Retrospective study on the tolerability using a four-cycle completion in elderly patients with extensive-stage small-cell lung cancer: a body mass index-based analysis

Introduction

The combination of an anti-programmed death-ligand 1 (PD-L1) antibody with etoposide and either carboplatin or cisplatin (platinum-etoposide) has become the standard of treatment for extensive-stage small-cell lung cancer (ES-SCLC) (1-3). Approximately 30% of patients with SCLC are over 70 years of age at diagnosis (4). Previous studies have reported the efficacy of anti-PD-L1 antibody combined with platinum-etoposide in elderly patients with ES-SCLC (5,6). However, elderly patients with unresectable cancer represent a heterogeneous group characterized by physiological decline, immune dysfunction, and multiple comorbidities (7). Elderly patients are often excluded from clinical trials, and those who are included tend to be selected, fit individuals without major comorbidities. Therefore, addressing both the efficacy and adverse events of immunochemotherapy in elderly patients with ES-SCLC is critically important in clinical practice.

The World Health Organization defines older adults as individuals aged ≥65 years (8). Commonly used evaluations such as chronological age and the globally adopted Eastern Cooperative Oncology Group performance status (ECOG-PS) have limitations when assessing elderly patients with unstable conditions. Therefore, the International Society of Geriatric Oncology recommends evaluating elderly patients with cancer using geriatric assessments to predict prognosis and support treatment decisions (9). One widely used screening tool is the Geriatric-8 (G-8) (10). This tool consists of eight items that assess diet, weight loss, physical activity, neuropsychiatric status, body mass index (BMI), number of oral medications, overall health perception, and age, providing a quick and practical evaluation. Although associations between geriatric assessment and treatment effectiveness or immune-related adverse events (irAEs) have been demonstrated, the relationship with treatment tolerability in elderly patients with ES-SCLC remains insufficiently understood (11,12). BMI, one of the parameters included in the G-8 score, can be retrospectively analyzed. Additionally, BMI can be assessed more easily than other nutritional indicators such as Geriatric Nutritional Risk Index (GNRI) or Prognostic Nutritional Index (PNI), and it was routinely evaluated in our institution. While the G-8 score is not specific to thoracic oncology, it is globally recognized and widely implemented in geriatric assessment. Moreover, the choice of a BMI <19 kg/m² as a cutoff should be viewed as a clinically meaningful question, and its appropriateness remains an important area for further evaluation.

We hypothesized that low BMI is associated with lower tolerability, defined as completion of fewer than four cycles of immunochemotherapy, in elderly patients with ES-SCLC. In this retrospective study, we aimed to examine the association between low BMI and treatment tolerability in elderly patients with ES-SCLC receiving immunochemotherapy. We also assessed treatment efficacy. We present this article in accordance with the STROBE reporting checklist (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-1058/rc).

Methods

Patients

Between August 1, 2019, and April 30, 2024, 72 patients aged 65 years or older with ES-SCLC were treated with anti-PD-L1 antibody combined with platinum-etoposide at Nippon Medical School Hospital, Tokyo, Japan. Of these, one patient was excluded due to loss to follow-up, leaving 71 patients for the final analysis. Clinical data were retrospectively extracted from medical records, including patient age, sex, clinical stage, smoking history, ECOG performance status at the initiation of immunochemotherapy, pretreatment BMI, use of pegfilgrastim, and the specific immunochemotherapy regimen administered. A low BMI was defined as <19 kg/m² immediately before treatment, based on the G-8 score cutoff value. Dose intensity (%) was calculated as follows: (cumulative dose/planned maximum dose) × 100% in overall cycles (4,5). Tolerability was defined as completion of four cycles of anti-PD-L1 antibody plus platinum-etoposide, according to the North East Japan Study Group (NEJSG) 045A study (13). We manually reviewed the medical records and evaluated only grade ≥3 AEs in entire course using Common Terminology Criteria for Adverse Events (CTCAE) version 6.0. All study procedures were conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study received ethical approval from the Institutional Review Board of the Graduate School of Medicine, Nippon Medical School (No. B-2023-768). The requirement for informed consent was waived because of the retrospective nature of the study; however, an opt-out option was provided.

Statistical analysis

Baseline patient characteristics were summarized as numbers and percentages. Fisher’s exact test was used for categorical data, and the Mann-Whitney U test was applied to continuous variables. Baseline characteristics and clinical responses to immunochemotherapy were compared between patients with low and non-low BMI. Progression-free survival (PFS) was defined as the interval from the start of immunochemotherapy to the first documented disease progression or death. Overall survival (OS) was defined as the time from treatment initiation to death from any cause. Patients who had not experienced disease progression or were still alive at the time of data cutoff were censored at the date of their last follow-up. Kaplan-Meier survival curves were generated for PFS and OS, and intergroup comparisons were performed using the log-rank test and Cox proportional hazards regression. Survival outcomes were reported as hazard ratios (HRs) with 95% confidence intervals (CIs). A two-tailed P value <0.05 was considered statistically significant. For univariate and multivariate analyses, logistic regression was used to estimate odds ratios (ORs) with 95% CIs. Given the limited sample size and number of events, we decided to include only the variables that were significant in the univariate analysis in the multivariate model. Statistical computations were carried out using EZR version 1.68 (Saitama Medical Center, Jichi Medical University, Saitama, Japan) (14).

Results

Patient characteristics

The study included 71 patients aged ≥65 years with ES-SCLC who underwent treatment with anti-PD-L1 antibody in combination with platinum-etoposide. Baseline characteristics are summarized in Table 1. The median age was 73 years (range, 65–91 years), and 51 patients (71.8%) were male. Most patients (94.4%) were current or former smokers, and 54 (76.1%) had an ECOG-PS of 0 or 1. According to the 8th edition of the tumor-node-metastasis (TNM) staging system for lung cancer, 52 patients (73.2%) had stage IV disease, 7 (9.9%) had stage III disease, and 12 (16.9%) presented with recurrent disease. Fifty-three patients (74.6%) received immunochemotherapy as first-line treatment. For the platinum agents, 64 patients (90.1%) received carboplatin and 7 (9.9%) received cisplatin. The median dose intensities of cisplatin, carboplatin, and etoposide were 88.6%, 86.9%, and 75.0%, respectively. Regarding immune checkpoint inhibitors (ICIs), 37 patients (52.1%) received durvalumab and 34 patients (47.9%) received atezolizumab.

Association of BMI with the tolerability of immunochemotherapy

Patients were categorized into non-low and low BMI groups [n=55 (77.5%) and n=16 (22.5%), respectively]. There was no significant difference in the median dose intensities of cisplatin, carboplatin, and etoposide between the two groups (Table 1). Among patients with non-low BMI, 44 (80.0%) demonstrated tolerability of immunochemotherapy, and the median number of maintenance cycles was 2 (range, 0–30) (Table 2). Among patients with low BMI, 8 (50.0%) demonstrated tolerability, and the median number of maintenance cycles was 1 (range, 0–30). Fisher’s exact test indicated a statistically significant association between BMI and tolerability. Univariate analysis showed that tolerability was significantly associated with BMI (<19 vs. ≥19 kg/m²) (OR: 0.25; 95% CI: 0.08–0.82; P=0.02) and ECOG-PS (≥2 vs. <2) (OR: 0.14; 95% CI: 0.04–0.47; P=0.001) (Table 3). Similarly, multivariate analysis revealed significant associations between tolerability and BMI (<19 vs. ≥19 kg/m²) (OR: 0.24; 95% CI: 0.06–0.88; P=0.03) and ECOG-PS (≥2 vs. <2) (OR: 0.13; 95% CI: 0.04–0.48; P=0.002) (Table 3).

Table 4 summarizes the reasons for not completing immunochemotherapy. In the non-low BMI group, discontinuation occurred due to AE (54.5%), disease progression (36.4%), and ECOG-PS deterioration due to comorbidities (9.1%). In the low BMI group, discontinuation was due to AE (12.5%), disease progression (12.5%), ECOG-PS deterioration due to comorbidities (25.0%), ECOG-PS deterioration due to lung cancer (37.5%), and patient preference (12.5%). No statistically significant differences were observed in reasons for discontinuation between the two groups.

Association of BMI with the efficacy and safety of immunochemotherapy

Among the study population, 53 patients received immunochemotherapy as first-line treatment. The median follow-up period was 15.3 months for non-low BMI group and 10.2 months for low BMI group. We analyzed PFS and OS in this cohort. The median PFS was 5.9 months (95% CI: 4.6–7.4) in patients with non-low BMI and 8.6 months (95% CI: 3.5–10.5) in those with low BMI (Figure 1A). The median OS was 14.6 months (95% CI: 7.6–19.7) in patients with non-low BMI and not attained (NA) in those with low BMI [95% CI: 3.2–NA] (Figure 1B). PFS and OS did not differ significantly between patients with and without low BMI (HR, 0.83; 95% CI: 0.38–1.83; P=0.64 and HR, 0.87; 95% CI: 0.31–2.42; P=0.71, respectively).

Figure 1 Kaplan-Meier survival curves for (A) PFS and (B) OS in elderly patients with ES-SCLC treated with anti-PD-L1 antibody plus platinum-etoposide as first-line therapy, comparing patients with low BMI (n=11) and non-low BMI (n=42). BMI, body mass index; CI, confidence interval; ES-SCLC, extensive-stage small-cell lung cancer; NA, not attained; OS, overall survival; PD-L1, programmed death-ligand 1; PFS, progression-free survival.

In the safety analysis of the total cohort, grade ≥3 AEs occurred in 43 patients (78.2%) with non-low BMI and 11 patients (68.8%) with low BMI (Table 5), with no significant difference between the groups (P=0.51). Grade ≥3 hematologic AEs occurred in 42 patients (76.4%) with non-low BMI and 11 patients (68.8%) with low BMI, whereas grade ≥3 non-hematologic AEs occurred in 6 patients (10.9%) with non-low BMI and 1 patient (6.3%) with low BMI. Similarly, no significant differences were observed between the two groups (P=0.53 and P>0.99, respectively).

Discussion

In this retrospective study of 71 elderly patients with ES-SCLC receiving anti-PD-L1 antibody combined with platinum-etoposide, multivariate analysis revealed that tolerability was significantly reduced in patients with low BMI and ECOG-PS ≥2. Most elderly patients with cancer represent a vulnerable population due to physiological decline, immune dysfunction, neuropsychiatric impairment, multiple comorbidities, nutritional disorders, and limited treatment support.

We focused on tolerability based on the NEJSG 045A study (15). Identifying patients likely to tolerate immunochemotherapy is essential for shared decision-making among clinicians and patients. To our knowledge, this is the first study to demonstrate an association between low BMI and reduced tolerability of immunochemotherapy in elderly patients with ES-SCLC. Additionally, we showed the correlation between poor ECOG-PS and reduced tolerability, consistent with prior evidence showing poorer prognosis in non-SCLC (NSCLC) patients with poor PS (15,16). Low BMI may reflect tumor-induced malnutrition, which is associated with impaired treatment response, increased toxicity, and reduced survival across several cancers (17). In patients with stage III NSCLC, poor PS and low BMI (<18.5 kg/m²) were associated with reduced tolerance of concurrent chemoradiation and poor OS (18). Several studies have demonstrated a significant association between low BMI (<20 kg/m²) and OS in advanced NSCLC, and between low BMI (<18.5 kg/m²) and OS in SCLC (19-21). However, almost all patients in these studies were treated with cytotoxic chemotherapy. In the present study, no association was observed between BMI and PFS or OS in patients treated with immunochemotherapy as first-line therapy. Likewise, no significant difference was observed in the intensity of cytotoxic chemotherapy between the two groups. Based on our findings, in elderly patients with low BMI, transitioning to maintenance immunotherapy without completing four cycles of immunochemotherapy may not necessarily lead to shorter PFS or OS. However, it is important to acknowledge that the median OS in the non-low BMI group was not reached, which complicates the clinical interpretation of the survival comparison. It should also be noted that this analysis was based on a small sample size, which warrants cautious interpretation of the findings.

Low BMI may be attributed to cancer-related inflammation, disrupted balance between anabolic and catabolic processes, insufficient nutritional intake, and endocrine dysfunction (22). Low BMI is strongly associated with sarcopenia and cachexia. Cancer-related cachexia and sarcopenia are linked to poor prognosis, reduced response to treatment, longer hospital stays, and decreased quality of life (22-26). A previous study reported that the Glasgow Prognostic Score, a system based on serum C-reactive protein (CRP) and albumin concentrations, was significantly associated with PFS and OS in patients with ES-SCLC treated with atezolizumab plus carboplatin and etoposide (27). Cachexia and sarcopenia are known contributors to increased susceptibility to chemotherapy-related toxicities, such as fatigue, dysgeusia, mucositis, nausea/vomiting, hematologic toxicity, and pain (22). Moreover, malnutrition significantly impairs quality of life, contributing to psychological distress and discouraging continuation of treatment (28). In this study, serum CRP and albumin levels, chronic disease or genetic predisposition were not assessed. However, the combined influence of these factors may have contributed to the association between low BMI and reduced tolerability.

Elderly patients with cancer should be evaluated using geriatric assessments, including BMI. The GNRI and PNI are established tools for assessing nutritional status (29). A low baseline PNI may be associated with poor prognosis and the occurrence of irAEs in patients with ES-SCLC receiving immunochemotherapy (30). By contrast, BMI can be measured more routinely, requires neither specialized expertise nor costly equipment, and places minimal burden on patients. In the non-low BMI group, most discontinuations (90.9%) were due to adverse events or progressive disease, whereas in the low-BMI group, 62.5% discontinued due to PS deterioration related to comorbidities or lung cancer. This pattern suggests different underlying mechanisms of treatment intolerance. Thus, nutritional support for frail or malnourished patients may be important. Close collaboration among healthcare professionals is necessary to implement effective nutritional interventions.

This study is subject to several limitations. First, in this study, BMI was measured at the nearest available time point prior to treatment initiation. As a result, some variability in measurement timing among patients may have occurred. Second, in our cohort, approximately 25% of patients received immunochemotherapy as a second-line or later treatment. This occurred because, for some patients who experienced disease progression after first-line therapy, immunochemotherapy became the standard option during their subsequent treatment course. We agree that tolerability, treatment intensity, and the incidence of adverse events may vary depending on the line of therapy, and this point should be taken into consideration. Third, due to its retrospective, single-center, and non-randomized design, the possibility of selection bias cannot be ruled out. The small sample size may limit generalizability and reduce statistical power. As a result, the CIs for several estimates were wide. Additionally, although the completion rate was lower in the low-BMI group, their PFS appeared numerically longer. The limited duration of follow-up may not sufficiently capture long-term survival outcomes. Nonetheless, multivariate analyses were conducted to adjust for potential confounders. Fourth, the endpoint of completing four cycles may have reflected not only treatment-related toxicities but also early progressive disease and differences in institutional treatment practices. Further prospective validation, geriatric-oncology pathways, and trials of nutritional/sarcopenia interventions targeting treatment completion are warranted.

Conclusions

To conclude, low BMI and ECOG-PS ≥2 were associated with lower completion of induction immunochemotherapy; survival and ≥G3 AE rates did not differ significantly in elderly patients with ES-SCLC. These findings underscore the importance of incorporating geriatric assessments into treatment planning for this population.

Acknowledgments

We sincerely thank the patients, their families, and all investigators who participated in this study. We would like to thank Editage (www.editage.jp) for English language editing. A portion of this research was presented as an abstract at ESMO Asia 2024, and the associated abstract was published accordingly.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-1058/rc

Data Sharing Statement: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-1058/dss

Peer Review File: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-1058/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-1058/coif). Y.T., S.T., T.T., Y.K., and K.H. received honoraria from AstraZeneca and Chugai Pharmaceutical. S.N. received grants from Chugai Pharmaceutical and honoraria from AstraZeneca and Chugai Pharmaceutical. A.M. and K.K. received honoraria from AstraZeneca. M.S. received grants and honoraria from AstraZeneca and Chugai Pharmaceutical. The other 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 study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study received ethical approval from the Institutional Review Board of the Graduate School of Medicine, Nippon Medical School (No. B-2023-768). The requirement for informed consent was waived because of the retrospective nature of the study; however, an opt-out option was provided.

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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