Myelopreservation effect of trilaciclib in extensive-stage small cell lung cancer (ES-SCLC): a systematic review and meta-analysis with trial sequential analysis of randomized clinical trials

Introduction

Background

Small cell lung cancer (SCLC), which constitutes 15% of the new lung cancer diagnoses, has long been recognized as one of the most lethal malignancies with a 5-year survival rate below 7% (1-3). Notably, due to the highly aggressive nature of neuroendocrine tumors, over 80% of SCLC patients are diagnosed with advanced or extensive-stage SCLC (ES-SCLC) (4). Traditionally, the management of ES-SCLC has depended on platinum-based chemotherapy regimens developed in the 1980s, etoposide-platinum as an instance, which initially offer significant therapeutic benefits (5). However, the standard chemotherapy regimens are usually associated with significant cytotoxicity, such as chemotherapy-induced myelosuppression (CIM), which adversely affects hematopoietic stem and progenitor cells (HSPCs) in the bone marrow (6).

Addressing myelosuppression has thus become a critical component of ES-SCLC management, with current interventions like the administration of granulocyte colony-stimulating factors (G-CSFs) and erythropoiesis-stimulating agents (ESAs), which are lineage-specific with potential adverse effects and often only initiated upon symptomatic myelosuppression (7,8). In this context, trilaciclib, a cyclin-dependent kinase (CDK) 4/6 inhibitor developed by G1 Therapeutics, was approved by the US Food and Drug Administration (FDA) in February 2021 as a novel therapeutic approach (9). Trilaciclib works by inducing reversible G1 cell cycle arrest in proliferating HSPCs within the bone marrow, thereby shielding these cells from chemotherapy-induced damage (10). Several clinical trials have successfully proved the efficacy and safety of trilaciclib (11-13), with further studies ongoing to solidify its therapeutic profile.

Although trilaciclib has shown a prominent myeloprotective effect in multiple studies, the sample sizes of current trials are generally too small to provide substantial insights into its efficacy and safety profile. This controversy highlights the need for more evidence to fully understand trilaciclib’s long-term effects and potential relationship with clinical outcomes, raising the question of whether previous observations are enough to draw a definite conclusion on the measured outcomes. In this study, we address the issue of limited samples by using trial sequential analysis (TSA) in addition to meta-analysis as a method to confirm the robustness of each outcome.

Rationale and knowledge gap

Despite the promising evidence on trilaciclib’s myeloprotective ability, existing studies are isolated and remain disparate. A comprehensive systematic review and meta-analysis are essential to consolidate these findings and provide robust evidence for clinical decision-making. A recent meta-analysis, which included four randomized controlled trials (RCTs), confirmed the efficacy of trilaciclib as expected. This analysis incorporated three of the four ES-SCLC trials identified in our current study, along with an additional trial focusing on breast cancer patients. However, while this previous meta-analysis was not exclusively limited to ES-SCLC patients, it did not include the most recent phase 3 clinical trial evaluating trilaciclib in ES-SCLC (14). Given the limited trials and studies available due to trilaciclib’s recent market introduction, including only a small number of studies in meta-analysis may lead to misleading conclusions due to random errors (15). Therefore, it is crucial to employ additional methods to assess the stability and reliability of results derived from small sample sizes, thereby further ensuring the robustness of the findings. TSA is an advanced statistical methodology developed to address the limitations of conventional meta-analyses with sparse data. As described by Wetterslev et al. [2008] (16), cumulative meta-analyses are prone to produce spurious significant results (type I errors) because of repeated testing of significance as trial data accumulate. TSA combines cumulative meta-analysis with monitoring boundaries analogous to interim analyses in individual RCTs, thereby controlling type I errors and estimating the required information size (RIS) needed for reliable conclusions. This approach is considered particularly valuable when dealing with few trials or small sample sizes (15). In this study, we introduced TSA method in addition to the meta-analysis in order to access the conclusiveness of the clinical evidence synthesized from RCTs using a meta-analysis.

Objective

Trilaciclib has already demonstrated promising myeloprotection ability in a small number of studies. The purpose of this study is to pool efficacy data from RCTs via meta-analysis, and to uncover potential associated factors and issues. The TSA analysis was applied to assess the reliability of the findings. The results of this study provide further insights for future research. This study was conducted following the Cochrane Handbook for Systematic Reviews of Interventions (17). We present this article in accordance with the PRISMA reporting checklist (18) (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-67/rc).

Methods

Protocol and registration

The study protocol was registered on PROSPERO (registered ID: CRD42024586935).

Search strategy

A comprehensive retrieval of literature was conducted by an experienced investigator with predetermined search terms including “trilaciclib”, “SCLC”, “small cell lung cancer”, “clinic trial”, and etc. (Table 1). The articles published in PubMed, Embase, the Cochrane Library, and ClinicalTrials.gov were searched from inception to July 2024 in both English and Chinese.

Inclusion and exclusion criteria

Inclusion criteria:

• Study design is RCTs;
• Participants are ES-SCLC patients;
• Patients in the intervention group are receiving trilaciclib;
• Patients in the control group are receiving placebo or/and other usual hematopoietic growth factors;
• Study reports contain the outcomes evaluating the efficacy and safety of trilaciclib.

Exclusion criteria:

• Animal experiments;
• Pilot studies and feasibility studies;
• Studies compare the efficacy of trilaciclib and other chemotherapy agents.

Study selection and data extraction

Two experienced researchers independently assessed the studies according to the inclusion and exclusion criteria. Studies were selected for full-text review based on title and abstract screening.

Data from included studies were extracted using an Excel sheet. Any deviation from this approach was resolved by discussion with a third experienced researcher. Extracted data including (I) study basic information (title, first author, year of publication, and phase of clinical trial); (II) study population (age, sample size, detailed description of participants); (III) details of interventions and comparison; and (IV) outcomes.

Outcomes

Given the most concerned clinical outcomes of SCLC patients receiving trilaciclib, which are generally in accordance with the selected studies, the primary outcomes of this study were defined as occurrence of severe neutropenia (SN) in cycle 1, duration of SN (DSN), occurrence of febrile neutropenia (FN), and overall tumor response. Other outcomes, such as evaluation of infectious events, occurrence of hematopoietic growth factors administration, and occurrence of transfusion, were considered as secondary outcomes. It should be noted that synthesis of results for an outcome requires data from at least three individual studies.

Quality and bias assessment

The study applied the Risk of Bias 2 tools recommended by the Cochrane Handbook to evaluate the risk of bias of included studies with two researchers independently reviewed all included studies. Five domains (randomization process, deviation from intended interventions, missing outcome data, measurement of the outcome, and selection of the reported result) with three levels (low risk, some concerns, and high risk) in this tool were used to determine the overall risk of bias. The quality of included studies was assessed by the Grading of Recommendations Assessment, Development and Evaluation (GRADE) Handbook and a Summary of Findings table was prepared according to the Cochrane guideline (19) using GRADEprofiler version 3.6 to report the quality of included studies.

Statistical analysis of meta-analysis

All statistical analyses were performed using Review Manager version 5.4.1. The variables and outcomes of the meta-analysis were evaluated following the guidance of the Cochrane Handbook. The results were displayed using Forest plots. Specifically, dichotomous variables were evaluated using hazard ratios (HRs) and 95% confidence intervals (CIs), and continuous variables were measured using mean differences (MDs) with 95% CIs. Outcome parameters were estimated by application of a random-effect model. Heterogeneity was calculated using Chi-squared and I². Results with an I² greater than 50% were considered with a high potential for heterogeneity.

Statistical analysis of TSA

In this study, TSA was employed to adjust for random errors due to repeated significance testing in the cumulative meta-analysis (20). TSA was conducted using the software TSA version 0.9.5.10 Beta, developed by the Copenhagen Trial Unit. This method was chosen to control type I and type II errors, which can occur due to multiple comparisons in meta-analyses.

The RIS for each outcome was determined using a fixed-effects model, which accounted for the diversity (D²) across studies. The two-sided alpha level was set at 5% with a power at 80%. Relative risk reduction (RRR) was defined as 10%, 20%, or 30% with a comprehensive discussion. In addition, we calculated TSA-adjusted CIs and applied trial sequential monitoring boundaries to evaluate the cumulative evidence for efficacy, harm, or futility.

The TSA analysis results were interpreted based on the relative position of the cumulative Z-curve and the predefined monitoring boundaries. Specifically, the intervention was considered effective if the Z-curve crossed the efficacy boundary while crossing the futility boundary suggested that further studies would be unlikely to change the result. If neither boundary was crossed, the results were considered inconclusive, indicating that more data are needed to draw reliable conclusions.

Results

Study selection and characteristics

A PRISMA flow diagram was illustrated to exhibit our study selection process (Figure 1). A total of 135 records were retrieved by search terms in our initial search. The result included four RCTs focusing on the efficacy and safety of trilaciclib for ES-SCLC patients (NCT02499770, NCT02514447, NCT03041311, and NCT04902885). These four trials are all focusing on the ES-SCLC, with three in global sites and one in China. The patients in intervention groups of these trials are all receiving trilaciclib and chemotherapy agents, especially the complex of platinum.

Figure 1 Flow diagram of systemic review procedure. SCLC, small cell lung cancer.

According to the Risk of Bias tools 2 (Figure 2) and Summary of Finding table (Table 2), the four included trials exhibited low risk of bias across all critical domains, including selection of the reported results, measurement of the outcome, missing outcome data, deviations from intended interventions, and randomization process. This consistent low-risk profile across studies provides strong evidence that our meta-analysis results are not substantially influenced by methodological biases, thereby supporting the internal validity of our pooled estimates. However, due to the small sample size of these trials, the GRADE results of some outcomes are downgraded to Moderate, which means that the obtaining of robust evidence requires more future studies and trials with larger sample sizes.

Figure 2 Risk of bias graph.

Meta and TSA results

According to the meta results of main outcomes, trilaciclib could significantly reduce the occurrence of SN (grade 4) [odds ratio (OR): 0.08; 95% CI: 0.04 to 0.15; I²=3%], shorten the DSN (grade 4) in cycle 1 (MD: −3.19; 95% CI: −3.96 to −2.42; I²=86%) and also reduce the occurrence of FN (OR: 0.22; 95% CI: 0.08 to 0.59; I²=0%) (Figure 3). However, the results of overall tumor response were assessed with Response Evaluation Criteria in Solid Tumors (RECIST) v1.1 did not provide positive results, which may indicate poor relation between trilaciclib and tumor response (Figure 4).

Figure 3 Meta results of main outcomes: part I. (A) Occurrence of SN (grade 4); (B) DSN (grade 4) in cycle 1; (C) occurrence of FN. CI, confidence interval; DSN, duration of severe neutropenia; FN, febrile neutropenia; IV, inverse variance; M-H, Mantel-Haenszel; SD, standard deviation; SN, severe neutropenia.

Figure 4 Meta results of main outcomes: part II (RECIST v1.1). (A) CR; (B) PR; (C) SD; (D) PD; (E) NE; (F) ORR. CI, confidence interval; CR, complete response; M-H, Mantel-Haenszel; NE, not evaluable; ORR, objective response rate; PD, progressive disease; PR, partial response; RECIST, Response Evaluation Criteria in Solid Tumors; SD, stable disease.

The TSA results indicated that the Z-curve for the occurrence and DSN (grade 4) crossed the TSA boundary under all three RRR settings (Figures S1,S2). This suggests that the conclusions regarding to these two outcomes are stable. Meanwhile, the Z-curve for occurrence of the FN stayed below the TSA boundary, indicating that the result is inconclusive (Figure S3).

The secondary outcomes include general safety indicators for trilaciclib, the utilization of traditional treatment for neutropenia, and assessment of infectious events during the chemotherapy (Figure 5). Our results suggest that trilaciclib had no general safety issues due to no difference between intervention and control groups in mortality and adverse events (AEs) outcomes [including severe AEs (SAEs) and other AEs]. Furthermore, our results indicate that the administration of trilaciclib could reduce some utilization of traditional therapies for patients with neutropenia, like G-CSF administration and red blood cell (RBC) transfusion, while having no effect on the occurrence of ESA administration or platelet transfusion. Additionally, the results did not provide positive feedback regarding infection-related parameters, including infectious SAEs, pulmonary infection SAEs, and intravenous (IV) antibiotic administration. This should suggest a weak relationship between trilaciclib administration and infection.

Figure 5 GRADE evidence quality table. *, the basis for the assumed risk (e.g., the median control group risk across studies) is provided in footnotes. The corresponding risk (and its 95% CI) is based on the assumed risk in the comparison group and the relative effect of the intervention (and its 95% CI). ¹, small sample size with wide CIs. ², RR =0.2. ³, small sample size with wider CIs. GRADE Working Group grades of evidence: high quality: further research is very unlikely to change our confidence in the estimate of effect. Moderate quality: further research is likely to have an important impact on our confidence in the estimate of effect and may change the estimate. Low quality: further research is very likely to have an important impact on our confidence in the estimate of effect and is likely to change the estimate. Very low quality: we are very uncertain about the estimate. ⊕, factors that may increase the quality of evidence; ⊝, factors that may decrease the quality of evidence. AE, adverse event; CI, confidence interval; CR, complete response; DSN, duration of severe neutropenia; ESA, erythropoiesis-stimulating agent; FN, febrile neutropenia; G-CSF, granulocyte colony-stimulating factor; GRADE, Grading of Recommendations Assessment, Development and Evaluation; IV, intravenous; NE, not evaluable; OR, odds ratio; ORR, objective response rate; PD, progressive disease; PR, partial response; RBC, red blood cell; RECIST, Response Evaluation Criteria in Solid Tumors; RR, relative risk; SAE, severe adverse event; SCLC, small cell lung cancer; SD, stable disease; SN, severe neutropenia.

Discussion

Trilaciclib has shown good safety and efficacy profiles with high consistency in the limited trials. Therefore, regarding to the small sample size of clinical trials, it is necessary to validate the robustness of the results for the meta-analysis study. To our best knowledge, this is the first systematic review and meta-analysis confirming trilaciclib’s myelosuppression ability for ES-SCLC patients with TSA providing robustness of these results.

CIM is one of the most common side effects of chemotherapy, which result in diminished treatment effect (21). Previous studies reported that patients receiving trilaciclib prior to chemotherapy could get lower occurrence of SN (grade 4) and shorter DSN (grade 4) (13,14,22). Our results also demonstrated major consistency with the previous research. Specifically, the meta-analysis results support trilaciclib’s ability in reducing the occurrence and DSN (grade 4), and the TSA analysis also confirmed the stability of these findings. Together, the result indicates that trilaciclib can protect bone marrow progenitor cells from the deleterious effects of chemotherapy drugs, and the evidence extracted from current studies is sufficient to support the respective efficacy and safety of trilaciclib in ES-SCLC.

Additionally, our study also reveals that the administration of trilaciclib does not significantly improve tumor response metrics such as complete response or partial response rates. This suggests that the protective role of trilaciclib is primarily focused on mitigating the hematologic toxicity associated with chemotherapy rather than directly enhancing the antitumor efficacy of chemotherapeutic agents. This can be supported by the previous mechanistic studies, which demonstrated that trilaciclib benefits SCLC cells through a different replication pathway than CDK 4/6, and that trilaciclib has a minimal effect on the cytotoxicity of chemotherapy agents (23). This insight is crucial for understanding the clinical applications of trilaciclib that its myeloprotective ability does not influence the anticipated anti-tumor effects of chemotherapy drugs.

Furthermore, the previous findings suggested the ability of trilaciclib in reducing the occurrence of severe hematologic toxicities and the need for G-CSF and RBC transfusions. Our meta-analysis result is generally consistent with the previous findings, with TSA result suggests that more evidence is needed to confirm reliability.

Notably, the meta-analysis shows positive results for the occurrence of FN. Although the TSA result indicated that more future studies are required for a definitive conclusion, the result highlights the significance of FN in future research as a potential life-threatening complication, which demonstrated strong relation with common chemotherapies in ES-SCLC patients (24,25). Meanwhile, however, the meta-analysis also indicates that trilaciclib has little effect on preventing infectious complications. Given the complexity of infectious events with limited sample size in clinical trials, our result suggests that additional measurements and larger study population are necessary to clarify the relationship between trilaciclib and infectious complications to access the overall risk factors when using trilaciclib as a chemotherapy adjunct.

There are two potential limitations in our study. Firstly, due to limited number of studies, the measured outcomes in our study might not cover the overall clinical concerns. Some survival outcomes, such as the rate of overall survival and progression-free survival, were excluded due to the insufficient data extracted from studies. Given the high survival pressure of ES-SCLC patients, this relationship may require a relatively large sample size for validation. Besides, trilaciclib is also expanding its applications into other oncological areas. For instance, there’s one phase 2 clinical trial study indicates that trilaciclib administration in breast cancer patients yields significant survival benefits (26). Secondly, the discussion of subgroup analysis was not conducted due to insufficient sample size from available studies. The differences of study countries, phase of trials, and antitumor agents applied for patients might be the source of high heterogeneity for some outcomes, while it requires more studies to confirm the hypothesis.

Conclusions

In summary, our study confirmed the effective role of trilaciclib in reducing the risk of SN in SCLC patients, while having no negative effects on the efficacy of combination chemotherapeutics, with TSA providing robustness to this evidence. In addition, our study suggests that the relationship between trilaciclib and infectious events remains elusive, which requires further research on the mechanisms or larger sample studies.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the PRISMA reporting checklist. Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-67/rc

Peer Review File: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-67/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-2025-67/coif). The 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.

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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