistry or molecular testing as needed (29-31).

Follow-up

Postoperative follow-up consisted of chest X-rays every three months for the first 2 years, CT every 6 months for the first 2 years, and annually thereafter until 5 years post-surgery. Additional imaging or examinations were performed if recurrence was suspected.

Statistical analysis

No formal sample size calculation was performed. All patients who met the eligibility criteria and underwent complete resection for primary lung cancer at our institution between 2010 and 2016 were consecutively included in this study.

All data were presented in numerical form as a percentage of the total sample size (N) or as a mean value with a standard deviation (SD). To identify the significant factors for predicting survival outcomes (OS, RFS, LCSS), a Cox proportional hazards analysis was performed. Subsequently, receiver operating characteristic (ROC) curve analysis was conducted using these factors to evaluate their feasibility in predicting OS and identify an optimal threshold, with the area under the curve (AUC) calculated to assess discriminatory ability. OS and RFS were calculated using the Kaplan-Meier method, and a log-rank test was performed for group comparisons. Patients with missing preoperative %FEV1 or PNI values were excluded from ROC and subgroup analyses. No imputation was performed. Statistical significance was set at P<0.05. All analyses were conducted using JMP version 16.4.0 (SAS Institute Inc., Cary, NC, USA).

Ethics

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Institutional Review Board of Tohoku University (No. 2021-1-912), and the requirement for informed consent was waived owing to the retrospective nature of the study.

Results

Patient characteristics

Figure 1 illustrates the patient selection flow. Of the 562 patients who underwent pulmonary resection, 34 with R1 or more residual disease were excluded, leaving 528 R0-resected patients for analysis. Among them, 153 had a history of previous operated malignancy. Table 1 summarizes the baseline characteristics. Among the 153 patients with previous operated malignancy, the most common primary sites were lung (n=41), stomach (n=23), and colorectum (n=22). Three patients had undergone surgery for multiple malignancies. Compared with those without previous operated malignancy, this group exhibited a significantly lower body mass index (BMI) and a lower number of PS 0 (85.6% vs. 90.9%, P=0.001). They also had lower pre-PNI, smaller tumor size (22.0 vs. 28.9 mm, P<0.001), and a higher rate of clinical stage ≤ IA3 disease (78.8% vs. 66.2%, P=0.007).

Figure 1 Flow of patient selection in this study. During the study period, 562 patients underwent pulmonary resection for lung cancer, of whom 34 had R1 or more residual disease. The remaining 528 patients with R0 resection were included in the analysis. Among them, 153 had a history of previous operated malignancy. Of the 293 patients with pathological stage 0–IA3 lung cancer, 106 had previous operated malignancy.

Regarding the detection pathway, lung cancer in the previous operated malignancy group was most often identified during follow-up or imaging for other diseases (81.7%), whereas screening was the main detection method in the group without previous operated malignancy. No significant differences were found between the two groups in terms of tumor markers (CEA, SCC, KL-6) or %FVC, %FEV1, and %DLco.

Surgical procedures

Patients with previous operated malignancy were significantly less likely to undergo segmentectomy or more extensive resection (77.1% vs. 91.5%, P<0.001; Table 1), lobectomy or more (67.9% vs. 87.4%, P<0.001), and ND2 or more extensive lymph node dissection (50.9% vs. 75.4%, P<0.001). Recurrence or mortality rates did not differ significantly between the two groups during follow-up.

Subgroup analysis in pStage 0–IA3

Of the total cohort, 293 patients (55.5%) had pStage 0–IA3 disease (Table 2). Among them, 106 (36.2%) had a history of previous operated malignancy. In this subgroup, detection during follow-up for other diseases was more frequent in the previous operated malignancy group than in the no-history group (82.0% vs. 33.6%, P<0.001), and tumor size was smaller (18.0 vs. 21.9 mm, P<0.001). This group also underwent fewer extensive resections and lymph node dissections. Recurrence and mortality rates remained similar between the groups.

Survival analysis

In the entire cohort, previous operated malignancy was not a significant prognostic factor for OS, RFS, or LCSS. However, in pStage 0–IA3 patients, previous operated malignancy was a significant predictor of poorer OS and RFS (Table 3).

Kaplan-Meier analysis showed no significant OS difference in the entire cohort (n=528, P=0.56; Figure 2A, A₁), but significantly worse OS in the pStage 0-1A3 subgroup with previous operated malignancy (n=293, P=0.03; Figure 2A, A₂). For RFS, no difference was seen in the entire cohort (Figure 2B, B₁, P=0.87), whereas the pStage 0–IA3 subgroup with no previous operated malignancy had significantly higher RFS (P=0.02; Figure 2B, B₂).

Figure 2 Kaplan-Meier curves for overall survival and recurrence-free survival according to the presence of previous operated malignancy. (A) Overall survival for all cohort (n=528) (A₁) and for patients with pStage 0–IA3 (n=293) (A₂). (B) Recurrence-free survival for all cohort (n=528) (B₁) and for patients with pStage 0–IA3 (n=293) (B₂).

Prognostic factor analysis

Univariate and multivariable analyses identified different prognostic factors across subgroups (Tables S1-S4). In pStage 0–IA3 patients with previous operated malignancy, both pre-%FEV1 and pre-PNI remained significant independent predictors of OS in multivariable analysis (Table 4).

ROC analysis and combined risk stratification

ROC curve analysis identified optimal thresholds of 101.1% for pre-%FEV1 (AUC 0.70) and 43.1 for pre-PNI (AUC 0.67) in predicting OS among patients with pStage 0–IA3 lung cancer and a history of previous operated malignancy (Figures S1). Based on these thresholds, 95 evaluable patients were stratified into four distinct subgroups (Table 5, Figure 3).

Figure 3 A color-coded visualization of the cases for preoperative %FEV1 (pre-%FEV1) and preoperative PNI (pre-PNI) is presented. Ninety-five cases were classified into four groups. The dotted line on the vertical axis represents the threshold for pre-PNI. The dotted line on the horizontal axis represents the threshold for pre-%FEV1. The black solid line indicates the correlation between pre-PNI and pre-%FEV1. %FEV1, percent predicted forced expiratory volume in 1 second; PNI, prognostic nutritional index.

Patients in Group 1 (pre-%FEV1 ≥101.1% and pre-PNI ≥43.1) demonstrated the most favorable outcomes, with both OS and RFS consistently superior to the other groups. Groups 2 and 3, characterized by impairment in either pre-%FEV1 or pre-PNI alone, showed intermediate survival outcomes, suggesting that functional or nutritional compromise in isolation confers a moderate adverse impact. Notably, Group 4, in which both pre-%FEV1 and pre-PNI were below the threshold, exhibited the poorest survival, with a 5-year OS of only ~80% and markedly higher recurrence rates (60%) compared to other groups (P<0.001).

Figure 4 illustrates these differences in Kaplan-Meier curves. OS curves (Figure 4A) clearly separated the four groups, with Group 4 patients showing a significantly higher risk of mortality compared with Groups 1–3. Similarly, RFS curves (Figure 4B) confirmed a consistent trend, highlighting the synergistic adverse impact of impaired pulmonary function and poor immunonutritional status. Importantly, the stepwise survival gradient across the groups underscores the additive prognostic value of combining pre-%FEV1 and pre-PNI, beyond the predictive capacity of either marker alone.

Figure 4 Survival outcomes stratified by combined pre-%FEV1 and pre-PNI categories. (A) Overall survival for all groups. (B) Recurrence-free survival for all groups. Group 1: patients with pre-%FEV1 ≥101.1% and pre-PNI ≥43.1; Group 2: patients with pre-%FEV1 ≥101.1% and pre-PNI <43.1; Group 3: patients with pre-%FEV1 <101.1% and pre-PNI ≥43.1; Group 4: patients with pre-%FEV1 <101.1% and pre-PNI <43.1.

This combined stratification model emphasizes that patients with early-stage lung cancer and a history of previous operated malignancy are not a homogeneous population; rather, their prognosis is strongly influenced by the interplay between pulmonary reserve and systemic nutritional/immune status.

Additional findings by cancer type

Patients with previous lung cancer surgery had significantly lower pre-%FEV1 than those without previous operated malignancy (95.8±18.0 vs. 102.8±21.5, P=0.02; Figure S2). Those with previous esophageal or gastric cancer surgery had significantly lower pre-PNI (46.9±5.5 vs. 48.7±4.8, P=0.04; Figure S3).

Discussion

One of the most notable findings of this study was that primary lung cancer was detected an earlier stage in patients with a history of previous operated malignancy compared with those without. In our current cohort, nearly 40% of such patients had no abnormal findings on chest X-ray, and their tumors were significantly smaller than that of their counterparts at the first visit to our department. These findings suggest that intensive follow-up after prior cancer treatment, often involving periodic CT examinations, contributed to early detection. Previous studies have reported that annual CT screening facilitates the identification of lung cancer at a curable stage, and long-term follow-up confirmed durable survival benefits (14,15). Thus, enhanced surveillance likely explains the earlier detection in our cohort. Despite this time advantage, however, patients with previous operated malignancy exhibited significantly worse OS when restricted to pathological stage 0–IA3 disease. This paradox indicates that host-related vulnerabilities, such as impaired pulmonary function, poor nutritional status, and comorbidities related to previous malignancy or its treatment, outweighed the survival benefit of early detection. Accordingly, early-stage diagnosis alone may not ensure improved outcomes in this population unless functional and nutritional reserves are simultaneously addressed.

Another important finding of this study was that prognostic determinants differed between patients with and without previous operated malignancy. In patients without such history, tumor-related factors, particularly tumor size and consolidation size, were dominant predictors of survival. Conversely, in patients with a history of previous operated malignancy, host-related parameters—specifically pre-%FEV1 and pre-PNI—emerged as significant prognostic indicators, even among those with early-stage lung cancer. This contrast highlights the importance of stratifying patients according to prior cancer history when evaluating prognostic factors and suggests that functional and nutritional status are more decisive than tumor burden in this subgroup.

The combined assessment of pre-%FEV1 and pre-PNI further refined risk stratification. ROC-derived thresholds enabled categorization into four groups, revealing a clear stepwise pattern of outcomes: patients with both preserved pulmonary function and nutritional status had the best survival, whereas those with impairments in both domains (Group 4) had markedly worse overall and RFS. To our knowledge, this is the first study to demonstrate that a combined model of pre-%FEV1 and pre-PNI provides a simple yet powerful tool for prognostic stratification in patients with previous operated malignancy. The clear separation across four groups underscores the synergistic impact of functional and nutritional impairment, offering an easily applicable framework for preoperative risk assessment and perioperative management.

From a clinical perspective, this combined model suggests two key targets for intervention: nutritional optimization and pulmonary rehabilitation. Preoperative nutritional support, including immunonutrition, and incorporation into structured Enhanced Recovery After Surgery (ERAS) protocols have been reported to improve perioperative outcomes and are now recommended (32-34). At the time of surgery in our cohort, ERAS pathways were not implemented, and supportive care was provided at the discretion of individual surgeons, preventing assessment of standardized interventions. Future studies should evaluate whether ERAS-based optimization of nutrition and pulmonary function can improve outcomes specifically in patients with impaired PNI and FEV1. In addition, pulmonary rehabilitation and pharmacologic optimization, including bronchodilators, have been shown to improve respiratory function and reduce postoperative complications (35-38). Given the relatively high threshold identified for pre-%FEV1 in our analysis, proactive rehabilitation and pharmacotherapy could help shift high-risk patients into lower-risk groups, thereby improving surgical tolerance and survival.

Although patients with previous operated malignancy were less likely to undergo lobectomy or ND2 dissection, particularly after prior thoracic surgery, these surgical factors were not independent predictors of OS in our analysis. Instead, host-related factors, namely pulmonary function and nutritional status, proved more decisive. This underscores the need to prioritize functional and nutritional optimization over surgical extent when managing this population.

The study had several limitations. First, this was a single-center, retrospective study with a limited sample size. Second, only patients with surgically treated prior malignancies were included, whereas those with non-surgically managed cancers were excluded. Moreover, detailed information on the treatment modalities for prior malignancies was not available, which may further limit the generalizability of our findings. Third, surveillance practices in Japan are relatively intensive compared to many other countries, leading to frequent CT examinations and earlier detection. This may limit the generalizability of our findings to regions with less stringent follow-up protocols. Fourth, because our cohort included cases from 2010–2016, results may differ under contemporary surgical and perioperative management strategies, including current ERAS implementation. Finally, the lack of detailed data on perioperative interventions such as nutritional support or pulmonary rehabilitation precluded assessment of their influence. Multicenter, prospective validation is warranted.

Conclusions

The findings of this study indicated that patients with previous operated malignancy are more likely to have lung cancer detected at an early stage but do not necessarily experience better survival. Host-related factors, particularly pulmonary function and nutritional status, outweigh the benefits of early detection and emerge as key prognostic determinants. The combined model of pre-%FEV1 and pre-PNI provides a simple, practical approach to risk stratification and may guide individualized perioperative interventions. Incorporating this model into structured ERAS-based protocols could represent a promising strategy to improve survival outcomes in this growing patient population.

Acknowledgments

The authors would like to express their sincerest gratitude to all members of the Department of Thoracic Surgery and our technical staff at Tohoku University Hospital, as well as to the patients and their families.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-844/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-844/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-844/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-2025-844/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. The study was approved by the Institutional Review Board of Tohoku University (No. 2021-1-912), and individual consent for this retrospective analysis was waived.

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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