Postoperative short-term prognostic factors in patients with primary lung cancer who undergo lobectomy: a study on the prognostic predictors of early postoperative recurrence
Original Article

Postoperative short-term prognostic factors in patients with primary lung cancer who undergo lobectomy: a study on the prognostic predictors of early postoperative recurrence

Yuki Noda1,2 ORCID logo, Hideki Matsudaira1,2, Daiki Kato2, Takamasa Shibazaki2, Shohei Mori2, Takeo Nakada2, Mitsuo Yabe2, Jun Hirano2, Yoshiyuki Hoya1, Takashi Ohtsuka2

1Department of Surgery, Machida Municipal Hospital, Tokyo, Japan; 2Division of Thoracic Surgery, Department of Surgery, The Jikei University School of Medicine, Tokyo, Japan

Contributions: (I) Conception and design: H Matsudaira, Y Hoya; (II) Administrative support: J Hirano, S Mori; (III) Provision of study materials or patients: T Ohtsuka; (IV) Collection and assembly of data: M Yabe, H Matsudaira; (V) Data analysis and interpretation: D Kato, T Nakada, T Shibazaki; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

Correspondence to: Hideki Matsudaira, MD, PhD. Department of Surgery, Machida Municipal Hospital, 2-15-41 Asahi-cho, Machida, Tokyo 194-0023, Japan; Division of Thoracic Surgery, Department of Surgery, The Jikei University School of Medicine, Tokyo, Japan. Email: hideki.matsudaira@gmail.com.

Background: Lung cancer is among the most common types of cancers worldwide, and surgery can be a curative treatment option for this condition. However, some patients experience postoperative recurrence. Hence, predicting early postoperative recurrence to improve patient prognosis is important. This study aimed to determine the usefulness of nutritional inflammation indexes in predicting the prognosis of early recurrence after lung cancer surgery.

Methods: A retrospective cohort study was conducted on 310 patients with primary lung cancer who underwent lung lobectomy at Jikei University Hospital from January 1, 2013, to December 31, 2017. The prognostic nutrition index (PNI), neutrophil-to-lymphocyte ratio (NLR), platelet-to-lymphocyte ratio (PLR), and modified Glasgow prognostic score (mGPS) were calculated. The patients were classified into the high and low groups based on the receiver operating characteristic (ROC) curves. Furthermore, the association between these indexes and postoperative recurrence was analyzed via univariate analysis and using the Kaplan-Meier method.

Results: The mean age of the patients was 67.0 years, and the male-to-female ratio was 199:111. The mean observation period was 30.6 months. Patients with a low NLR and mGPS had a significantly longer 5-year recurrence-free survival than those with a high NLR and mGPS (P=0.045 and 0.02, respectively). Patients with a low PNI had a significantly higher 1-year recurrence rate than those with a high PNI (P=0.007).

Conclusions: The PNI is associated with 1-year recurrence, and NLR and mGPS are considerably associated with 5-year postoperative recurrence in patients with lung cancer. Hence, these nutritional inflammatory indices can be useful in predicting postoperative recurrence.

Keywords: Lung cancer; lobectomy; prognosis; prognostic factor

Submitted Jul 26, 2024. Accepted for publication Sep 27, 2024. Published online Nov 29, 2024.

doi: 10.21037/jtd-24-987

Highlight box

Key findings

• Patients with a low neutrophil-to-lymphocyte ratio (NLR) and modified Glasgow prognostic score (mGPS) had substantially longer 5-year recurrence-free survival.

• Low prognostic nutrition index (PNI) was associated with a significantly higher 1-year recurrence rate.

What is known and what is new?

• Nutritional and inflammatory markers can affect cancer prognosis.

• This study highlights specific indices (NLR, mGPS, and PNI) that are predictive of postoperative recurrence in patients with lung cancer.

What is the implication, and what should change now?

• For cases where surgical treatment is borderline due to advanced age or comorbidities, the application of our study findings can aid in reaching treatment decisions that account for recurrence risk. Furthermore, as neoadjuvant chemotherapy for lung cancer is expected to become more prevalent, these findings may potentially be appliable for evaluating the efficacy of such treatments.

• Further evidence in other cohorts are warranted to confirm the utility of regular monitoring with NLR, mGPS, and PNI in the early detection of recurrence risk in patients with lung cancer.

Introduction

Lung cancer is among the most common types of cancers worldwide and is associated with a high cancer-related mortality rate. In addition to smoking, a major cause of lung cancer, other factors such as air pollution and chemical exposure are also considered as etiologic agents. The prognosis of lung cancer is generally poor despite the availability of different treatment options including surgical intervention, radiotherapy, chemotherapy, and immunotherapy. Hence, prognostic factors should be identified to optimize treatment strategies and improve prognosis. Recent studies on lung cancer have identified several important markers (1,2) such as genetic mutations, serum protein markers, tumor antigens, immune checkpoint markers, and microRNAs, which can be used to accurately predict prognosis in patients with lung cancer. However, the evaluation of these markers requires tissue sampling and rare techniques. Therefore, prognostic factors that can be easily evaluated using straightforward and common preoperative measures are preferred. In addition, lung cancer is frequently associated with recurrence immediately after surgery. Therefore, markers that can establish prognosis in the early postoperative period are ideal. Previous studies have reported that nutritional inflammatory indexes derived from peripheral blood samples, such as the prognostic nutrition index (PNI), neutrophil-to-lymphocyte ratio (NLR), platelet-to-lymphocyte ratio (PLR), and modified Glasgow prognostic score (mGPS), are associated with prognosis in various carcinomas (3-6). These four indexes have been extensively examined since their initial development, with ongoing studies evaluating their use in determining efficacy and prognosis of various treatments, including surgery and chemotherapy. However, no clear data on markers with the best prognostic performance for lung cancer are unclear. Considering that patients with lung cancer commonly have a short time to recurrence after surgery, the current study aimed to determine markers strongly associated with early postoperative recurrence in lung cancer. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-987/rc).

Methods

This retrospective study included 310 patients who underwent radical lobectomy for primary lung cancer between January 1, 2013, and December 31, 2017, in the Jikei University Hospital. Patients with prior treatment for lung cancer, those who underwent surgery beyond bilobectomy, and those with hematologic disorders were excluded. All patients underwent physical examination, blood tests, chest X-ray, and chest computed tomography imaging. Thoracoscopic or open surgery was performed based on the decision made in a preoperative conference with Jikei thoracic surgery team, and lymph node dissection was performed. The diagnosis and classification on lung cancer were in accordance with the 8th edition of the World Health Organization and the TNM classification by Union for International Cancer Control. Patients were categorized into those with and without recurrence at one year after surgery, and the following were compared between the two groups: age, comorbidities, operation duration, blood loss, drainage duration, postoperative hospital stay, postoperative complications, pathologic stage, histologic type, PNI, NLR, PLR, and mGPS. PNI was calculated as follows: PNI = 10 × serum albumin (g/dL) + 0.005 × total peripheral blood lymphocyte count (/µL). NLR and PLR were calculated by dividing the number of neutrophils (/µL) by the number of lymphocytes and dividing the number of platelets (/µL) by the number of lymphocytes (/µL). In the previous study, the following scoring system was used for mGPS: mGPS of 0, C-reactive protein (CRP) level of ≤0.5 mg/dL and serum albumin level of ≥3.5 g/dL; mGPS of 1, CRP level of >0.5 mg/dL or serum albumin level of <3.5 g/dL; mGPS of 2, CRP level of >0.5 mg/dL and serum albumin level of <3.5 g/dL (3). All prognostic factors were calculated using blood tests performed within 1–3 days before surgery.

The present study was approved by the Ethics Committee of Jikei University School of Medicine (approval date, February 12, 2020; approval No. 31-384[9964]). The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The need for individual patient consent was waived due to the retrospective study design.

Statistics analysis

Dichotomous demographic data were compared using the Fisher’s exact test or Student’s t-test. The distribution of continuous data was assessed using histograms and the Shapiro-Wilk test. Normally distributed data were analyzed using the independent samples t-test. However, there were 35 cases of random missing data out of 310 cases for the variables of operative time and blood loss only, and the analysis was performed using simple imputation. The receiver operating characteristic (ROC) curves for PNI, NLR, PLR, and mGPS were constructed based on recurrence within one year after surgery, and cutoff values were determined. We used the Kaplan-Mayer method to compare 1- and 5-year recurrence-free survival with a log-rank test. We conducted hazard risk analysis using the Cox proportional hazards model. All statistical analyses were performed using EZR, 2012 (Saitama Medical Center, Jichi Medical University; http://www.jichi.ac.jp/Saitama-sct/SaitamaHP.files/statmedEN.html; Kanda, Japan), which is a graphical user interface for R (Version 2.13.0; the R Foundation for Statistical Computing, Vienna, Austria) (7). All P values were two-sided, and a P value of <0.05 was considered statistically significant.

Results

In the overall cohort, mean patient age was 67.0 years, with a male/female ratio of 199:111. Mean observation period was 30.6 months. Of the overall cohort of 310 patients, comorbidities were present in 149 patients, and mean Charlson Comorbidity Index score was 1 in both the recurrence and no-recurrence groups. There were 47 (17.9%) and 7 (14.9%) postoperative complications in the no-recurrence and recurrence groups, respectively, with no significant difference. Complications included prolonged air leak, arrhythmia, pneumonia, pyothorax, subcutaneous emphysema, and induction of Home Oxygen Therapy in 26, 8, 4, 3, 3, and 2 patients, respectively, and chylothorax, atelectasis, recurrent nerve palsy, delirium, stroke, wound infection, liver dysfunction, and superior mesenteric artery thrombosis in 1 patient each. The more severe complication was selected in cases with multiple postoperative complications. There were no in-hospital mortalities. The mean postoperative hospital stay was 8.4 days in the no-recurrence group and 8.1 days in the recurrence group with no statistical significance. The two groups did not exhibit significant differences in mean chest drain duration, operative time, or blood loss. Comparison of the patient background characteristics and PNI, NLR, PLR, and mGPS between recurrence and no-recurrence groups with univariate analysis are presented in Table 1. Briefly, the pathologic stage, histologic type, and NLR were significantly different between the two groups. Figure 1 illustrates the ROC curve analyses used for determining the cutoff values for PNI, NLR and PLR, and the patients were divided into those with high and low values, only mGPS was grouped by score.

Table 1

Patients characteristics

Patients characteristics Univariate analysis P value
No recurrence (n=263) Recurrence (n=47)
Sex 0.41
   Male 166 33
   Female 97 14
Age (years) 67 68 0.77
Comorbidities (CCI score) 1 1 0.64
Operation time (min) 261 261 0.97
Blood loss (mL) 104 159 0.28
Postoperative hospital stay (day) 8.4 8.1 0.75
Chest drain (day) 3.9 4.5 0.15
Complications 47 (17.9%) 7 (14.9%) 0.84
pStage <0.001
   IA 161 8
   IB 51 11
   IIA 18 12
   IIB 13 7
   IIIA 20 9
Histologic type 0.03
   Ad 197 31
   SCC 52 8
   Others 14 8
PNI 48.8 47.4 0.10
NLR 2.53 2.88 0.18
PLR 144.1 155.3 0.31
mGPS 0.24 0.47 0.02
CEA (ng/mL) 6.1 7.5 0.56

CCI, Charlson Comorbidity Index; Ad, adenocarcinoma, SCC, squamous cell carcinoma; PNI, prognostic nutrition index; NLR, neutrophil-to-lymphocyte ratio; PLR, platelet-to-lymphocyte ratio; mGPS, modified Glasgow prognostic score; CEA, carcinoembryonic antigen.

Figure 1 ROC curve for each parameter. ROC curves and cutoff values for each prognostic factor of 5- and 1-year recurrence were calculated, and patients were divided into the high and low groups. (A) PNI for 5 years. (B) NLR for 5 years. (C) PLR for 5 years. (D) PNI for 1 year. (E) NLR for 1 year. (F) PLR for 1 year. PNI, prognostic nutrition index; NLR, neutrophil-to-lymphocyte ratio; PLR, platelet-to-lymphocyte ratio; AUC, area under the curve; ROC, receiver operating characteristic.

The 1-year recurrence rate was higher in patients with low PNI than in those with high PNI (27.8% vs. 6.7%; P=0.02). However, no significant difference in the recurrence rate between patients with high and low PLR, NLR, or mGPS was noted (Table 2).

Table 2

Fisher test for each parameter in recurrence within 5 years and 1 year

Fisher test for each parameter Fisher χ2 (high:low) P value
No recurrence Recurrence
Recurrence within 5 years† n=263 n=47
   PNI 136:127 20:27 0.27
   NLR 137:126 17:30 0.057
   PLR 52:211 6:41 0.31
   mGPS‡ 212:40:11 30:12:5 0.02
Recurrence within 1 year§ n=287 n=23
   PNI 269:18 18:5 0.02
   NLR 155:132 8:15 0.09
   PLR 226:61 15:8 0.19
   mGPS‡ 227:47:13 15:5:3 0.10

†, for recurrence within 5 years, PNI was 49. NLR was 2.1, and PLR was 91.4. The recurrence rate was divided into two groups: high and low. ‡, since only mGPS is categorized by scores, it is represented as (0:1:2). §, for recurrence within 1 year, PNI was 40. NLR was 2.2, and PLR was 184.4. The recurrence rate was divided into two groups: high and low. PNI, prognostic nutrition index; NLR, neutrophil-to-lymphocyte ratio; PLR, platelet-to-lymphocyte ratio; mGPS, modified Glasgow prognostic score.

Results of the Fisher’s exact test dividing the ROC curve into high and low groups (mGPS by score) revealed that PNI was associated with 1-year prognosis. Log-rank test for 5-year recurrence-free survival (Figure 2) revealed that patients with low NLR and mGPS had significantly longer recurrence-free periods than those with high NLR and mGPS (P=0.045 and 0.02, respectively). As illustrated in Figure 3, 1-year recurrence-free survival revealed that the recurrence rate was significantly higher in patients with low PNI than in those with high PNI (P=0.007), and significant differences were not observed when patients were categorized according to the low and high values for the other markers.

Figure 2 Recurrence-free survival in 5 years. Kaplan-Meier method was used to draw the survival curve for each prognostic index within 5 years. Log-rank test was used to investigate 5-year recurrence, and results indicated a significant difference in recurrence rates based on NLR and mGPS. NLR, neutrophil-to-lymphocyte ratio; mGPS, modified Glasgow prognostic score; PLR, platelet-to-lymphocyte ratio; PNI, prognostic nutrition index; HR, hazard ratio.
Figure 3 Recurrence-free survival in 1 year. Survival curves were created for each prognostic index in 1 year, as depicted in Figure 2. Results revealed that the group with a lower PNI had significantly high recurrence rates. NLR, neutrophil-to-lymphocyte ratio; mGPS, modified Glasgow prognostic score; PLR, platelet-to-lymphocyte ratio; PNI, prognostic nutrition index; HR, hazard ratio.

Discussion

Although pathological staging is the gold standard for predicting cancer prognosis, studies evaluating inflammation, nutritional value, and prediction in patients with advanced cancer confirm the association of increased neutrophil percentage in peripheral blood with prognosis (8-10). The influence of inflammatory factors on the development and progression of cancer and its pathogenesis is increasingly recognized. The mechanism underlying their impact on cancer is not completely understood. However, neutrophils promote tumor cell growth by releasing growth factors, oxygen free radicals, proteases, and chemokines and by activating related nuclear factors.

Our analyses indicated that NLR and mGPS were useful prognostic markers to predict long-term recurrence in patients with lung cancer who undergo surgical resection. Additionally, only PNI was associated with the risk of recurrence within the first postoperative year. These findings are consistent with previous studies on predictors of various cancers, including lung cancer (11-15). First, NLR reflects the balance between the host immune response and tumor microenvironment and is considered a marker of systemic inflammation (2). Inflammation plays an important role in tumor growth, invasion, and metastasis by promoting angiogenesis, immunosuppression, and tumor cell survival. The NLR is a predictor of poor survival in several types of cancers, including lung cancer (1,11,12,16-18).

mGPS, which is based on serum levels of CRP and albumin, is another useful marker for predicting cancer prognosis (13). CRP is an acute phase protein that reflects systemic inflammatory response, whereas albumin is a marker of nutritional status. mGPS is associated with clinical outcomes in various cancer types, including lung cancer. In the present study, we found that patients with a high mGPS were at significantly higher risk of recurrence than those with a low mGPS, consistent with previous studies demonstrating the prognostic value of mGPS in patients with lung cancer (8,19). PNI, a marker of nutritional status, reflects the immune and nutritional status of the host. Onodera et al. was the first to report the association between cancer and perioperative risk using a parameter calculated using serum albumin level and peripheral blood lymphocyte count (20). Since then, numerous studies elucidated the association between immunity and cancer, with some reporting an association between the immune status and prognosis in several cancers (3-6). PNI has been reported as a prognostic predictor of various cancers, including non-small cell carcinoma (15,21,22). In the present study, PNI was significantly associated with recurrence within the first postoperative year but not with long-term prognosis, which is a new finding. Conversely, we did not find a significant difference in the recurrence rate between the patients with high and low PLR. PLR is a marker of systemic inflammation that reflects the balance between platelet activation and lymphocyte-mediated immune response. The prognostic value of PLR in lung cancer has been investigated in several studies, with contradictory findings (8,9,23-25). In the present study, we did not find a significant association between PLR and recurrence in patients with lung cancer who underwent surgical resection. Based on previous studies, information on prognostic indexes, which can be easily obtained preoperatively, can aid in reaching a decision on appropriate treatment modalities, such as surgery, chemotherapy, and radiotherapy. A recent study has investigated the use of preoperative chemotherapy for non-small cell lung cancer (26). For example, determination of PNI and mGPS using preoperative blood samples might aid in determining the priority between surgery and preoperative chemotherapy.

Our findings should be interpreted with the consideration of its limitations. First, this was a single-center retrospective study and the potential for selection bias remains. Second, the sample size was relatively small; therefore, the statistical power might be limited. In studies similar to the present one, in which clearly defined cutoffs for indexes are not utilized, larger sample sizes are desirable. Moreover, various composite factors based on inflammation and nutrition are currently under investigation for their prognostic utility, and a study evaluating systemic immune-inflammation index and advanced lung cancer inflammation index are anticipated (27). Third, we examined the prognostic value of inflammatory markers only in patients who underwent surgical resection and did not consider postoperative chemotherapy as an outcome. It is unclear whether these markers would be useful in predicting outcomes in patients who received treatments other than surgery, such as chemotherapy or radiotherapy. Fourth, there were patients who did not receive adjuvant chemotherapy according to the guidelines for various reasons, and the details could not be tracked. This may have affected the recurrence rate. However, the rate of recurrence was not higher among patients with stage II or worse disease. Finally, the histologic type of lung cancer was not restricted to non-small cell lung cancer. Although this also did not bias the number of recurrent cases toward small cell carcinoma, its influence could not be ruled out.

Conclusions

Our findings suggest that PNI might be a useful marker to predict short-term recurrence in patients undergoing radical lobectomy for primary lung cancer. PNI is a cost-effective marker that can be easily calculated and incorporated into routine clinical practice. Unlike other cancers, lung cancer is often not definitively diagnosed preoperatively. PNI, which can be easily obtained by preoperative blood sampling, may assist respiratory surgeons in making treatment decisions. Further studies with larger sample sizes and more diverse patient populations are needed to validate our findings and to elucidate the potential utility of PNI in predicting outcomes in patients who receive treatments other than surgery.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-987/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-987/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-987/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-987/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 present study was approved by the Ethics Committee of Jikei University School of Medicine (approval date, February 12, 2020; approval No. 31-384[9964]). The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The need for individual patient consent was waived due to the retrospective study design.

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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Cite this article as: Noda Y, Matsudaira H, Kato D, Shibazaki T, Mori S, Nakada T, Yabe M, Hirano J, Hoya Y, Ohtsuka T. Postoperative short-term prognostic factors in patients with primary lung cancer who undergo lobectomy: a study on the prognostic predictors of early postoperative recurrence. J Thorac Dis 2024;16(11):7490-7498. doi: 10.21037/jtd-24-987

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