Open Access

Feasibility and safety of platinum‑doublet therapy in patients with small‑cell lung cancer in the third‑line setting:
A multi‑institutional retrospective study

  • Authors:
    • Takashi Fukushima
    • Tomonori Makiguchi
    • Yusuke Tanaka
    • Kei Chubachi
    • Mina Ishidoya
    • Sachio Suzuki
    • Hisashi Tanaka
    • Kageaki Taima
    • Yukihiro Hasegawa
    • Koichi Okudera
    • Sadatomo Tasaka
  • View Affiliations

  • Published online on: September 1, 2022     https://doi.org/10.3892/ol.2022.13488
  • Article Number: 368
  • Copyright: © Fukushima et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Small‑cell lung cancer (SCLC) is a highly malignant tumor, and no standard third‑line therapy has been established. The present study retrospectively analyzed the efficacy and safety of platinum‑based regimens in patients with third‑line SCLC who received third‑line chemotherapy. The association of regimen type with overall survival (OS) or time to treatment failure (TTF) was evaluated using the Cox hazard proportional method, including well‑known covariates affecting the prognosis of SCLC. TTF and OS analyses were conducted using the Kaplan‑Meier method. The data cutoff date was June 30, 2020. As a result, from January 2015 to August 2019, 111 patients were diagnosed with SCLC, and 37 received third‑line chemotherapy. Subsequently, 15 patients received a platinum‑doublet regimen, and 22 patients received a single‑agent regimen. Only the type of regimen was significantly associated with TTF in univariate analysis (odds ratio, 0.44; 95% confidence interval, 0.20‑0.95; P=0.03). There were no significant factors associated with OS. The median TTF of patients receiving a platinum‑doublet regimen and those receiving a single‑agent regimen were 3.9 and 2.3 months, respectively (P=0.03). The overall response rates of the platinum‑doublet and single‑agent regimens were 20.0 and 4.5%, respectively. Similarly, the disease control rates were 73.3 and 36.4% for platinum‑doublet and single‑agent regimens, respectively. There was a tendency for adverse events (AEs) with any grade to occur more often in platinum‑based regimens compared with in single‑agent regimens. Severe AEs of grade 3 or higher were observed more often in the platinum‑based regimen, especially in myelosuppression. In conclusion, the present study demonstrated the feasibility and safety of platinum‑doublet regimens in patients with SCLC in a third‑line setting (Registration no. 2020‑048. Date of registration, June 5, 2020).

Introduction

Small-cell lung cancer (SCLC) is a highly malignant lung tumor that accounts for 10–15% of all lung cancers (1). It is a poorly differentiated tumor immunohistochemically expresses neuroendocrine markers and is characterized by rapid progression, early metastatic spread, and early response to treatment. In the first-line setting, SCLC is highly sensitive to chemotherapy with or without radiotherapy; however, most patients experience relapse within one year after treatment.

Japanese guidelines recommend platinum-doublet therapy with etoposide (VP-16) or irinotecan (CPT-11) as the first-line treatment for extensive stage SCLC and additional immune checkpoint inhibitors have recently become an option (2,3). However, little progress has been made in treating patients with recurrent diseases. In the second-line setting, the time from the completion of first-line therapy to recurrence is considered a prognostic factor. In cases of recurrence later than 90 days after the first-line treatment, we refer to it as ‘sensitive relapse’ and otherwise as ‘refractory relapse’ (4). For sensitive relapse, the efficacy of some regimens, including single-agent or combined therapies, has been reported. As for single agents, nogitecan (NGT) and amrubicin (AMR) are included (511). Combined chemotherapy consists of cisplatin (CDDP) plus VP-16, CPT-11, or carboplatin (CBDCA) plus VP-16 (1214). AMR is preferred for refractory relapses (9,11,15). However, there is no recommendation for third-line or later treatments. Compared with non-small cell carcinoma (NSCLC), fewer options are available for SCLC. Therefore, we aimed to explore the efficacy of chemotherapy as a third-line treatment.

Patients and methods

Patients diagnosed with SCLC between January 2015 and August 2019 at Hirosaki University Hospital, Aomori Prefectural Central Hospital, and Hirosaki Central Hospital were retrospectively reviewed. All patients were checked for age, sex, stage (limited or extended), date of last observation and survival, time to treatment failure (TTF), performance status (PS), the existence of metastatic brain tumor, hematological and non-hematological toxicities, and timing of relapse after first-line therapy (e.g., sensitive or refractory). TTF was defined as the time from the start of third-line chemotherapy to the date of treatment discontinuation (all-cause death, disease progression, or all-causal treatment discontinuation, including toxicity or aggravation of general condition). In this study, we adopted TTF, not progression-free survival (PFS) time, because patients who were assessed as having progressive disease not by the Response Evaluation Criteria in Solid Tumors (RECIST) but by the definitive deterioration of clinical symptoms or radiological evaluation were included. All data were analyzed with a cut-off date of June 30, 2020. All categorical variables were analyzed using Fisher's exact test. The primary endpoints were overall survival (OS) and TTF. The association between the type of regimen (platinum-doublet or single-agent) and either TTF or OS was examined using the Cox proportional hazards model. Age, sex, stage, PS, the existence of metastatic brain tumor, and manner of relapse were included as covariates. Significant factors were assessed in the univariate analysis. Toxicity was assessed using the National Cancer Institute Common Toxicity Criteria, version 4.0. P-values are considered to be significant if less than 0.05. Statistical analyses were performed using JMP Pro version 15.2. The study was performed according to the protocol approved by the Ethics Committee of the Hirosaki University Graduate School of Medicine (approval number; 2020-048). As this was a retrospective cohort study, the requirement for informed consent was waived. An opt-out option was conducted on the website of each hospital.

Results

Recruitment of patients

Of the 111 patients diagnosed with SCLC between January 2015 and August 2019, 37 received third-line treatment. Fifteen patients received a platinum-doublet regimen, and 22 patients received a single-agent regimen. The patient characteristics are summarized in Table I. No significant differences in age, sex, PS at third-line treatment, disease extent at diagnosis, relapse manner following first-line treatment, the existence of brain metastases, and proportion of patients who could undergo subsequent chemotherapy after third-line treatment failure were found between the two groups. The previous treatments are listed in Table II. As the first-line treatment, VP-16 was the preferred complementary agent for platinum over CPT-11 in our institutions. In the second-line setting, the most commonly used regimen was amrubicin (AMR), followed by CDBCA + paclitaxel (PTX). The third-line treatment regimen is shown in Fig. 1. In the platinum doublet group, CBDCA + VP-16 and CBDCA + PTX accounted for 60 and 40%, respectively. In the single-agent regimen, CPT-11, NGT, AMR, and PTX accounted for 40.9, 40.9, 9.1, and 9.1% of cases, respectively.

Table I.

Comparison of characteristics between two groups.

Table I.

Comparison of characteristics between two groups.

CharacteristicPlatinum-doublet (n=15)Single-agent regimen (n=22)P-value
Age, median (range)64 (46–81)67 (44–82)0.33
Sex (male/female)11/417/51.00
PS (0-1/≥2)12/319/30.67
Manner of relapse
  Sensitive/refractory3/128/140.47
Disease extent
  Limited disease/extensive disease3/125/171.00
Brain metastases, n (%)8 (53)10 (55)0.74
Post treatment, n (%)7 (47)14 (64)0.33

[i] PS, performance status.

Table II.

Previous treatment regimen in the two groups.

Table II.

Previous treatment regimen in the two groups.

RegimenPlatinum-doublet (n=15)Single-agent (n=22)
First line
  Platinum + etoposide919
  Platinum + irinotecan63
Second line
  Carboplatin + etoposide24
  Carboplatin + paclitaxel21
  Amrubicin1117
Evaluating the endpoint

We evaluated the impact of the type of regimen on the endpoint (TTF or OS) using a Cox proportional hazards model, including covariates. In univariate analysis, only the type of regimen (platinum-doublet) was significantly associated with TTF (odds ratio 0.44 (95% confidence interval 0.20-0.95), P=0.03) (Table III). Thus, we did not conduct a multivariate analysis of TTF. We evaluated the association between regimen type and OS. In the univariate analysis, none of the variables were associated with OS. Subsequently, we evaluated the TTF using log-rank tests for the type of regimen. The median TTF was 2.3 and 3.9 months in single-agent and platinum-doublet regimens, respectively (P=0.03) (Fig. 2).

Table III.

Association of variables with TTF or OS using Cox proportional hazard model.

Table III.

Association of variables with TTF or OS using Cox proportional hazard model.

TTFOS


VariableOdds ratioP-valueOdds ratioP-value
Sex (male)0.74 (0.35-1.60)0.461.28 (0.53-3.05)0.56
Age1.01 (0.97-1.05)0.511.02 (1.07-0.97)0.39
Third-line regimen
  Platinum-doublet vs. single-agent0.44 (0.20-0.95)0.031.41 (0.66-3.00)0.36
PS at the start of third-line
  0–1 vs. ≥21.09 (0.44-2.70)0.830.73 (0.21-2.55)0.64
Disease extent
  LD vs. ED0.94 (0.42-2.07)0.870.83 (0.35-1.97)0.66
Manner of relapse
  Sensitive vs. refractory0.98 (0.48-2.00)0.960.65 (0.26-1.62)0.34
Existence of brain metastases
  Yes vs. No1.45 (0.73-2.85)0.281.29 (0.61-2.71)0.49

[i] TTF, time to treatment failure; OS, overall survival; PS, performance status; LD, limited disease; ED, extensive disease.

Efficacy

We also evaluated the efficacy in both groups (Table IV). The platinum-doublet and single-agent regimens' overall response rates (ORR) were 20.0 and 4.5%, respectively. Disease control rates (DCR) were 73.3 and 36.4% for platinum-doublet and single-agent regimens, respectively. In addition, we evaluated the efficacy of the platinum doublet group (Table SI). Six patients received the CBDCA+VP-16 regimen, and nine patients received the CBDCA + PTX regimen. The ORR was 0 and 55.5% in the CBDCA + VP-16 and CBDCA + PTX groups, respectively. The DCRs were 66.7 and 44.4%, respectively.

Table IV.

Best response following third-line treatment.

Table IV.

Best response following third-line treatment.

ResponsePlatinum-doublet regimen, nSingle-agent regimen, n
Complete response00
Partial response31
Stable disease87
Progressive disease414
Response rate, %20.04.5
Disease control rate, %73.336.4
Toxicity

Concerning treatment-related adverse events (TRAEs), most TRAEs of any grade were more frequent in the platinum-doublet group, except for anorexia, febrile neutropenia, and fatigue (Table V). Severe TRAEs, defined as Common Terminology Criteria for Adverse Events (CTCAE) grade 3 or higher regarding myelosuppression, were more frequent in the platinum-doublet group.

Table V.

Adverse events.

Table V.

Adverse events.

Toxicity, n (%)

AllGrade 3≤


Adverse eventPlatinum-doublet regimenSingle-agent regimenPlatinum-doublet regimenSingle-agent regimen
Neutropenia11 (73.3)13 (59.0)4 (26.6)3 (13.6)
Anemia11 (73.3)12 (54.5)8 (53.3)6 (27.2)
Thrombocytopenia10 (66.6)11 (50.0)2 (13.3)1 (4.5)
Febrile neutropenia0 (0)2 (9.0)0 (0)2 (9.0)
Anorexia5 (33.3)13 (59.0)0 (0)2 (9.0)
Fatigue2 (13.3)7 (31.8)0 (0)0 (0)
Constipation6 (40.0)5 (22.7)0 (0)0 (0)
Neuropathy5 (33.3)0 (0)0 (0)0 (0)
Pneumonitis1 (6.6)1 (4.5)1 (6.6)1 (4.5)

Discussion

Most patients with extensive SCLC progress after first-line therapy. The selection of second-line therapy depends on the response to first-line chemotherapy, and the treatment strategy is divided into two types. One is sensitive relapse, and the other is refractory relapse. Generally, sensitive relapse is defined as patients who respond to first-line therapy and relapse more than three months after the completion of first-line chemotherapy. Refractory relapse is defined as relapse within three months (4). This distinction is important because sensitive diseases tend to respond to further systemic therapies, including agents used for first-line chemotherapy. In refractory or recurrent disease, we administer drugs other than those used in first-line therapy (8,16,17). Moreover, there is little evidence supporting the introduction of third-line treatment rather than the best supportive care. There is no recommended drug or combination in the third-line setting or after that. Given that life expectancy is shorter in patients with SCLC than in those with NSCLC, we assumed that platinum-doublet therapy would be admissible in third-line settings. In the second-line setting, a meta-analysis of the efficacy of platinum-doublet chemotherapy has been reported (18). Most reports have demonstrated that platinum-doublet chemotherapy may be superior to single-agent chemotherapy in terms of OS and PFS. For example, in the second-line setting of sensitive relapse, a phase 3 study on the superiority of CBDCA + VP-16 to NGT in terms of PFS has been recently reported (14). In our analysis, the number of patients who could move to third-line therapy was 24% (27/111), which was similar to the number shown in a previous report (19). In the analysis of the association between treatment regimens and TTF or OS, we included the well-known covariates affecting the prognosis for ED-SCLC, among which only treatment regimen was identified as the significant factor affecting TTF. In our analysis, the platinum doublet demonstrated a relatively high efficacy. In a retrospective analysis of third-line chemotherapy for SCLC, the platinum-doublet regimen tended to improve OS (hazard ratio: 0.84, 95% confidence interval: 0.59-1.19) and ORR (P=0.086) (19). In our analysis, platinum-doublet therapy tended to deteriorate OS in contrast to TTF. OS is likely to be affected by some factors, including pre-and post-treatment complications, such as interstitial lung disease. Therefore, we considered that the platinum-doublet regimen might be the first choice for appropriate patients. In the platinum doublet group, the CBDCA + PTX group showed better ORR and DCR. Meanwhile, in the CBDCA+VP-16 group, all patients except for one received a second dose as a re-challenge setting. Although none of the patients responded to CBDCA+VP-16, the DCR was somewhat high. Considering these results, in third-line settings, the platinum-doublet regimen might play a role in disease control even in the re-challenge setting. Notably, the CBDCA + PTX group demonstrated a high ORR and DCR. The CBDCA + PTX group, which accounted for a large proportion of the platinum-doublet group, might have contributed to the better TTF. In the last few years, there have been reports regarding the efficacy of immune checkpoint inhibitors (nivolumab) for previously treated SCLC. Ready et al evaluated patients with SCLC who received nivolumab in the third or later setting in the CheckMate 032 trial. The median PFS and ORR were 1.4 months and 11.9%, respectively (20). Spigel et al evaluated the superiority of nivolumab over chemotherapy for OS in a second-line setting (21). However, they could not demonstrate the superiority of nivolumab in terms of OS. PFS and ORR were 1.4 months and 13.7%, respectively. We assume that the high response rate provided by the platinum-doublet regimen might be important for better outcomes in rapidly growing tumors, such as SCLC. The platinum doublet demonstrated good tolerability in the present study, even in a third-line setting. In the above meta-analysis, some studies demonstrated that grade 3 or 4 neutropenia was observed in more than 70% of patients who received the CBDCA plus VP-16 regimen (18). In contrast, the phase 3 study stated above demonstrated that the incidence of any grade 3 or 4 adverse events was less than 30% in the CBDCA plus VP-16 group (14). In our study, grade 3 or 4 neutropenia was relatively less frequent, and grade 3 or 4 thrombocytopenia was more frequent in the platinum-doublet group. We speculated that neutropenia was less frequent in our study because pegfilgrastim was administered to most patients who received a platinum-doublet regimen as primary prevention. However, in late-line settings, careful attention must be paid to adverse events, including myelosuppression. We might be able to consider the platinum-doublet regimen in a third-line setting when the patients are considered to be in good condition and well tolerated.

Our study had some limitations. First, those who could move onto the third-line therapy were very few, which might have been why well-known covariates affecting the prognosis of SCLC were not significant even in univariate analysis. Second, since the present report was a retrospective analysis, it remains unclear whether a platinum-doublet regimen should be administered to all patients. Third, most patients with ED-SCLC receive platinum-doublet chemotherapy plus anti-PD-L1 as the first-line therapy. Therefore, we must address whether platinum-based chemotherapy is feasible for relapsed disease following platinum-based chemotherapy plus anti-PD-L1.

In conclusion, we have demonstrated the feasibility and safety of platinum-based regimens in patients with SCLC in a third-line setting. The platinum doublet regimen might favor some patients who can access third-line treatment. However, this study was only a small retrospective analysis. Currently, because the standard first-line therapy is platinum-based chemotherapy plus anti-PD-L1, we need to explore the feasibility of platinum-based therapy for patients with relapse following platinum-based chemotherapy plus anti-PD-L1.

Supplementary Material

Supporting Data

Acknowledgements

Not applicable.

Funding

Funding: No funding was received.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Authors' contributions

TF, TM, and HT conceptualized this study. TF, YT, KC, MI, SS, YH and KO obtained data. TF, TM and HS prepared figures and tables. TF, TM, HT, KT and ST designed the study and drafted the manuscript. KT and ST analyzed the data and provided critical revisions. KO and YH confirmed the authenticity of the raw data. All authors contributed to the manuscript revision and have read and approved the final version of the manuscript.

Ethics approval and consent to participate

Ethical approval for the present study was obtained from the Ethics Committee of the Hirosaki University Graduate School of Medicine (approval no. 2020-048). As this was a retrospective cohort study, the requirement for informed consent was waived. Opt-out was carried out on the Hirosaki University Hospital website.

Patient consent for publication

This was a retrospective study. The requirement for informed consent was waived, and an opt-out option was conducted on the website of each hospital.

Competing interests

The authors declare that they have no competing interests.

References

1 

van Meerbeeck JP, Fennell DA and De Ruysscher DK: Small-cell lung cancer. Lancet. 378:1741–1755. 2011. View Article : Google Scholar : PubMed/NCBI

2 

Horn L, Mansfield AS, Szczęsna A, Havel L, Krzakowski M, Hochmair MJ, Huemer F, Losonczy G, Johnson ML, Nishio M, et al: First-line atezolizumab plus chemotherapy in extensive-stage small-cell lung cancer. N Engl J Med. 379:2220–2229. 2018. View Article : Google Scholar : PubMed/NCBI

3 

Paz-Ares L, Dvorkin M, Chen Y, Reinmuth N, Hotta K, Trukhin D, Statsenko G, Hochmair MJ, Özgüroğlu M, Ji JH, et al: Durvalumab plus platinum-etoposide versus platinum-etoposide in first-line treatment of extensive-stage small-cell lung cancer (CASPIAN): A randomised, controlled, open-label, phase 3 trial. Lancet. 394:1929–1939. 2019. View Article : Google Scholar : PubMed/NCBI

4 

Kim YH, Goto K, Yoh K, Niho S, Ohmatsu H, Kubota K, Saijo N and Nishiwaki Y: Performance status and sensitivity to first-line chemotherapy are significant prognostic factors in patients with recurrent small cell lung cancer receiving second-line chemotherapy. Cancer. 113:2518–2523. 2008. View Article : Google Scholar : PubMed/NCBI

5 

O'Brien ME, Ciuleanu TE, Tsekov H, Shparyk Y, Cuceviá B, Juhasz G, Thatcher N, Ross GA, Dane GC and Crofts T: Phase III trial comparing supportive care alone with supportive care with oral topotecan in patients with relapsed small-cell lung cancer. J Clin Oncol. 24:5441–5447. 2006. View Article : Google Scholar : PubMed/NCBI

6 

von Pawel J, Schiller JH, Shepherd FA, Fields SZ, Kleisbauer JP, Chrysson NG, Stewart DJ, Clark PI, Palmer MC, Depierre A, et al: Topotecan versus cyclophosphamide, doxorubicin, and vincristine for the treatment of recurrent small-cell lung cancer. J Clin Oncol. 17:658–667. 1999. View Article : Google Scholar : PubMed/NCBI

7 

Eckardt JR, von Pawel J, Pujol JL, Papai Z, Quoix E, Ardizzoni A, Poulin R, Preston AJ, Dane G and Ross G: Phase III study of oral compared with intravenous topotecan as second-line therapy in small-cell lung cancer. J Clin Oncol. 25:2086–2092. 2007. View Article : Google Scholar : PubMed/NCBI

8 

Jotte R, Conkling P, Reynolds C, Galsky MD, Klein L, Fitzgibbons JF, McNally R, Renschler MF and Oliver JW: Randomized phase II trial of single-agent amrubicin or topotecan as second-line treatment in patients with small-cell lung cancer sensitive to first-line platinum-based chemotherapy. J Clin Oncol. 29:287–293. 2011. View Article : Google Scholar : PubMed/NCBI

9 

von Pawel J, Jotte R, Spigel DR, O'Brien ME, Socinski MA, Mezger J, Steins M, Bosquée L, Bubis J, Nackaerts K, et al: Randomized phase III trial of amrubicin versus topotecan as second-line treatment for patients with small-cell lung cancer. J Clin Oncol. 32:4012–4019. 2014. View Article : Google Scholar : PubMed/NCBI

10 

Inoue A, Sugawara S, Yamazaki K, Maemondo M, Suzuki T, Gomi K, Takanashi S, Inoue C, Inage M, Yokouchi H, et al: Randomized phase II trial comparing amrubicin with topotecan in patients with previously treated small-cell lung cancer: North Japan lung cancer study group trial 0402. J Clin Oncol. 26:5401–5406. 2008. View Article : Google Scholar : PubMed/NCBI

11 

Horita N, Yamamoto M, Sato T, Tsukahara T, Nagakura H, Tashiro K, Shibata Y, Watanabe H, Nagai K, Nakashima K, et al: Amrubicin for relapsed small-cell lung cancer: A systematic review and meta-analysis of 803 patients. Sci Rep. 6:189992016. View Article : Google Scholar : PubMed/NCBI

12 

Goto K, Ohe Y, Shibata T, Seto T, Takahashi T, Nakagawa K, Tanaka H, Takeda K, Nishio M, Mori K, et al: Combined chemotherapy with cisplatin, etoposide, and irinotecan versus topotecan alone as second-line treatment for patients with sensitive relapsed small-cell lung cancer (JCOG0605): A multicentre, open-label, randomised phase 3 trial. Lancet Oncol. 17:1147–1157. 2016. View Article : Google Scholar : PubMed/NCBI

13 

Wakuda K, Miyawaki T, Miyawaki E, Mamesaya N, Kawamura T, Kobayashi H, Omori S, Nakashima K, Ono A, Kenmotsu H, et al: Efficacy of second-line chemotherapy in patients with sensitive relapsed small-cell lung cancer. In Vivo. 33:2229–2234. 2019. View Article : Google Scholar : PubMed/NCBI

14 

Baize N, Monnet I, Greillier L, Geier M, Lena H, Janicot H, Vergnenegre A, Crequit J, Lamy R, Auliac JB, et al: Carboplatin plus etoposide versus topotecan as second-line treatment for patients with sensitive relapsed small-cell lung cancer: An open-label, multicentre, randomised, phase 3 trial. Lancet Oncol. 21:1224–1233. 2020. View Article : Google Scholar : PubMed/NCBI

15 

Murakami H, Yamamoto N, Shibata T, Takeda K, Ichinose Y, Ohe Y, Yamamoto N, Takeda Y, Kudoh S, Atagi S, et al: A single-arm confirmatory study of amrubicin therapy in patients with refractory small-cell lung cancer: Japan clinical oncology group study (JCOG0901). Lung Cancer. 84:67–72. 2014. View Article : Google Scholar : PubMed/NCBI

16 

Ardizzoni A, Hansen H, Dombernowsky P, Gamucci T, Kaplan S, Postmus P, Giaccone G, Schaefer B, Wanders J and Verweij J: Topotecan, a new active drug in the second-line treatment of small-cell lung cancer: A phase II study in patients with refractory and sensitive disease. The European organization for research and treatment of cancer early clinical studies group and new drug development office, and the lung cancer cooperative group. J Clin Oncol. 15:2090–2096. 1997. View Article : Google Scholar : PubMed/NCBI

17 

Kondo R, Watanabe S, Shoji S, Ichikawa K, Abe T, Baba J, Tanaka J, Tsukada H, Terada M, Sato K, et al: A Phase II study of irinotecan for patients with previously treated small-cell lung cancer. Oncology. 94:223–232. 2018. View Article : Google Scholar : PubMed/NCBI

18 

Horiuchi K, Sato T, Kuno T, Takagi H, Hirsch FR, Powell CA and Fukunaga K: Platinum-doublet chemotherapy as second-line treatment for relapsed patients with small-cell lung cancer: A systematic review and meta-analysis. Lung Cancer. 156:59–67. 2021. View Article : Google Scholar : PubMed/NCBI

19 

Saruwatari K, Umemura S, Nomura S, Kirita K, Matsumoto S, Yoh K, Niho S, Ohmatsu H, Ohe Y and Goto K: Prognostic factor analysis in patients with small-cell lung cancer treated with third-line chemotherapy. Clin Lung Cancer. 17:581–587. 2016. View Article : Google Scholar : PubMed/NCBI

20 

Ready N, Farago AF, de Braud F, Atmaca A, Hellmann MD, Schneider JG, Spigel DR, Moreno V, Chau I, Hann CL, et al: Third-line nivolumab monotherapy in recurrent SCLC: CheckMate 032. J Thorac Oncol. 14:237–244. 2019. View Article : Google Scholar : PubMed/NCBI

21 

Spigel DR, Vicente D, Ciuleanu TE, Gettinger S, Peters S, Horn L, Audigier-Valette C, Pardo Aranda N, Juan-Vidal O, Cheng Y, et al: Second-line nivolumab in relapsed small-cell lung cancer: CheckMate 331. Ann Oncol. 32:631–641. 2021. View Article : Google Scholar : PubMed/NCBI

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Fukushima T, Makiguchi T, Tanaka Y, Chubachi K, Ishidoya M, Suzuki S, Tanaka H, Taima K, Hasegawa Y, Okudera K, Okudera K, et al: Feasibility and safety of platinum‑doublet therapy in patients with small‑cell lung cancer in the third‑line setting: <br />A multi‑institutional retrospective study. Oncol Lett 24: 368, 2022.
APA
Fukushima, T., Makiguchi, T., Tanaka, Y., Chubachi, K., Ishidoya, M., Suzuki, S. ... Tasaka, S. (2022). Feasibility and safety of platinum‑doublet therapy in patients with small‑cell lung cancer in the third‑line setting: <br />A multi‑institutional retrospective study. Oncology Letters, 24, 368. https://doi.org/10.3892/ol.2022.13488
MLA
Fukushima, T., Makiguchi, T., Tanaka, Y., Chubachi, K., Ishidoya, M., Suzuki, S., Tanaka, H., Taima, K., Hasegawa, Y., Okudera, K., Tasaka, S."Feasibility and safety of platinum‑doublet therapy in patients with small‑cell lung cancer in the third‑line setting: <br />A multi‑institutional retrospective study". Oncology Letters 24.4 (2022): 368.
Chicago
Fukushima, T., Makiguchi, T., Tanaka, Y., Chubachi, K., Ishidoya, M., Suzuki, S., Tanaka, H., Taima, K., Hasegawa, Y., Okudera, K., Tasaka, S."Feasibility and safety of platinum‑doublet therapy in patients with small‑cell lung cancer in the third‑line setting: <br />A multi‑institutional retrospective study". Oncology Letters 24, no. 4 (2022): 368. https://doi.org/10.3892/ol.2022.13488