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 Table of Contents  
ORIGINAL ARTICLE
Year : 2016  |  Volume : 12  |  Issue : 2  |  Page : 945-951

Prognostic impact of the high-sensitivity modified Glasgow prognostic score in patients with resectable non-small cell lung cancer


Department of Regenerative Surgery, School of Medicine, Fukushima Medical University, Fukushima 960-1295, Japan

Date of Web Publication25-Jul-2016

Correspondence Address:
Hiroyuki Suzuki
Department of Regenerative Surgery, School of Medicine, Fukushima Medical University, 1 Hikarigaoka, Fukushima 960-1295
Japan
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0973-1482.176168

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 > Abstract 


Objective: The present study compared the prognostic value of the Glasgow prognostic score (GPS), modified GPS (mGPS), high-sensitivity mGPS (HS-mGPS), neutrophil/lymphocyte ratio (NLR), platelet/lymphocyte ratio (PLR), prognostic index (PI), and prognostic nutritional index (PNI) in patients with resectable non-small cell lung cancer (NSCLC).
Materials and Methods: This retrospective study included 327 consecutive patients with resectable NSCLC with a follow.-up period. >5. years. Initially, the HS-mGPS was directly compared with the GPS and mGPS in terms of their ability to predict survival in patients with resectable NSCLC. Second, inflammation.-based scores, including the HS-mGPS, NLR, PLR, PI, and PNI, were analyzed preoperatively using multivariate Cox analysis. Clinical characteristics reflecting cancer progression were also analyzed.
Results: Elevated GPS (P < 0.001), mGPS (P < 0.001), and HS-mGPS (P < 0.001) levels were associated with reduced overall survival. The HS-mGPS (P < 0.001) was superior to the GPS and mGPS (P = 0.884) as a prognostic marker of postoperative outcomes. On multivariate Cox analysis, age (P = 0.026), p-T status (P < 0.001), p-N status (P < 0.001), lymphatic vessel invasion (P = 0.008), and the HS-mGPS (P = 0.016) were independent prognostic factors for survival.
Conclusion: These results suggest that the HS-mGPS might have a greater prognostic impact than the GPS, mGPS, NLR, PLR, PI, or PNI in patients with resectable NSCLC.

Keywords: Glasgow prognostic score, high-sensitivity modified Glasgow prognostic score, modified Glasgow prognostic score, nonsmall cell lung cancer, surgery, survival


How to cite this article:
Osugi J, Muto S, Matsumura Y, Higuchi M, Suzuki H, Gotoh M. Prognostic impact of the high-sensitivity modified Glasgow prognostic score in patients with resectable non-small cell lung cancer. J Can Res Ther 2016;12:945-51

How to cite this URL:
Osugi J, Muto S, Matsumura Y, Higuchi M, Suzuki H, Gotoh M. Prognostic impact of the high-sensitivity modified Glasgow prognostic score in patients with resectable non-small cell lung cancer. J Can Res Ther [serial online] 2016 [cited 2019 Oct 20];12:945-51. Available from: http://www.cancerjournal.net/text.asp?2016/12/2/945/176168




 > Introduction Top


The Glasgow prognostic score (GPS) is a useful prognostic score focusing on inflammation and nutrition status in patients with cancer.[1] More recently, the modified GPS (mGPS)[2] and the high-sensitivity mGPS (HS-mGPS)[3] were established as more sensitive prognostic markers. The HS-mGPS has been reported to have better prognostic value than the mGPS in patients with resectable gastric cancer.[4] However, few studies have evaluated the prognostic value of the HS-mGPS in resectable non-small cell lung cancer (NSCLC) patients. Thus, the prognostic value of the HS-mGPS was evaluated and compared with that of the other inflammation-based prognostic markers in patients with resectable NSCLC, including the GPS, mGPS, neutrophil/lymphocyte ratio (NLR), platelet/lymphocyte ratio (PLR), prognostic index (PI), and prognostic nutritional index (PNI).


 > Materials and Methods Top


Selection and description of participants

The participants were a series of 327 consecutive patients who underwent surgical resection for NSCLC at our institution from January 2005 to December 2009 and were followed for >5 years. Patients who did not undergo complete resection and received neoadjuvant treatment prior to surgery were excluded. The 327 patients included 128 women and 199 men with a median age of 69 years (range, 43–87 years); 232 (70.9%) had stage I disease, 49 (15.0%) had stage II, and 46 (14.1%) had stage III. The median observation period was 65.0 months (range, 0–116 months), and the 5-year survival rate was 80.1%. Full patient characteristics are listed in [Table 1]. Data were collected from clinical and pathological records. Tumor types and stages were determined according to the 7th ed.ition of the Union for International Cancer Control tumor-node-metastasis classification.
Table 1: Patients' characteristics

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Only data for those patients who had provided a blood sample within 1 month before surgery were included. The GPS, mGPS, HS-mGPS, NLR, PLR, PI, and PNI were constructed as described in [Table 2]. The NLR and PLR were derived by dividing the neutrophil and platelet count, respectively, with the lymphocyte count. An NLR >5.0 was defined as an elevated NLR, whereas a PLR >300 was defined as an elevated PLR in accordance with a previous study.[5] The GPS, mGPS, and HS-mGPS were combined with the C-reactive protein (CRP) and albumin concentrations. The CRP cut-off value for evaluation of the GPS and mGPS was set at 1.0 mg/dL while that for evaluation of the HS-mGPS was set at 0.3 mg/dL.[2],[3] The albumin cut-off value for both together was set at 3.5 mg/dL. Patients with an elevated CRP level and low albumin level were allocated a score of 2. In terms of the GPS, patients with abnormalities in either were given a score of 1, and those with no abnormal values were given a score of 0. Regarding the mGPS and HS-mGPS, patients with only an abnormal CRP level were given a score of 1, and those without an abnormal CRP level regardless of whether the albumin level was normal or abnormal were given a score of 0. The PI combines the CRP level and white blood cell count. Both an elevated CRP level (>1.0 mg/dL) and an elevated white blood cell count (>11,000/µL) were defined as an elevated PI.[6] The PNI was calculated as albumin (g/dL) + 5 × total lymphocyte count × 109·L −1. Patients with a PNI ≥45 were assigned a score of 0. Patients with a PNI <45 were assigned a score of 1.[7] Ethical approval for data analysis and access to patient information was obtained from the Ethics Committee of Fukushima Medical University Hospital. This study was conducted in accordance with the principles of the Declaration of Helsinki.
Table 2: Assessment of systemic inflammation-based prognostic scores

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Statistical analysis

Correlations of the GPS, mGPS, and HS-mGPS with the patients' clinical characteristics were assessed using the two-tailed Chi-squared test or Fisher's exact test. Cancer-specific overall survival (hereafter termed overall survival) was defined as the time from surgery to the last follow-up or the time of NSCLC-specific death. Overall survival was taken as the main outcome. Univariate and multivariate analyses were performed using a Cox proportional hazards model. Survival curves according to the GPS, mGPS, and HS-mGPS were assessed using the Kaplan–Meier method and compared with the log-rank test. All statistical analyses were performed using SPSS 21 software (SPSS Inc., Chicago, IL, USA), and P < 0.05 were considered significant.


 > Results Top


Associations of GPS, mGPS, and HS-mGPS with clinical characteristics of patients with resectable NSCLC:

Of the 327 patients, 286 (87.5%) had a GPS of 0, 30 (9.2%) had a GPS of 1, and 11 (3.4%) had a GPS of 2; 301 (92.0%) had an mGPS of 0, 15 (4.6%) had an mGPS of 1, and 11 (3.4%) had an mGPS of 2; and 255 (78.0%) had an HS-mGPS of 0, 53 (16.2%) had an HS-mGPS of 1, and 19 (5.8%) had an HS-mGPS of 2. Associations of the GPS, mGPS, and HS-mGPS with the patients' clinical features are shown in [Table 3]. The high GPS and HS-mGPS categories tended to include males (P = 0.003, P < 0.001) and individuals with a smoking history (P = 0.002, P < 0.001, respectively). In addition, high GPS, mGPS, and HS-mGPS scores were significantly correlated with non-Ad (P < 0.001, P < 0.001, P < 0.001, respectively), p-T2-4 (P < 0.001, P < 0.001, P < 0.001, respectively), lymph node metastasis (P = 0.004, P = 0.028, P = 0.014, respectively), advanced pathological stage (P < 0.001, P < 0.001, P < 0.001, respectively), and blood vessel invasion (P = 0.003, P = 0.003, P < 0.001, respectively). The HS-mGPS was associated with the most number of clinical characteristics, compared with the GPS and mGPS.
Table 3: Associations of clinical characteristics with Glasgow prognostic score, modified Glasgow prognostic score, and high-sensitivity modified Glasgow prognostic score

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Prognostic impact of GPS, mGPS, and HS-mGPS in patients with NSCLC by Kaplan-Meier survival analysis:

Kaplan-Meier survival analysis was performed to evaluate the differences in prognostic impact among GPS, mGPS, and HS-mGPS [Figure 1]. Increases in GPS (0 vs. 1, P < 0.001; 0 vs. 2, P < 0.001; and 1 vs. 2, P = 0.177) and mGPS (0 vs. 1, P = 0.032; 0 vs. 2, P < 0.001; and 1 vs. 2, P = 0.077) were correlated with overall survival [Figure 1]a and [Figure 1]b. In the same way, an elevated HS-mGPS (0 vs. 1, P = 0.015; 0 vs. 2, P < 0.001; and 1 vs. 2, P = 0.002) was associated with reduced overall survival [Figure 1]c. Further studies of overall survival were performed using multivariate analyses to confirm that the prognostic impact of the HS-mGPS was superior to that of the GPS and mGPS. On Cox multivariate analysis, the HS-mGPS showed a stronger prognostic impact than the GPS and mGPS (P < 0.001, hazard ratio [HR] = 5.774) [Table 4].
Figure 1: Kaplan–Meier survival curves for patients with nonsmall cell lung cancer. Overall survival stratified according to the (a) Glasgow prognostic score, (b) modified Glasgow prognostic score, and (c) high-sensitivity modified Glasgow prognostic score. HR: Hazard ratio

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Table 4: Overall survival in relation to Glasgow prognostic score and modified Glasgow prognostic score versus high-sensitivity modified Glasgow prognostic score analyzed by Cox-proportional regression

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Prognostic impact of the HS-mGPS among systemic inflammatory response markers in patients with resectable NSCLC:

The prognostic significance of the HS-mGPS among the various parameters reflecting cancer progression and systemic inflammatory markers including the NLR, PLR, PI, and PNI was also analyzed. Cox univariate analyses showed that age, p-T status, p-N status, blood vessel invasion, lymphatic vessel invasion, NLR, PI, PNI, and HS-mGPS were correlated with overall survival (P = 0.006, P < 0.001, P < 0.001, P < 0.001, P < 0.001, P = 0.018, P = 0.006, P < 0.001, and P < 0.001, respectively), whereas sex, pack-years, histological findings, and PLR were not correlated with overall survival [Table 4]. Furthermore, Cox multivariate analysis showed that age, p-T status, p-N status, lymphatic vessel invasion, and HS-mGPS were independent prognostic factors for overall survival (P = 0.026, P < 0.001, P < 0.001, P = 0.008, and P = 0.016, respectively) [Table 5].
Table 5: Overall survival of patients with nonsmall cell lung cancer in relation to clinical characteristics and systemic inflammation-based prognostic scoares analyzed by Cox proportional regression

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 > Discussion Top


Inflammation is a hallmark of cancer and plays important roles in carcinogenesis and tumor progression.[8] In particular, there has been great discussion regarding whether CRP, a sensitive marker of inflammatory status, may serve as a potential prognostic marker in various common cancers.[9] CRP has been combined with other systemic inflammatory response markers to enhance its role as a prognostic indicator. The best representative score among the CRP-based prognostic scores is GPS. GPS is calculated from the serum concentrations of CRP (cut-off value, 1.0 mg/dL) and albumin (cut-off value, 3.5 mg/dL) and was initially reported by Forrest et al.[10],[11] The GPS was subsequently revised by McMillan et al.[2] to form the mGPS. Proctor et al.[3] recently suggested that the additional use of a high-sensitivity CRP measurement (cut-off value, 0.3 mg/dL), which they termed the HS-mGPS, enhanced the prognostic impact of mGPS. Recently, HS-mGPS has been reported to have better prognostic value than mGPS in patients with resectable gastric cancer.[4] However, a similar study has not yet been reported for patients with resectable NSCLC. The present study is the first to investigate the prognostic value of the HS-mGPS in patients with resectable NSCLC. A multivariate analysis to determine whether the preoperative HS-mGPS might serve as a superior prognostic factor for patients with resectable NSCLC was also performed.

Recently, there has been a great discussion about the prognostic values of multiple inflammation-based factors in patients with various types of cancer.[12],[13],[14],[15] Two comparative studies examined multiple inflammation-based scores in patients with resectable NSCLC.[5],[16] The NLR was found to be superior to the mGPS and PLR as a prognostic marker in patients with resectable NSCLC, whereas the GPS was superior to the NLR and PLR. This discrepancy might have originated from the heterogeneity among the patients enrolled in each study; the former study included patients with stages I–III cancer, whereas the latter study included older patients with clinical stage I NSCLC. Thus, it remains controversial whether GPS/mGPS has better prognostic value than the NLR in patients with operable NSCLC. It can be said that both the NLR and GPS are good prognostic markers in patients with resectable NSCLC, because several studies have proven that the NLR and GPS have clinical impact as prognostic markers.[5],[16],[17],[18],[19],[20],[21],[22],[23] However, they are also considered to have disadvantages. First, the optimal threshold of the NLR remains controversial, because the prognostic values of different thresholds have been examined. In fact, the discriminatory value of the NLR varies from 1.9 to 5.0 in patients with resectable NSCLC.[5], 16, [19],[20],[21],[22],[23] Conversely, the GPS scoring system, including the HS-mGPS, had an advantage over the NLR in that it is categorized using only 3 points (0, 1, and 2). Second, Tomita et al.[17] reported that the number of patients with operable NSCLC with a high GPS was very small. The present data also support the same weak point of the GPS. The percentage of patients with GPS 1 and 2 in this study was less than in previous studies of operable NSCLC patients.[5],[16],[17] However, the rate of patients with a high GPS in a recent study was nearly identical to that of the present data.[24] The number of younger patients with stage I in the present study was larger than in the previous studies.[5],[16],[17] Therefore, the present study might have targeted patients with less systemic inflammation and better nutritional status than previous studies.[5],[16],[17] Meanwhile, the rate of patients with a high HS-mGPS increased from 12.6% to 22.0% in comparison with the rate of patients with a high GPS. Although there was no significant difference in survival between patients with a GPS of 1 and 2 (GPS 1 vs. 2; P = 0.177, HR = 1.825), an increase in high HS-mGPS resulted in a significant difference in survival between the HS-mGPS of 1 and 2 (HS-mGPS 1 vs. 2; P = 0.002 HR = 9.915) on Kaplan–Meier survival analysis [Figure 1]. Thus, it might be said that the HS-mGPS can compensate for the drawbacks of the NLR and GPS.

The present study confirmed for the 1st time that the HS-mGPS is a useful prognostic marker that is superior to both the GPS and mGPS in patients with resectable NSCLC. The CRP cut-off values of the GPS and mGPS have been defined as the standard threshold (1.0 mg/dL), whereas the threshold for CRP of the HS-mGPS has been defined as high-sensitivity CRP (0.3 mg/dL).[3],[10],[11] Proctor et al.[3] confirmed that the HS-mGPS could enhance the prognostic values of the GPS and mGPS. Furthermore, several studies have claimed that a high-sensitivity threshold for CRP (0.3 and 0.5 mg/dL) had superior prognostic value than the standard threshold (1.0 mg/dL).[3],[25] The present multivariate Cox analysis results are consistent with the findings of these previous studies. Furthermore, Takeno et al.[4] recently provided evidence that the preoperative HS-mGPS is a better prognostic indicator than the mGPS in patients with operable gastric cancer. In fact, a CRP threshold of >1.0 mg/dL has often been used in patients with advanced NSCLC, whereas the CRP cut-off value in patients with operable NSCLC has mostly been based on the high-sensitivity CRP level.[21],[26],[27],[28],[29],[30] Accordingly, there is a possibility that HS-mGPS is a more suitable prognostic marker for patients with operable NSCLC than GPS and mGPS.

The prognostic values of PLR, PI, and PNI were also evaluated in the present study. First, a recent meta-analysis showed that an elevated PLR was a negative predictor of survival in patients with various cancers, including NSCLC.[31] However, all patients enrolled in this previous study had advanced NSCLC. Moreover, although some univariate analyses supported the prognostic significance of the PLR in patients with operable NSCLC, the PLR was not associated with patient survival on multivariate analyses.[22] In the present study, the PLR was not correlated with patient survival on both univariate and multivariate analyses. Second, there were associations of the PI and PNI with survival in patients with operable NSCLC in the present univariate analysis. To the best of our knowledge, the present study is the first to validate the PI and PNI as prognostic markers in patients with resectable NSCLC. However, the prognostic values of the PI and PNI remain inconclusive, because few studies have attempted to evaluate them in patients with resectable NSCLC.

The present study showed that the HS-mGPS, among multiple inflammation-based indices, is an independent prognostic factor in patients with resectable NSCLC. The HS-mGPS is an objective, reproducible, and inexpensive indicator of survival in patients with resectable NSCLC. In the future, measurement of the HS-mGPS should be included in the routine assessment of all patients with resectable NSCLC.

However, the present study had several limitations. First, this study was preliminary and retrospective, and data were obtained from only a single institution. Therefore, the present results warrant further investigation and require independent validation. A large-scale prospective validation study is needed to confirm the results. Second, the role of NLR and PLR as prognostic factors might not have been clarified because their optimal cut-off values were not defined. Consequently, further studies are needed to determine the optimal thresholds of the NLR and PLR as prognostic markers in patients with resectable NSCLC.


 > Conclusion Top


To the best of our knowledge, this study is the first to verify the prognostic value of the HS-mGPS in patients with resectable NSCLC. The present results provide evidence that the preoperative HS-mGPS might be a superior prognostic factor for patients with resectable NSCLC, as well as those with operable gastric cancer.[3] Consequently, the HS-mGPS might also be a good prognostic indicator in patients with other malignancies. Furthermore, the preoperative GPS was reportedly a useful prognostic indicator in older patients with clinical stage I NSCLC.[16] We intend to investigate the prognostic value of the HS-mGPS for older patients with resectable NSCLC in a future study.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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