Research ArticleClinical Studies

Significance of Glasgow Prognostic Scores in NSCLC Patients Treated With Immunotherapy After Platinum-based Cytotoxic Chemotherapy

HYE SEON KANG, AH YOUNG SHIN, CHANG DONG YEO, SUNG KYOUNG KIM, CHAN KWON PARK, JU SANG KIM, SEUNG JOON KIM, SANG HAAK LEE and JIN WOO KIM
In Vivo November 2021, 35 (6) 3423-3430; DOI: https://doi.org/10.21873/invivo.12642

Abstract

Background/Aim: Little is known about the prognostic role of the Glasgow prognostic score (GPS) in non-small cell lung cancer (NSCLC) patients treated with immunotherapy after platinum-based cytotoxic chemotherapy. Patients and Methods: This study used a lung cancer cohort of the Catholic Medical Center of Korea between January 2018 and September 2020. Results: A total of 78 patients with NSCLC treated with immunotherapy as second or further-line therapy were included. Higher GPS values were significant predictors of shorter immune-related progression-free survival (irPFS) and overall survival (OS). The hazard ratios for irPFS were 0.249 for programmed death-ligand 1 (PD-L1) expression ≥50% and 9.73 for a GPS of 2. Older age, lower PD-L1 expression and higher GPS values were independently associated with shorter OS. Conclusion: Higher GPS values were identified as a poor prognostic factor for OS and irPFS in NSCLC patients who received immunotherapy as second or further-line therapy.

The introduction of immune-checkpoint inhibitors (ICIs) into the therapy for non-small cell lung cancer (NSCLC) has transformed the therapeutic landscape of metastatic NSCLC (1). The expression of programmed death-ligand 1 (PD-L1) on tumor cells and tumor mutation burden (TMB) have been used to select patients suitable for ICIs but not all patients with these predictive factors benefit from ICIs (2). However, the proper predictive factors for using ICIs to treat NSCLC patients have not been developed.

Inflammation is an important factor in tumor progression and is associated with poor response to treatment. The response to cancer treatment depends not only on the tumor’s characteristics and tumor stage but also on patient-related factors including nutrition and inflammation status (3). Recently, systemic inflammatory response to predict progression and survival has been reported in patients with malignancies. Thus, cancer-related prognosis has been validated using inflammatory markers such as the neutrophil-lymphocyte ratio (NLR) or the lung immune prognostic index consisting of the NLR and lactate dehydrogenase (LDH) levels, and the systemic inflammation response index (2, 4).

The Glasgow prognostic score (GPS), reflecting the host systemic inflammatory response and immune status has been validated as a prognostic factor in many malignancies. The GPS is the combination of the C-reactive protein (CRP) concentration (>10 mg/l) and hypoalbuminemia (<35 g/l) (5, 6). The association of the GPS and ICIs in lung cancer patients has been explored previously; however, previous studies have had small sample sizes or evaluated the post-treatment GPS in lung cancer patients treated with ICIs.

Few studies have evaluated the prognostic value of the GPS in metastatic NSCLC patients treated with ICIs who received at least one regimen of cytotoxic chemotherapy before the administration of ICIs (7, 8). Recently Takamori et al. reported the clinical utility of pre-treatment GPS in advanced or recurrent NSCLC patients treated with ICIs but included patients treated with ICIs as first line treatment.(9) In this study, we retrospectively analyzed the survival and immune-related progression-free survival (irPFS) data of patients with metastatic NSCLC and explored the prognostic role of the GPS in these patients.

Patients and Methods

Patients. We used the lung cancer registry database of the Catholic Medical Center, Seoul, Republic of Korea. Since October 2014, seven hospitals of the Catholic University of Korea (Seoul St. Mary’s Hospital, Yeouido St. Mary’s Hospital, Eunpyeong St. Mary’s Hospital, Uijeongbu St. Mary’s Hospital, Bucheon St. Mary’s Hospital, Incheon St. Mary’s Hospital and St. Vincent’s Hospital) have consecutively enrolled lung cancer patients. Clinical information including stage, pathology, treatment modality and survival was systematically recorded by qualified managers to improve data accuracy. The researchers were permitted access by newly assigned serial numbers and anonymizing the dataset.

Patients were eligible for the study if they were diagnosed from January 2018 to March 2020 with histologically confirmed NSCLC and received ICIs as second-line or further-line therapy after treatment failure with platinum-based cytotoxic chemotherapy. Patients who received ICIs as first-line therapy, were diagnosed with small cell lung cancer, received post-chemoradiation consolidation treatment with durvalumab, were lost to follow up, or had no pre-treatment CRP and albumin levels were excluded. The study flow is summarized in Figure 1. The follow-up period ended on September 30, 2020.

Figure 1.
Figure 1.

Study flow diagram. ICI, Immune-checkpoint inhibitors; SCLC, small cell lung cancer; CRP, C-reactive protein; NSCLC, non-small cell lung cancer; GPS, Glasgow prognostic score.

This study was approved by the Clinical Research Ethics Committee of the Catholic Medical Center (approval number: XC20RIDI0192). All methods were performed in accordance with the Declaration of Helsinki, participants were informed about the study, the handling of personal data and how confidentiality would be maintained in the management of material and in publishing and presenting results. Researchers were permitted to conduct this study by accessing dataset newly assigned with a serial number whose personal information was removed after ethical approval. We included only patients over 19 years old and written informed consent was obtained from all patients prior to registry enrollment.

Data. We extracted the following data from the patient medical records: patient demographics, smoking history, stage of lung cancer, Eastern Cooperative Oncology Group performance status, laboratory data, history of chemotherapy and/or radiation, survival status, and the dates of disease progression and death. Blood samples drawn within one week prior to ICI treatment were used to compile a pretreatment GPS for each patient using the laboratory values. The patients were classified into three groups based on GPS values as follows: (I) GPS of 2, elevated CRP level (>1.0 mg/dl) and hypoalbuminemia (<3.5 g/dl); (II) GPS of 1, elevated CRP level or hypoalbuminemia; and (III) GPS of 0, neither elevated CRP level nor hypoalbuminemia (5, 10). The serum CRP levels were measured using immunoturbidimetric assays (CRPL3, Roche Diagnostics, Indianapolis, IN, USA).

Statistical analysis. The patient baseline demographics and clinical outcomes were compared according to the GPS. We used Pearson’s chi-squared test to compare the discrete variables and the Student’s t-test or analysis of variance to compare the continuous variables. Kaplan-Meier survival analysis was used to compare OS and irPFS according to GPS. Differences in survival and irPFS were determined by the log-rank test. The Mann-Whitney test was used to compare the median values. Hazard ratios (HRs) and the corresponding 95% confidence intervals (CIs) were calculated for the predictors that were significant in multivariate Cox regression analysis. A two-sided p-value of <0.05 was considered statistically significant. All statistical analyses were performed using SPSS for Windows software (ver. 20.0; IBM Corp., Armonk, NY, USA) (11).

Results

Patient characteristics. Overall, 122 NSCLC patients treated with ICIs were enrolled, of whom 44 met the exclusion criteria (treatment with ICIs as first-line therapy, small cell lung cancer treated with ICIs, treatment with durvalumab, and patients lost to follow-up, or those who had no pre-treatment CRP/albumin levels). Thus, 78 patients were finally included in our analysis (Figure 1). The mean age of the included subjects was 67.1±9.17 years (range=38.0-84.0 years). There were 64 (82.1%) males. Of all the included patients, 19 (24.4%), 35 (44.9%), and 24 (30.8%) were classified into the GPS 0, GPS 1, and GPS 2 groups, respectively. We compared these three groups and explored the clinical factors predicting treatment outcomes including OS and irPFS. The total and median follow-up times were 12.7, 14.2, 15.0, and 6.4 person-months, respectively.

The baseline characteristics of these three groups are summarized in Table I. The mean age and smoking history were not different between the three groups. The proportion of poor performance status, histologic type, treatment line of ICIs, driving mutations, and PD-L1 expression were similar between the three groups. However, the GPS 0 group tended to receive atezolizumab and the GPS 2 group tended to receive pembrolizumab as ICIs (p=0.042).

View this table:
Table I.

Baseline characteristics of NSCLC patients treated with immunotherapy according to GPS values.

Prognostic analysis. The GPS 2 group displayed a shorter median irPFS than the GPS 0 or GPS 1 group [23.0 (95% CI=12.43-33.57) days vs. 89.0 (95% CI=57.6-120.4) days vs. 107.0 (95% CI=41.92-172.1) days respectively, p<0.001]. Also, the GPS 2 group showed significantly shorter median OS than the GPS 0 or GPS 1 group [412.9 (95% CI=278.5-547.27) days vs. 593.7 (95% CI=504.3-683.2) days in GPS 0 and 768.5 (95% CI=655.7-881.2) days in GPS 1, p<0.001] (Figure 2).

Figure 2.
Figure 2.

Clinical outcomes according to Glasgow prognostic score (GPS) in non-small cell lung cancer (NSCLC) patients treated with immunotherapy after platinum-based cytotoxic chemotherapy.

In the multivariate analysis of irPFS, the HR was 0.249 (95% CI=0.084-0.739, p=0.012) for PD-L1 expression ≥50% and 9.73 (95% CI=2.931-32.298, p<0.001) for GPS 2 (Table II). In multivariate analysis for OS, the HR was 0.189 for PD-L1 expression between 1 and 10%, 0.297 for PD-L1 expression ≥50%, 4.247 in the GPS 1 group, and 9.710 in the GPS 2 group (Table III).

View this table:
Table II.

Univariate and multivariate analysis for predicting progression-free survival in NSCLC patients treated with immunotherapy after platinum-based cytotoxic chemotherapy.

View this table:
Table III.

Univariate and multivariate analysis for predicting overall survival in NSCLC patients treated with immunotherapy after platinum-based cytotoxic chemotherapy.

Discussion

In the present study, we compared the clinical outcomes of NSCLC patients treated with ICIs as second-line or further-line therapy after treatment failure with platinum-based cytotoxic chemotherapy according to the GPS values and explored the prognostic role of GPS values for treatment outcomes. We found that the baseline characteristics were not different according to GPS. Patients with higher GPS values displayed shorter median irPFS and OS than those in the GPS 0 or GPS 1 groups. In multivariate analysis, lower PD-L1 expression and higher GPS was associated with shorter irPFS and OS.

Chronic inflammation is known to be associated with tumor development through the induction of oncogenic mutations, genomic instability, early tumor promotion, and enhanced angiogenesis (12). During inflammation, reactive oxygen and nitrogen species are created to combat pathogens, but also damage DNA, which in turn promote mutations that initiate cancer (13, 14). Inflammatory responses may act together with oncogenes by driving cells to undergo high levels of transcriptional activity that leads to genome instability (15). Tumorigenesis can be enhanced through increased genomic instability (16). Various cancers induce an inflammatory microenvironment (17). Nutrition is a critical component of immune responses (18). In lung cancer, systemic inflammation, malnutrition, and tumor immune microenvironments are associated with each other, and these are key determinants of tumor progression and treatment response (3). Elevated levels of circulating CRP could be a marker of the increased predisposition to malignancy due to chronic inflammation, a marker of occult cancer leading to inflammation, or both (17).

In the era of immunotherapy in cancer treatment, proper predictive factors of NSCLC patients for immunotherapy have not been developed. The expression of PD-L1 on tumor cells and the TMB have been used in qualifying patients to receive immunotherapy, but not all patients with these predictive factors benefit from immunotherapy (2). Patients with high TMB who received nivolumab and ipilimumab did not show significant survival benefit compared to those who received chemotherapy (19). The presence of immune cells in the anti-tumor immune response such as cluster of differentiation (CD) 8-positive cytotoxic T lymphocytes as well as CD4-positive memory and regulatory T lymphocytes has been postulated to be a prognostic marker of the disease course and predictors of activity or modulation of immune system function (20). For simpler prognostic markers, systemic inflammatory marker such as lung immune prognostic index are suggested as biomarker for ICIs in lung cancer. Poor combination of lung immune prognostic index and derived NLR or LDH value are associated with poorer outcomes in patients treated with ICIs (21).

Several studies have demonstrated that systemic inflammatory biomarkers in peripheral blood were predictive markers for treatment outcomes in different solid tumors including prostate, colorectal, and esophageal cancer, melanoma, and NSCLC (22-26). Although the exact biological basis for these findings has not been thoroughly elucidated, inflammatory cells such as neutrophils play a significant role in tumor development and progression via effects on tumor cells or other components of the tumor microenvironment, by secreting chemokines and cytokines such as transforming growth factor-β, interleukin-6 (IL-6) and matrix metalloproteinases (27, 28). CRP is a surrogate marker of IL-6, which is involved in the activation of immune cells, tumor migration and invasion and epithelial-to-mesenchymal transition (29, 30).

Cancer prognosis is associated with not only tumor staging but also patient-related factors such as nutritional and functional decline. CRP represents systemic inflammation, and albumin reflects both systemic inflammation and the amount of lean tissue (31, 32). GPS is a reliable independent prognostic factor in patients with various malignancies and also a marker for predicting prognosis, even in surgery, chemoradiation, and various subgroups incapable of surgery (5, 6). In 15 studies including >2,000 patients, GPS was associated with increased weight loss, poor performance status, increased comorbidity, increased proinflammatory and angiogenic cytokines, and complications from cancer treatments (5). In resectable lung cancer, the pre- and post-operative GS predicts adverse survival outcomes in patients with resected stage I NSCLC (33, 34).

Few previous studies have been conducted on the association between GPS and clinical outcomes in lung cancer patients treated with ICIs. Taichi et al. reported that modified GPS values checked before treatment were associated with shorter OS in NSCLC patients treated with atezolizumab (8). In another study, post-treatment GPS predicted anti-programmed cell death protein 1 (PD1) treatment (nivolumab or pembrolizumab) efficacy in NSCLC patients (7). Recently, Takamori et al. reported that pretreatment GPS were associated with shorter OS and PFS in NSCLC patients treated with ICIs as first line or higher (9). These studies included populations from single institutions and reported the results of groups treated with anti-PD1 or anti-PD-L1 antibody, or those treated with ICIs as first line therapy. Our study had a moderate sample size and analyzed the prognostic role of pre-treatment GPS values in all of the NSCLC patients treated with anti-PD1 or anti-PD-L1 antibodies after failure of platinum-based cytotoxic chemotherapy.

Limitations. This study had some limitations. Firstly, it was a retrospective study. Nonetheless, our study was based on a lung cancer cohort with a moderate sample size using medical records that were faithfully collected from the time of enrollment, and the data were rechecked by authorized data managers. Therefore, data including the baseline characteristics and clinical outcomes were of high quality and reliable. Also, we enrolled lung cancer patients from seven teaching hospitals in the Republic of Korea, so our data represent the Korean general population to some extent. Secondly, since our analyzed results were based on clinical parameters, we could not exactly elucidate the mechanisms of GPS on NSCLC patients treated with immunotherapy. However, hematologic biomarkers are promising predictors of the response to ICIs due to their convenience and accessibility in clinical practice.

Conclusion

Patients with higher GPS values before treatment showed shorter median irPFS and OS in NSCLC patients treated with ICIs as a second-line or further-line therapy. The pre-treatment serum GPS, along with PD-L1 expression, is a promising value to identify NSCLC patients who could benefit more from ICIs as a second-line or further-line therapy after treatment failure with platinum-based cytotoxic chemotherapy. Further large-scale studies are warranted to validate its clinical value.

Acknowledgements

The Authors would like to acknowledge and thank Bora Kwon, data manager for help with data collection and management of lung cancer registry.

Footnotes

  • This article is freely accessible online.

  • Author’s Contributions

    HSK: conception, design, definition of intellectual content, data analysis, statistical analysis, manuscript preparation and manuscript review; CDY: conception, design, definition of intellectual content, data analysis and manuscript review; SHL: conception, design, definition of intellectual content, data analysis and manuscript review; JWK: conception, design, definition of intellectual content, data analysis, manuscript preparation and manuscript review; AYS: literature search, clinical studies, data acquisition and manuscript review; SKK: literature search, clinical studies, data acquisition, manuscript preparation and manuscript review; CKP: literature search, clinical studies, data acquisition and manuscript review; JSK: literature search, clinical studies, data acquisition and manuscript review; SJK: literature search, clinical studies, data acquisition, manuscript preparation and manuscript review.

  • Conflicts of Interest

    All Authors have completed the ICMJE uniform disclosure form. The Authors have declared that no competing interests exist.

  • Received July 29, 2021.
  • Revision received September 23, 2021.
  • Accepted September 27, 2021.

References

  1. ↵
    1. Doroshow DB,
    2. Sanmamed MF,
    3. Hastings K,
    4. Politi K,
    5. Rimm DL,
    6. Chen L,
    7. Melero I,
    8. Schalper KA and
    9. Herbst RS
    : Immunotherapy in non-small cell lung cancer: facts and hopes. Clin Cancer Res 25(15): 4592-4602, 2019. PMID: 30824587. DOI: 10.1158/1078-0432.CCR-18-1538
    OpenUrlAbstract/FREE Full Text
  2. ↵
    1. Wojas-Krawczyk K,
    2. Kalinka E,
    3. Grenda A,
    4. Krawczyk P and
    5. Milanowski J
    : Beyond PD-L1 markers for lung cancer immunotherapy. Int J Mol Sci 20(8): 1915, 2019. PMID: 31003463. DOI: 10.3390/ijms20081915
    OpenUrlCrossRefPubMed
  3. ↵
    1. Alifano M,
    2. Mansuet-Lupo A,
    3. Lococo F,
    4. Roche N,
    5. Bobbio A,
    6. Canny E,
    7. Schussler O,
    8. Dermine H,
    9. Régnard JF,
    10. Burroni B,
    11. Goc J,
    12. Biton J,
    13. Ouakrim H,
    14. Cremer I,
    15. Dieu-Nosjean MC and
    16. Damotte D
    : Systemic inflammation, nutritional status and tumor immune microenvironment determine outcome of resected non-small cell lung cancer. PLoS One 9(9): e106914, 2014. PMID: 25238252. DOI: 10.1371/journal.pone.0106914
    OpenUrlCrossRefPubMed
  4. ↵
    1. Hu M,
    2. Xu Q,
    3. Yang S,
    4. Han S,
    5. Zhu Y,
    6. Lin Q,
    7. Sun X,
    8. Liu H and
    9. Xu Y
    : Pretreatment systemic inflammation response index (SIRI) is an independent predictor of survival in unresectable stage III non-small cell lung cancer treated with chemoradiotherapy: a two-center retrospective study. Ann Transl Med 8(20): 1310, 2020. PMID: 33209890. DOI: 10.21037/atm-20-6484
    OpenUrlCrossRefPubMed
  5. ↵
    1. McMillan DC
    : The systemic inflammation-based Glasgow Prognostic Score: a decade of experience in patients with cancer. Cancer Treat Rev 39(5): 534-540, 2013. PMID: 22995477. DOI: 10.1016/j.ctrv.2012.08.003
    OpenUrlCrossRefPubMed
  6. ↵
    1. Simmons CPL,
    2. McMillan DC,
    3. McWilliams K,
    4. Sande TA,
    5. Fearon KC,
    6. Tuck S,
    7. Fallon MT and
    8. Laird BJ
    : Prognostic tools in patients with advanced cancer: a systematic review. J Pain Symptom Manage 53(5): 962-970.e10, 2017. PMID: 28062344. DOI: 10.1016/j.jpainsymman.2016.12.330
    OpenUrlCrossRefPubMed
  7. ↵
    1. Kasahara N,
    2. Sunaga N,
    3. Tsukagoshi Y,
    4. Miura Y,
    5. Sakurai R,
    6. Kitahara S,
    7. Yokobori T,
    8. Kaira K,
    9. Mogi A,
    10. Maeno T,
    11. Asao T and
    12. Hisada T
    : Post-treatment Glasgow Prognostic Score predicts efficacy in advanced non-small-cell lung cancer treated with anti-PD1. Anticancer Res 39(3): 1455-1461, 2019. PMID: 30842182. DOI: 10.21873/anticanres.13262
    OpenUrlAbstract/FREE Full Text
  8. ↵
    1. Matsubara T,
    2. Takamori S,
    3. Haratake N,
    4. Toyozawa R,
    5. Miura N,
    6. Shimokawa M,
    7. Yamaguchi M,
    8. Seto T and
    9. Takenoyama M
    : The impact of immune-inflammation-nutritional parameters on the prognosis of non-small cell lung cancer patients treated with atezolizumab. J Thorac Dis 12(4): 1520-1528, 2020. PMID: 32395289. DOI: 10.21037/jtd.2020.02.27
    OpenUrlCrossRefPubMed
  9. ↵
    1. Takamori S,
    2. Takada K,
    3. Shimokawa M,
    4. Matsubara T,
    5. Fujishita T,
    6. Ito K,
    7. Toyozawa R,
    8. Yamaguchi M,
    9. Okamoto T,
    10. Yoneshima Y,
    11. Tanaka K,
    12. Okamoto I,
    13. Tagawa T and
    14. Mori M
    : Clinical utility of pretreatment Glasgow prognostic score in non-small-cell lung cancer patients treated with immune checkpoint inhibitors. Lung Cancer 152: 27-33, 2021. PMID: 33341085. DOI: 10.1016/j.lungcan.2020.11.026
    OpenUrlCrossRefPubMed
  10. ↵
    1. McMillan DC,
    2. Crozier JE,
    3. Canna K,
    4. Angerson WJ and
    5. McArdle CS
    : Evaluation of an inflammation-based prognostic score (GPS) in patients undergoing resection for colon and rectal cancer. Int J Colorectal Dis 22(8): 881-886, 2007. PMID: 17245566. DOI: 10.1007/s00384-006-0259-6
    OpenUrlCrossRefPubMed
  11. ↵
    1. Kang HS,
    2. Lee HY,
    3. Jung JI,
    4. Kim JS,
    5. Kim YH,
    6. Kim SJ,
    7. Kim SC,
    8. Kwon SS,
    9. Kim YK and
    10. Kang JY
    : Clinical significance of Glasgow Prognostic Score in patients with tuberculous pleurisy. J Thorac Dis 10(11): 6077-6087, 2018. PMID: 30622779. DOI: 10.21037/jtd.2018.10.02
    OpenUrlCrossRefPubMed
  12. ↵
    1. Arbour KC and
    2. Riely GJ
    : Systemic therapy for locally advanced and metastatic non-small cell lung cancer: a review. JAMA 322(8): 764-774, 2019. PMID: 31454018. DOI: 10.1001/jama.2019.11058
    OpenUrlCrossRefPubMed
  13. ↵
    1. Kay J,
    2. Thadhani E,
    3. Samson L and
    4. Engelward B
    : Inflammation-induced DNA damage, mutations and cancer. DNA Repair (Amst) 83: 102673, 2019. PMID: 31387777. DOI: 10.1016/j.dnarep.2019.102673
    OpenUrlCrossRefPubMed
  14. ↵
    1. Lin R,
    2. Zhang C,
    3. Zheng J,
    4. Tian D,
    5. Lei Z,
    6. Chen D,
    7. Xu Z and
    8. Su M
    : Chronic inflammation-associated genomic instability paves the way for human esophageal carcinogenesis. Oncotarget 7(17): 24564-24571, 2016. PMID: 27028857. DOI: 10.18632/oncotarget.8356
    OpenUrlCrossRefPubMed
  15. ↵
    1. Tubbs A and
    2. Nussenzweig A
    : Endogenous DNA damage as a source of genomic instability in cancer. Cell 168(4): 644-656, 2017. PMID: 28187286. DOI: 10.1016/j.cell.2017.01.002
    OpenUrlCrossRefPubMed
  16. ↵
    1. Champeris Tsaniras S,
    2. Villiou M,
    3. Giannou AD,
    4. Nikou S,
    5. Petropoulos M,
    6. Pateras IS,
    7. Tserou P,
    8. Karousi F,
    9. Lalioti ME,
    10. Gorgoulis VG,
    11. Patmanidi AL,
    12. Stathopoulos GT,
    13. Bravou V,
    14. Lygerou Z and
    15. Taraviras S
    : Geminin ablation in vivo enhances tumorigenesis through increased genomic instability. J Pathol 246(2): 134-140, 2018. PMID: 29952003. DOI: 10.1002/path.5128
    OpenUrlCrossRefPubMed
  17. ↵
    1. Allin KH and
    2. Nordestgaard BG
    : Elevated C-reactive protein in the diagnosis, prognosis, and cause of cancer. Crit Rev Clin Lab Sci 48(4): 155-170, 2011. PMID: 22035340. DOI: 10.3109/10408363.2011.599831
    OpenUrlCrossRefPubMed
  18. ↵
    1. Chandra RK
    : Nutrition and the immune system: an introduction. Am J Clin Nutr 66(2): 460S-463S, 1997. PMID: 9250133. DOI: 10.1093/ajcn/66.2.460S
    OpenUrlAbstract/FREE Full Text
  19. ↵
    1. Remon J,
    2. Esteller L and
    3. Taus Á
    : Nivolumab plus ipilimumab combination therapy for the first-line treatment NSCLC: evidence to date. Cancer Manag Res 11: 4893-4904, 2019. PMID: 31213908. DOI: 10.2147/CMAR.S164935
    OpenUrlCrossRefPubMed
  20. ↵
    1. Fridman WH,
    2. Zitvogel L,
    3. Sautès-Fridman C and
    4. Kroemer G
    : The immune contexture in cancer prognosis and treatment. Nat Rev Clin Oncol 14(12): 717-734, 2017. PMID: 28741618. DOI: 10.1038/nrclinonc.2017.101
    OpenUrlCrossRefPubMed
  21. ↵
    1. Varga A,
    2. Bernard-Tessier A,
    3. Auclin E,
    4. Mezquita Pérez L,
    5. Baldini C,
    6. Planchard D,
    7. Marabelle A,
    8. Hollebecque A,
    9. Besse B and
    10. Massard C
    : Applicability of the lung immune prognostic index (LIPI) in patients with metastatic solid tumors when treated with immune checkpoint inhibitors (ICI) in early clinical trials. Annals of Oncology 30: i2, 2020. DOI: 10.1093/annonc/mdz027.001
    OpenUrlCrossRef
  22. ↵
    1. Bilen MA,
    2. Martini DJ,
    3. Liu Y,
    4. Shabto JM,
    5. Brown JT,
    6. Williams M,
    7. Khan AI,
    8. Speak A,
    9. Lewis C,
    10. Collins H,
    11. Kissick HT,
    12. Carthon BC,
    13. Akce M,
    14. Shaib WL,
    15. Alese OB,
    16. Pillai RN,
    17. Steuer CE,
    18. Wu CS,
    19. Lawson DH,
    20. Kudchadkar RR,
    21. El-Rayes BF,
    22. Ramalingam SS,
    23. Owonikoko TK,
    24. Harvey RD and
    25. Master VA
    : Combined effect of sarcopenia and systemic inflammation on survival in patients with advanced stage cancer treated with immunotherapy. Oncologist 25(3): e528-e535, 2020. PMID: 32162807. DOI: 10.1634/theoncologist.2019-0751
    OpenUrlCrossRefPubMed
    1. Liang S,
    2. Li C,
    3. Gao Z,
    4. Li J,
    5. Zhao H,
    6. Yu J and
    7. Meng X
    : A nomogram to predict short-term outcome of radiotherapy or chemoradiotherapy based on pre/post-treatment inflammatory biomarkers and their dynamic changes in esophageal squamous cell carcinoma. Int Immunopharmacol 90: 107178, 2021. PMID: 33218939. DOI: 10.1016/j.intimp.2020.107178
    OpenUrlCrossRefPubMed
    1. Maruyama T,
    2. Shimoda M,
    3. Hakoda H,
    4. Sako A,
    5. Ueda K and
    6. Suzuki S
    : Preoperative prognostic nutritional index predicts risk of recurrence after curative resection for stage IIA colon cancer. Am J Surg 222(1): 179-185, 2021. PMID: 33138968. DOI: 10.1016/j.amjsurg.2020.10.032
    OpenUrlCrossRefPubMed
    1. Santos PB,
    2. Patel H,
    3. Henrique R and
    4. Félix A
    : Can epigenetic and inflammatory biomarkers identify clinically aggressive prostate cancer? World J Clin Oncol 11(2): 43-52, 2020. PMID: 32133274. DOI: 10.5306/wjco.v11.i2.43
    OpenUrlCrossRefPubMed
  26. ↵
    1. Xia WY,
    2. Zhu XR,
    3. Feng W,
    4. Liu J,
    5. Wang JM,
    6. Lv CX,
    7. Zhang Q,
    8. Yu W,
    9. Cai XW and
    10. Fu XL
    : Neutrophil-lymphocyte ratio and platelet-lymphocyte ratio associations with heart and body dose and their effects on patient outcomes in locally advanced non-small cell lung cancer treated with definitive radiotherapy. Transl Lung Cancer Res 9(5): 1996-2007, 2020. PMID: 33209619. DOI: 10.21037/tlcr-20-831
    OpenUrlCrossRefPubMed
  27. ↵
    1. Treffers LW,
    2. Hiemstra IH,
    3. Kuijpers TW,
    4. van den Berg TK and
    5. Matlung HL
    : Neutrophils in cancer. Immunol Rev 273(1): 312-328, 2016. PMID: 27558343. DOI: 10.1111/imr.12444
    OpenUrlCrossRefPubMed
  28. ↵
    1. Templeton AJ,
    2. McNamara MG,
    3. Šeruga B,
    4. Vera-Badillo FE,
    5. Aneja P,
    6. Ocaña A,
    7. Leibowitz-Amit R,
    8. Sonpavde G,
    9. Knox JJ,
    10. Tran B,
    11. Tannock IF and
    12. Amir E
    : Prognostic role of neutrophil-to-lymphocyte ratio in solid tumors: a systematic review and meta-analysis. J Natl Cancer Inst 106(6): dju124, 2014. PMID: 24875653. DOI: 10.1093/jnci/dju124
    OpenUrlCrossRefPubMed
  29. ↵
    1. Ozawa Y,
    2. Amano Y,
    3. Kanata K,
    4. Hasegwa H,
    5. Matsui T,
    6. Kakutani T,
    7. Koyauchi T,
    8. Tanahashi M,
    9. Niwa H,
    10. Yokomura K and
    11. Suda T
    : Impact of early inflammatory cytokine elevation after commencement of PD-1 inhibitors to predict efficacy in patients with non-small cell lung cancer. Med Oncol 36(4): 33, 2019. PMID: 30825015. DOI: 10.1007/s12032-019-1255-3
    OpenUrlCrossRefPubMed
  30. ↵
    1. Liu W,
    2. Wang H,
    3. Bai F,
    4. Ding L,
    5. Huang Y,
    6. Lu C,
    7. Chen S,
    8. Li C,
    9. Yue X,
    10. Liang X,
    11. Ma C,
    12. Xu L and
    13. Gao L
    : IL-6 promotes metastasis of non-small-cell lung cancer by up-regulating TIM-4 via NF-κB. Cell Prolif 53(3): e12776, 2020. PMID: 32020709. DOI: 10.1111/cpr.12776
    OpenUrlCrossRefPubMed
  31. ↵
    1. McMillan DC,
    2. Elahi MM,
    3. Sattar N,
    4. Angerson WJ,
    5. Johnstone J and
    6. McArdle CS
    : Measurement of the systemic inflammatory response predicts cancer-specific and non-cancer survival in patients with cancer. Nutr Cancer 41(1-2): 64-69, 2001. PMID: 12094630. DOI: 10.1080/01635581.2001.9680613
    OpenUrlCrossRefPubMed
  32. ↵
    1. McMillan DC,
    2. Watson WS,
    3. O’Gorman P,
    4. Preston T,
    5. Scott HR and
    6. McArdle CS
    : Albumin concentrations are primarily determined by the body cell mass and the systemic inflammatory response in cancer patients with weight loss. Nutr Cancer 39(2): 210-213, 2001. PMID: 11759282. DOI: 10.1207/S15327914nc392_8
    OpenUrlCrossRefPubMed
  33. ↵
    1. Lindenmann J,
    2. Fink-Neuboeck N,
    3. Taucher V,
    4. Pichler M,
    5. Posch F,
    6. Brcic L,
    7. Smolle E,
    8. Koter S,
    9. Smolle J and
    10. Smolle-Juettner FM
    : Prediction of postoperative clinical outcomes in resected stage I non-small cell lung cancer focusing on the preoperative Glasgow Prognostic Score. Cancers (Basel) 12(1): 152, 2020. PMID: 31936329. DOI: 10.3390/cancers12010152
    OpenUrlCrossRefPubMed
  34. ↵
    1. Tomita M,
    2. Ayabe T,
    3. Chosa E and
    4. Nakamura K
    : Prognostic significance of pre- and postoperative glasgow prognostic score for patients with non-small cell lung cancer. Anticancer Res 34(6): 3137-3140, 2014. PMID: 24922684.
    OpenUrlAbstract/FREE Full Text
Back to top

In this issue

Print
Download PDF
Article Alerts
Email Article
Citation Tools
Reprints and Permissions
Significance of Glasgow Prognostic Scores in NSCLC Patients Treated With Immunotherapy After Platinum-based Cytotoxic Chemotherapy
HYE SEON KANG, AH YOUNG SHIN, CHANG DONG YEO, SUNG KYOUNG KIM, CHAN KWON PARK, JU SANG KIM, SEUNG JOON KIM, SANG HAAK LEE, JIN WOO KIM
In Vivo Nov 2021, 35 (6) 3423-3430; DOI: 10.21873/invivo.12642
Reddit logo Twitter logo Facebook logo Mendeley logo

Jump to section

Keywords