Reasearch ArticleClinical Studies

Large Tumor Size and High Neutrophil-to-lymphocyte Ratio Predicts Poor Prognosis After Pneumonectomy or Sleeve Lobectomy in Patients With Non-small-cell Lung Cancer

TAKUMA TSUKIOKA, NOBUHIRO IZUMI, HIROAKI KOMATSU, HIDETOSHI INOUE, RYUICHI ITO, SATOSHI SUZUKI and NORITOSHI NISHIYAMA
Anticancer Research June 2022, 42 (6) 3029-3034; DOI: https://doi.org/10.21873/anticanres.15788

Abstract

Background/Aim: The neutrophil-to-lymphocyte ratio (NLR) and platelet-to-lymphocyte ratio (PLR) are useful biomarkers in non-small cell lung cancer (NSCLC). The aim of this study was to identify novel prognostic factors after pneumonectomy or sleeve lobectomy. Patients and Methods: The clinical courses of 68 patients with NSCLC who underwent pneumonectomy or sleeve lobectomy were retrospectively investigated. Results: High NLR (p=0.002) and PLR (p=0.006), and large tumor (>40 mm) (p=0.024) were indicative of poor prognosis in univariate analysis. High NLR (p=0.021) and large tumor (>40 mm) (p=0.017) remained independent factors indicating poor prognosis in multivariate analysis. Eighteen patients with both high NLR and large tumor (>40 mm) had significantly poorer prognoses than the remaining patients, 10 of them having recurrences within a short time after surgery. Conclusion: A high NLR and large tumor size indicate a poor prognosis after pneumonectomy or sleeve lobectomy. Our findings may be helpful in selecting optimal treatments for this subgroup of patients.

Key Words:

Systemic inflammatory responses play a key role in cancer growth, development, invasion, and metastasis (1). Inflammatory biomarkers, such as the neutrophil-to-lymphocyte ratio (NLR) and platelet-to-lymphocyte ratio (PLR), are reportedly factors indicating poor prognosis in patients with non-small cell lung cancer (NSCLC) (2-4).

We perform pneumonectomy to remove centrally located advanced NSCLC or NSCLC with hilar lymph node metastasis. Sleeve lobectomy is performed when anatomically feasible and margin-negative resection can be achieved. The type of surgical procedure, pathological N status, and pathological T status are reportedly prognostic factors in patients who have undergone pneumonectomy or sleeve lobectomy (5, 6). However, to the best of our knowledge, the effects on prognosis of inflammatory biomarkers, such as NLR and PLR, have not yet been investigated in patients with NSCLC who have undergone these surgical procedures. Identifying prognostic factors in patients undergoing invasive surgery is potentially helpful in selecting optimal treatments.

The aim of this study was to identify novel prognostic factors in patients with locally advanced NSCLC who had undergone pneumonectomy or sleeve lobectomy.

Patients and Methods

Clinical and pathological staging was determined according to the eighth edition of the TMN Classification of Malignant Tumors (7). We retrospectively investigated the clinical courses of 68 patients with NSCLC who underwent pneumonectomy or sleeve lobectomy at our Institute from January 2010 to December 2019. Right lower sleeve lobectomy was selected to avoid middle and lower bilobectomy. Patients who had undergone right lower sleeve lobectomy were excluded from the analyses. Before surgery, all patients gave informed consent for the use of their examination data in clinical studies. This study was approved by the local Institutional Ethics Committee (Approval no. 4403, approval date: 3 October 2019).

Mediastinal lymph nodes with a short axis of >10 mm on enhanced computed tomography were diagnosed as clinically positive for metastasis. The criteria for surgical resection were the absence of distant metastasis, no cancer cell-positive pleural or pericardial effusion, no N2 disease at two or more mediastinal levels, no bulky N2 disease, no N3 disease, and a predicted postoperative vital capacity of >40%. Patients with T4 lung cancer with N0 or N1 nodal extension and tumors that could be completely removed were considered candidates for surgery. Sleeve lobectomy was performed when anatomically appropriate. Bronchial stumps were confirmed to be free of cancer cell infiltration through intraoperative pathological examination.

Induction chemoradiotherapy with platinum-based doublet and concurrent radiotherapy (40 Gy) was mainly recommended for patients with enlarged but completely removable N2 lymph node metastasis but was not mandatory for all patients with N2 lymph node metastasis. Patients with pathological stage II and III lung cancer received adjuvant platinum-based doublet chemotherapy, while those with stage I lung cancer received oral tegafur adjuvant chemotherapy. We did not set criteria for omitting adjuvant treatment, and such treatments were initiated at the discretion of the physician in charge of each case.

After discharge, all patients underwent follow-up chest radiographs and measurement of tumor markers every 2 to 4 months, with computerized tomography after 6 months and every year thereafter. The final follow-up review was conducted on 31 December 2021.

Blood samples were obtained within a few days before surgery. Body height and weight were measured at the time of hospital admission. Comorbidities were defined as disorders being treated at the time of diagnosis of the primary lung cancer. Medians were used as cut-off points for age, NLR, PLR, and tumor size. The cut-off for body mass index was calculated in accordance with World Health Organization guidelines (8). Overall survival after surgery was calculated using the Kaplan–Meier method and survival differences were compared using the log-rank test. Independent risk factors associated with survival were calculated using a Cox proportional hazard model. A p-value of less than 0.05 indicated statistical significance. Statistical analyses were carried out using JMP 10 software (SAS Institute, Cary, NC, USA).

Results

Table I shows the study patients’ characteristics. Pneumonectomy was performed in 14 patients and sleeve lobectomy in 54. Locoregional recurrence was identified in three patients, two of whom had recurrence at the chest wall cut end and the third at the residual lung tissue cut end. Table II shows the results of univariate and multivariate analyses for predictors of poor prognosis. High NLR (p=0.002) and PLR (p=0.006), and large tumor (>40 mm) (p=0.024) were significant predictors of poor prognosis according to univariate analysis. However, only high NLR (p=0.021) and large tumor (>40 mm) (p=0.017) were found to be independent predictors of poor prognosis by multivariate analysis.

View this table:
Table I.

Characteristics of patients in this study (N=68).

View this table:
Table II.

Univariate and multivariate analyses of prognostic factors.

Figure 1 shows overall survival curves according to NLR and tumor size. Patients with both high NLR and large tumor (>40 mm) had significantly poorer prognoses than the remaining patients.

Figure 1.
Figure 1.

Overall survival curves according to the neutrophil-to-lymphocyte ratio (NLR) and tumor size.

Table III shows the characteristics of the 18 patients with both high NLR and large tumor (>40 mm). Four of these patients had pathological N2 lymph node metastasis and 10 of them developed recurrences during the study period. All lymph node recurrences occurred outside of the usual dissection area. Recurrence was commonly identified shortly after surgery.

View this table:
Table III.

Detail characteristics of patients with both tumor size >40 mm and neutrophil-to-lymphocyte ratio >3.1 (N=18).

Discussion

In this retrospective study, we found that high NLR and PLR, and large tumor were predictors of poor prognoses after pneumonectomy or sleeve lobectomy in patients with locally advanced NSCLC. Moreover, high NLR and large tumor were independent predictors of poor prognoses in this cohort. Patients with both high NLR and large tumors had significantly poorer prognoses than the remaining patients. Our findings may be helpful in selecting optimal treatments for patients with locally advanced NSCLC.

Inflammatory cells such as neutrophils and lymphocytes play an important role in tumor progression. A high NLR indicates the presence of tumor-associated inflammation, neutrophil-mediated tumor progression, and suppression of lymphocytic antitumor immune responses (1). Circulating tumor cells (CTCs) are cancer cells that have escaped from the primary lesion or from metastatic foci and entered the bloodstream, denoting a switch from localized to systemic disease (9). It has been reported that the NLR is significantly higher in CTC-positive than in CTC-negative patients with pancreatic ductal adenocarcinoma (10). Additionally, neutrophils secrete vascular endothelial growth factor and proteases into the bloodstream, promoting adhesion of CTCs and their seeding in distant organs (11, 12). The current findings are consistent with previous findings, our study patients’ recurrences commonly taking the form of distant organ metastasis rather than local recurrence.

Large tumor size is reportedly a significant predictor of poor prognosis in locally advanced, operable NSCLC (6, 13), which our findings confirm. In this study, we found that both large tumors and high NLR were independent predictors of poor prognosis. There was no difference in NLR values for those with tumor size of 40 mm or less than or more 40 mm (p=0.218), indicating that large tumor size and high NLR are not associated with each other. There is reportedly no correlation between CTC count and pathological T factors in patients with NSCLC (14, 15). It has been reported that hypoxia-inducible factor 1 alpha (HIF-1α) is more frequently expressed in patients with operable NSCLC and T2 stage than in those with T1 stage disease (16). HIF-1α plays a central role in progression of NSCLC. HIF-1α expression has a demonstrable impact on survival and vascular endothelial growth factor is consistently more strongly expressed in patients with strong expression of HIF-1α (17). Thus, the poor prognosis of patients with large tumors is likely attributable to various mechanisms, including the HIF-1α pathway. We believe that several mechanisms are involved in patients with both high NLR and large tumors.

Although we succeeded in preoperatively identifying patients with poor prognoses in our study cohort, no effective measures for improving their outcomes have yet been identified. Conventional platinum-doublet adjuvant chemotherapy did not have a beneficial effect on our patients’ prognoses. Adjuvant molecular therapy has been demonstrated to have beneficial effects in patients with lung adenocarcinoma (18). However, squamous cell carcinoma was a more common histological subtype in our patients. Use of immune checkpoint inhibitors has been approved for treatment of advanced and metastatic solid tumors of many types. Nonetheless, their only established role in an adjuvant setting is after resection of melanomas (19). No benefit of adjuvant immunotherapy in patients with NSCLC has yet been identified. Surgical resection following induction therapy with chemotherapy plus nivolumab is reportedly safe and achieves acceptable oncological outcomes in patients with locally advanced NSCLC (20). Moreover, immunochemotherapy followed by sleeve lobectomy is reportedly feasible and has favorable outcomes in patients with locally advanced NSCLC (21). Of note, Bott et al. reported a high incidence of inflammatory responses and fibrosis at sites of the primary tumor and involved nodal stations after neoadjuvant administration of nivolumab (22). Establishment of novel perioperative treatments for locally advanced NSCLC is needed.

Pneumonectomy is commonly performed for more advanced NSCLC. In a study including a large number of patients, prognosis was significantly poorer after pneumonectomy than after sleeve lobectomy. However, after propensity scorematching, the difference in prognosis was no longer significant (5). Local recurrence reportedly occurs more frequently after sleeve lobectomy than after pneumonectomy in patients with node-positive NSCLC (23). In the current study, pneumonectomy was not a factor for poor prognosis. We commonly perform pneumonectomy for advanced NSCLC when this procedure is the only means of achieving complete resection and the patient has adequate respiratory function.

This study had some limitations. Firstly, it was a small retrospective study. Accumulation of data from more patients and further analyses are now ongoing. Secondly, surgical procedures and ancillary treatments were selected at the discretion of the physician in charge of each case. Hence, selection criteria for surgical procedures and perioperative therapy should be established. Thirdly, our identification of prognostic factors is only of theoretical value in the absence of effective treatment. We are planning to investigate the molecular mechanisms underlying poor prognoses in patients with NSCLC in whom sleeve lobectomy or pneumonectomy is required to achieve complete tumor removal. Finally, the immunonutritional condition was reported to be an important indicator of efficacy of lung cancer treatments (24). The immunonutritional status should also be investigated in further analyses.

In conclusion, high NLR and large tumor size are independent predictors of poor prognosis after pneumonectomy or sleeve lobectomy in patients with NSCLC. Patients with both high NLR and large tumors have significantly poorer prognoses than other patients. Our findings may be helpful in selecting optimal treatments for locally advanced NSCLC.

Footnotes

  • Authors’ Contributions

    Takuma Tsukioka designed this study, analyzed the data, prepared the figures, and wrote original draft. Hiroaki Komatsu, Hidetoshi Inoue, Ryuichi Ito and Satoshi Suzuki collected the clinical data. Nobuhiro Izumi and Noritoshi Nishiyama critically reviewed the article. All Authors read and approved the final article.

  • Conflicts of Interest

    The Authors have no conflicts of interest to declare regarding this study.

  • Received April 14, 2022.
  • Revision received May 6, 2022.
  • Accepted May 10, 2022.

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Large Tumor Size and High Neutrophil-to-lymphocyte Ratio Predicts Poor Prognosis After Pneumonectomy or Sleeve Lobectomy in Patients With Non-small-cell Lung Cancer
TAKUMA TSUKIOKA, NOBUHIRO IZUMI, HIROAKI KOMATSU, HIDETOSHI INOUE, RYUICHI ITO, SATOSHI SUZUKI, NORITOSHI NISHIYAMA
Anticancer Research Jun 2022, 42 (6) 3029-3034; DOI: 10.21873/anticanres.15788
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