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ORIGINAL
Ability of the Glasgow Prognostic Score to predict thetolerability and efficacy of platinum-combination
chemotherapy among elderly patients with advanced
non-small cell lung cancer
Kazuhisa Nakashima, Kojiro Hata, Takamasa Hotta, Seiko Tanaka, Yuki Mitarai, Takae Okuno, Akari Tanino,Mika Nakao, Yoshihiro Amano, Megumi Hamaguchi, Tamio Okimoto, Shunichi Hamaguchi, Taishi Nagao,
Noriaki Kurimoto, Takeshi Isobe, and Yukari Tsubata
Department of Internal Medicine, Division of Medical Oncology & Respiratory Medicine, Shimane University Faculty of Medicine, Shimane,Japan

Abstract : Background : Although platinum-combination chemotherapy is widely used to treat advanced nonsmall cell lung cancer (NSCLC), not all elderly patients benefit from this regimen. In this retrospective study,
we aimed to evaluate whether the Glasgow Prognostic Score (GPS), an indicator of systemic inflammation andmalnutrition, could predict the tolerability and efficacy of platinum-combination chemotherapy among elderly
patients with NSCLC. Methods : The eligibility criteria included patients aged ≥ 70 years with NSCLC treatedwith first-line platinum-combination chemotherapy at Shimane University Hospital between January 2015 andDecember 2018. Results : Thirty-two patients with NSCLC (median age, 74 years) were included. The GPS scores
were 0–1 for 19 patients and 2 for 13 patients. Four chemotherapy cycles were completed by 57.9% and 30.8%
of patients in the GPS 0–1 and GPS 2 groups, respectively. The GPS 0–1 group experienced better outcomesthan the GPS 2 group (response rate : 26% vs. 15%, P = 0.67 ; median progression-free survival : 4.1 vs. 2.1 months,
P = 0.0026 ; median overall survival : 22.8 vs. 9.6 months, P = 0.0092). Conclusions : Platinum-combination chemotherapy demonstrated promising efficacy among elderly NSCLC patients with a GPS 0–1. Therefore, GPS may
be crucial in determining whether treatments recommended for younger patients are suitable for older patientswith NSCLC. J. Med. Invest. 68 : 260-264, August, 2021
Keywords : non-small cell lung cancer, platinum-combination chemotherapy, Glasgow Prognostic Score, elderly patientsINTRODUCTION
Platinum-combination chemotherapy is a widely used
standard treatment for advanced non-small cell lung cancer(NSCLC) (1). The recent development of reduced toxicity in platinum-combinations has broadened its scope by including elderly
patients (2-5). However, elderly patients experience age-relatedchanges along with the development of comorbidities, implyingthat not all elderly patients benefit from platinum-combination
chemotherapy. For example, although a subset analysis of theCA031 study data demonstrated that carboplatin plus nanoparticle albumin-bound paclitaxel is safe and effective among elderly
patients, a phase II study to assess the efficacy and safety of thetreatment regimen was interrupted because of treatment-related mortality and serious adverse events among elderly patientswith NSCLC (4, 6).
The Glasgow Prognostic Score (GPS) is an indicator of systemic inflammation and malnutrition (7, 8). Fujio et al. retrospectively demonstrated that among patients with advanced NSCLC
and an Eastern Cooperative Oncology Group performance status(PS) of 2, a high GPS was associated with poorer outcomes thana low GPS (9). Thus, the GPS may be useful for identifying
elderly patients with NSCLC who are likely to benefit from
Received for publication January 18, 2021 ; accepted April 21, 2021.
Address correspondence and reprint requests to Yukari Tsubata, MD,
PhD, Department of Internal Medicine, Division of Medical Oncology& Respiratory Medicine, Shimane University Faculty of Medicine,89-1 Enya-cho, Izumo, Shimane, Japan and Fax : +81-853-20-2581.

platinum-combination chemotherapy. The present study aimed
to evaluate whether the GPS could predict the tolerability andefficacy of platinum-combination chemotherapy in elderly patients with NSCLC.

PATIENTS AND METHODSPatients

We retrospectively reviewed elderly patients with NSCLC
who received platinum-combination chemotherapy as first-line
treatment at the Shimane University Hospital between January
2015 and December 2018. The study’s retrospective protocol
was approved by our Institutional Review Board (approval
number : 4654, approval date : June 4, 2020), which also waived
the requirement for informed consent. Based on several previous
studies, “elderly” patients were defined as being aged ≥ 70 years(2, 4, 6). Patients were excluded from this study if they had
epidermal growth factor receptor gene mutations or anaplastic
lymphoma kinase fusion genes.

Assessments
Blood tests were conducted for all patients to determine theirpretreatment serum concentrations of serum albumin (Alb) andC-reactive protein (CRP). Those findings were used to determine
the GPS scores (7, 8) : a GPS of 0 was defined as patients with
CRP concentration of < 1.0 mg / dL and Alb concentration of ≥ 3.5
mg / dL ; a GPS of 1 was defined as patients with CRP concentration of ≥ 1.0 mg / dL or Alb concentration of < 3.5 mg / dL ; and a
GPS of 2 as patients with CRP concentration of ≥ 1.0 mg / dL and

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The Journal of Medical Investigation Vol. 68 August 2021
Alb concentration of < 3.5 mg / dL. In a retrospective study for advanced patients with NSCLC with a PS of 2, Fujio et al. compared
the outcomes to a GPS 0–1 group or a GPS 2 group (9). Similarly,
in our study, the patients were assigned to a GPS 0–1 groupor a GPS 2 group for the analyses to compare the tolerability
and efficacy of platinum-combination chemotherapy. Treatment
responses were retrospectively assessed using version 1.1 of the
Response Evaluation Criteria in Solid Tumors. Adverse eventswere evaluated using version 5.0 of the Common Terminology
Criteria for Adverse Events.

14 patients and GPS 1 included 5 patients), and the GPS 2 group
included 13 patients. The GPS 0–1 group included 6 patientswith a PS of 0, 11 with a PS of 1, and 2 with a PS of 2. All 13
patients in the GPS 2 group had a PS of 1. Chronic obstructive
pulmonary disease, diabetes mellitus, and heart disease werecommon comorbidities. Most patients received carboplatin as theplatinum agent. Although there were no significant differencesin the baseline characteristics of the two groups, the GPS 0–1
group had higher proportions of female patients, presence ofother cancers, and interstitial lung disease.

Statistical methods

Treatment parameters

Progression-free survival (PFS) and overall survival (OS)outcomes were evaluated using the Kaplan-Meier method andlog-rank test. All other analyses were performed using Fisher’s
exact test. Differences were considered statistically significant
at P-values of < 0.05. The analyses were performed using JMP
software (version 10.0 ; SAS Institute, Cary, NC, USA).

The treatment parameters are shown in Table 2. The median
number of chemotherapy cycles was 4 cycles (range : 1–11 cycles)in the GPS 0–1 group and 2 (range : 1–4 cycles) in the GPS 2group. Four chemotherapy cycles were completed by 57.9% of
patients in the GPS 0–1 group and 30.8% in the GPS 2 group.
The main cause of treatment discontinuation was disease progression, which was relatively common in the GPS 2 group (7patients, 53.4%).

RESULTS

Patient characteristics

Table 2. Treatment parameters

The study included 32 patients (29 men and 3 women) witha median age of 74 years, and their characteristics are listed inTable 1. The GPS 0–1 group included 19 patients (GPS 0 included

Median chemotherapy cycles (range)

GPS 0–1 (n = 19) GPS 2 (n = 13)
4 (1–11)

Patients who completed 4 cycles, n (%) 11 (57.9%)

2 (1–4)4 (30.8%)

Causes of discontinuation

Table 1. Patient characteristics
GPS 0–1(n = 19)GPS 2(n = 13)Age, years

Median (range)

74 (70–84)

74 (70–82)

Sex, n (%)

Female3 (15.8%)

0 (0%)

Histology, n (%)

Non-SCC

11 (57.9%)

6 (46.2%)SCC

8 (42.1%)

7 (53.8%)III

4 (21.0%)

2 (15.4%)IV

15 (78.9%)

11 (84.6%)

0

6 (31.6%)

0 (0%)1

11 (57.9%)

13 (100%)2

2 (10.5%)

0 (0%)

COPD

8 (42.1%)

5 (38.5%)DM

6 (31.6%)

6 (46.2%)

Heart disease

6 (31.6%)

4 (30.8%)

Other cancer

7 (36.8%)

1 (7.7%)ILD

6 (31.6%)

1 (7.7%)

Cerebrovascular disease

4 (21.0%)

2 (15.4%)

Hepatic disease

3 (15.8%)

2 (15.4%)

CBDCA

16 (84.2%)

12 (92.3%)CDDP

3 (15.8%)

1 (7.7%)PEM

5 (26.3%)

5 (38.5%)

Nab-PTX

3 (15.8%)

4 (30.8%)

TS-1

4 (21.0%)

3 (23.1%)

PEM + Bev

4 (21.0%)0 (0%)PTX

2 (10.5%)

0 (0%)

Stage, n (%)
PS, n (%)

Comorbidities, n (%)

Platinum agent, n (%)
Additional drugs, n (%)

GEM

1 (5.3%)1 (7.7%)

GPS, Glasgow Prognostic Score ; SCC, squamous cell carcinoma ; PS,
performance status ; COPD, chronic obstructive pulmonary disease ; DM, diabetes mellitus ; ILD, interstitial lung disease ; CBDCA,
carboplatin ; CDDP, cisplatin ; PEM, pemetrexed ; nab-PTX, nanoparticle albumin-bound paclitaxel ; TS-1, tegafur / gimeracil / oteracil ; BEV,
bevacizumab ; PTX, paclitaxel ; GEM, gemcitabine.

Disease progression, n (%)

4 (21.0%)

7 (53.4%)

Toxicity, n (%)

2 (10.5%)

2 (15.4%)

PS worsening, n (%)

2 (10.5%)

0 (0%)

GPS, Glasgow Prognostic Score ; PS, performance status.

Efficacy
Table 3 shows the tumor responses. The overall response rates(ORRs) were 26.3% in the GPS 0–1 group and 15.4% in the GPS
2 group ; however, the difference was not significant (P = 0.67).
The disease control rates were 68.4% in the GPS 0–1 groupand 23.1% in the GPS 2 group, and most patients in the GPS 2group developed progressive disease (10 patients, 76.9%). The
survival curves are shown in Figures 1 and 2. Patients in the
GPS 0–1 group had significantly longer median values for PFS(4.1 months [95% confidence interval : 2.2-7.4 months] vs. 2.1
months [95% confidence interval : 0.8-2.7 months], P = 0.0026)
and OS (22.8 months [95% confidence interval : 8.2-NA months]
vs. 9.6 months [95% confidence interval : 2.6-14.8 months],
P = 0.0092). In a subgroup analysis including patients aged ≥75
years (n = 15), the median PFS in the GPS 0–1 group and theGPS 2 group was 3.2 and 2.1 months (P = 0.11), respectively, andTable 3. Tumor responses
GPS 0–1 (n = 19)

GPS 2 (n = 13)

CR, n (%)

0 (0%)

0 (0%)

PR, n (%)

5 (26.3%)

2 (15.4%)

PSD, n (%)

8 (42.1%)

1 (7.7%)PD, n (%)

6 (31.6%)

10 (76.9%)

ORR

26.3%

15.4%

0.67

DCR

68.4%

23.1%

0.29

CR, complete response ; PR, partial response ; SD, stable disease ; PD, progressive disease ; ORR, overall response rate ; DCR,
disease control rate.

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K. Nakashima, et al. GPS and chemotherapy for elderly NSCLC
Table 4. Toxicities
GPS 0–1 (n = 19)

Figure 1. Kaplan-Meier curves for progression-free survival (PFS)

according to the Glasgow prognostic score (GPS).

GPS 2 (n = 13)

Hematological

All gradesn (%)

Grade ≥ 3n (%)

All gradesn (%)

Grade ≥ 3n (%)

Anemia19 (100%)

3 (15.8%)

13 (100%)

5 (38.5%)

Thrombocytopenia

12 (63.2%)

4 (21.0%)

10 (76.9%)

3 (23.1%)

Neutropenia

12 (63.2%)

6 (31.6%)

9 (69.2%)

2 (15.4%)

Leukopenia

11 (57.9%)

3 (15.8%)

9 (69.2%)

3 (23.1%)

Non-hematological

All gradesn (%)

Grade ≥ 3n (%)

All gradesn (%)

Grade ≥ 3n (%)

Anorexia

14 (73.7%)

0 (0%)

8 (61.5%)

1 (7.7%)

Constipation

12 (63.2%)

0 (0%)

9 (69.2%)

0 (0%)

Fatigue

11 (57.9%)

0 (0%)

10 (76.9%)

0 (0%)

Nausea6 (31.6%)

0 (0%)

4 (30.8%)

1 (7.7%)AST

5 (26.3%)

0 (0%)

5 (38.5%)

0 (0%)ALT

4 (21.0%)0 (0%)

3 (23.1%)

0 (0%)Creatinine

2 (10.5%)

0 (0%)

3 (23.1%)

1 (7.7%)Rash

2 (10.5%)

0 (0%)

2 (15.4%)

1 (7.7%)

GPS, Glasgow prognostic score ; AST, aspartate transaminase ; ALT,
alanine transaminase.

DISCUSSION

Figure 2. Kaplan-Meier curves for overall survival (OS) according
to the Glasgow prognostic score (GPS).

the median OS in the GPS 0–1 group and the GPS 2 group was
32.5 and 9.8 months (p = 0.11), respectively.
Additional chemotherapy regimens were administered to 14
patients (73.7%) in the GPS 0–1 group and 8 (61.5%) in the GPS
2 group. Immune checkpoint inhibitors (ICIs) were administered
to 9 patients (47.4%) (programmed death-ligand 1 tumor proportion score was 0% in 3 patients, 1-49% in 2 patients, ≥50% in 1
patient, and unknown in 3 patients) in the GPS 0–1 group and 6
patients (46.2%) (programmed death-ligand 1 tumor proportion
score was 0% in 2 patients, 1-49% in 2 patients, and unknownin 2 patients) in the GPS 2 group. In the GPS 0–1 group, ORR
of ICIs was 22% and 3 patients experienced PFS for more than
1 year by ICIs. In the GPS 2 group, ORR of ICIs was 0% and 1
patient experienced PFS for more than 1 year by ICIs.

Toxicity
The most common adverse events are shown in Table 4. No
significant inter-group differences were observed for all gradesof adverse events. However, both groups had relatively highrates of hematological adverse events, except febrile neutropenia,
with incidences of 15–40% for grade 3–4 hematological adverse
events. One patient in the GPS 0–1 group experienced febrileneutropenia. Although anorexia, constipation, and fatigue werecommon events, few cases involved grade 3 events. No grade 4
non-hematological adverse events were observed in either of thetwo groups. However, 1 treatment-related death caused by grade
5 acute kidney injury occurred in the GPS 2 group.

This retrospective study evaluated whether the GPS could
efficiently predict the tolerability and efficacy of platinum-combination chemotherapy among elderly Japanese patients with
NSCLC. The results revealed that the GPS 0–1 group had an
ORR of 26.3%, a median PFS of 4.1 months, and a median OS of
22.8 months. These results were comparable to the reported efficacy of platinum-combination chemotherapy among all patientswith NSCLC, including young patients (3, 10-12). The present
study revealed that the GPS 2 group had a higher disease progression rate and shorter PFS and OS intervals than the GPS
0–1 group. Similarly, in a subgroup analysis of patients aged ≥75
years, the median PFS and OS of the GPS 0–1 group tended to
be longer than those of the GPS 2 group (3.2 vs 2.1 months and32.5 vs 9.8 months, respectively). There were no significant differences observed with regard to adverse events between the twogroups, and only a few patients experienced febrile neutropenia
or grade 3 non-hematological adverse events. Moreover, in the
GPS 2 group, the main cause of treatment discontinuation was
disease progression, as opposed to toxicity. Thus, platinum-combination chemotherapy might be less effective, but not intolerable, for elderly patients with NSCLC and a GPS of 2.
Although in our study, all patients in the GPS 2 group possessed a good PS (PS = 1), they experienced poor response totreatment and had a poor prognosis. Therefore, for elderly patients, assessment using the PS alone may be insufficient, and
the GPS could be a valuable marker for predicting the tolerability, efficacy, and prognosis after various treatments for NSCLC(7, 8, 13-16). Furthermore, Fujio et al. reported that among
patients with advanced NSCLC and a PS of 2, a GPS of 2 wasassociated with poorer outcomes than a GPS of 0–1 (9). Basedon the results of our study and that conducted by Fujio et al., itappears that patients with NSCLC with a GPS of 0–1 might
benefit from standard treatment that is recommended for younger patients or patients with a good PS, even if the patient is in ahigh-risk group (older aged or poorer PS). Thus, the GPS might
be a helpful tool to guide treatment selection for NSCLC among
patients with higher risk factors. Additionally, the combinationof platinum-based chemotherapy and ICIs has recently become

The Journal of Medical Investigation Vol. 68 August 2021
standard therapy for advanced NSCLC (17-19). Therefore, we
further intend to verify whether the GPS can predict the tolerability and efficacy of platinum-based chemotherapy plus ICIs
among elderly patients with NSCLC.
The present study has several limitations. First, the retrospective design and small sample size are potential sources of bias.
Second, the patients were treated using various chemotherapy
regimens, and the small sample size precluded treatment-specific sub-analyses. Third, CRP and Alb concentrations are nonspecific markers, and comorbidities can also influence the GPS.
Therefore, the GPS may not always accurately reflect the condition of elderly patients with NSCLC. Fourth, additional therapy
with ICIs might affect the result for OS. The efficacy of ICIs was
better in the GPS 0–1 group than in the GPS 2 group.
In conclusion, platinum-combination chemotherapy provided
promising efficacy for elderly patients with NSCLC and a GPS of
0–1. Thus, elderly patients with NSCLC and a GPS of 0–1 may
benefit from standard treatment regimens that are generally
recommended for younger patients.

FUNDING
This research did not receive any specific grants from funding
agencies in the public, commercial, or not-for-profit sectors.

CONFLICTS OF INTEREST
Takeshi Isobe has received personal fees from AstraZeneca,
Pfizer, and Boehringer Ingelheim outside of the submitted work.
Yukari Tsubata has previously received personal fees from
AstraZeneca, Chugai Pharmaceutical, and Daiichi-Sankyo outside of the submitted work. The other authors have no conflictsof interest to declare.

ACKNOWLEDGEMENT
We would like to thank Editage (www.editage.com) for English language editing.

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