Liu XJ, Ge H, Yuan CL. Survival benefits of concurrent immune checkpoint inhibitor and radiotherapy in non-small cell lung cancer with brain metastases. World J Clin Oncol 2025; 16(8): 107009 [DOI: 10.5306/wjco.v16.i8.107009]
Corresponding Author of This Article
Chun-Luan Yuan, Department of Oncology, The First People’s Hospital of Lianyungang, No. 6 Zhenhua Road, Lianyungang 222016, Jiangsu Province, China. zhaoqin0909@sina.com
Research Domain of This Article
Oncology
Article-Type of This Article
Retrospective Study
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Co-corresponding authors: Heng Ge and Chun-Luan Yuan.
Author contributions: Liu XJ and Yuan CL participated in the conception and design of the study, wrote the manuscript, accessed and verified the study data; Liu XJ, Ge H, and Yuan CL were involved in the acquisition, analysis, and interpretation of data; Ge H and Yuan CL made equal contributions as co-corresponding authors. All authors critically reviewed and approved the final manuscript to be published.
Institutional review board statement: The present study was approved by the Research Ethics Committee of the First People’s Hospital of Lianyungang, No. 202308225.
Informed consent statement: Informed consent statement was finished prior to anticancer therapy.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
Data sharing statement: Not applicable.
Open Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Chun-Luan Yuan, Department of Oncology, The First People’s Hospital of Lianyungang, No. 6 Zhenhua Road, Lianyungang 222016, Jiangsu Province, China. zhaoqin0909@sina.com
Received: March 14, 2025 Revised: May 7, 2025 Accepted: June 26, 2025 Published online: August 24, 2025 Processing time: 159 Days and 21 Hours
Abstract
BACKGROUND
The optimal sequencing of immune checkpoint inhibitor (ICI) and brain radiotherapy in the management of brain metastasis from non-small cell lung cancer (NSCLC) is unclear.
AIM
To evaluate the survival of concurrent ICI and consolidation ICI in NSCLC patients treated with brain radiotherapy.
METHODS
We retrospectively analyzed NSCLC patients treated with brain radiotherapy and ICI. Treatment response and survival were estimated. The cox proportional hazards regression model was utilized to investigate the association between overall survival and clinical variables.
RESULTS
There were 54 patients in concurrent ICI and radiotherapy group, and 62 individuals treated with radiotherapy followed by consolidation ICI. The objective response rates were similar between the two group. The median progression free survival was significantly high in the concurrent ICI group compared with consolidation ICI group (9.56 months vs 8.15 months, P = 0.038). In addition, the median overall survival was 22.08 months in the concurrent ICI group, clearly longer than that in the consolidation group (13.24 months, P = 0.009).
CONCLUSION
In NSCLC patients with brain metastases, our analyses suggested that radiotherapy concurrent with ICI was associated with significant benefit compared with radiotherapy followed by consolidation ICI.
Core Tip: Immunotherapy can combine with radiotherapy to destroy cancer, either use radiotherapy and immunotherapy at the same time, or treated with radiotherapy first and then use immunotherapy. However, what is the better sequence of radiotherapy and immunotherapy for non-small cell lung cancer patients with brain metastasis? In the present study, we collected the data of non-small cell lung cancer patients with brain metastasis, we found some patients received radiotherapy at first, and then treated with immunotherapy. Those patients did not live as long as patients treated with radiotherapy and immunotherapy at the same time.
Citation: Liu XJ, Ge H, Yuan CL. Survival benefits of concurrent immune checkpoint inhibitor and radiotherapy in non-small cell lung cancer with brain metastases. World J Clin Oncol 2025; 16(8): 107009
Lung cancer is the most common malignant cancer across the world[1]. Approximately 80% to 85% of lung tumors fall into the histological category of non-small cell lung cancer (NSCLC), and the most prevalent types of NSCLC are adenocarcinoma and squamous cell carcinoma[2]. It has been reported that about 10% of newly diagnosed patients with advanced NSCLC present with brain metastases at first diagnosis[3-5]. For stage III NSCLC patients received antitumor treatment, about 15% to 33% individuals will develop brain metastases thereafter[6].
The brain blood barrier is a highly regulated vascular system and play a key role in maintaining homeostasis of the central nervous system. Due to the existence of blood brain barrier, it is difficult to deliver anticancer drugs to the brain metastases[7]. For several decades, surgical resection and radiotherapy are the primary treatment modalities for the metastatic brain tumors. Over the past few years, immunotherapy has been emerged as a novel treatment for advanced NSCLC[8]. Recently, several analyses reported similar treatment efficacy between intracranial metastases and extracranial metastases[9,10]. Notably, radiation effected integrity impairment of the brain blood barrier may increases the permeability of anticancer drugs[11]. Several preclinical studies have demonstrated the synergistic effect between radiotherapy and immune checkpoint inhibitor (ICI) because of both local and systemic immunomodulatory effects triggered by irradiation[12-14]. Evidence based medicine revealed the combination of brain radiotherapy and ICI exhibited favorable clinical outcomes and acceptable toxicity for NSCLC patient with brain metastases[15].
There are several researches suggested the application of ICI as a maintenance treatment after radiotherapy[16,17], However, others believed ICI could be given concurrently with radiotherapy[18,19]. Although the above evidence strongly advocates in favor of concurrent brain radiotherapy and ICI in patients with brain metastases from NSCLC, the sample sizes were small[20]. To date, the optimal sequence of ICI and brain radiotherapy remains unknown. In the current study, we explored the survival between concurrent ICI and consolidation ICI of advanced NSCLC patients treated with brain radiotherapy.
MATERIALS AND METHODS
Study design and participants
Medical records of NSCLC patients combined with brain metastases were retrospectively analyzed from 2019 to 2021. To assess the eligible patients, the following inclusion criteria were used: Histologically confirmed NSCLC, combined with brain metastases prior to any systemic anticancer therapy, no prior history of other brain malignant tumors, Eastern Cooperative Oncology Group performance status 0-2, treated with ICI and radiotherapy, and a written informed consent was obtained before treatment. The interval between radiotherapy and ICI was less than 6 months. Despite longer intervals may decrease treatment-related toxicities, the optimal duration of ICI and brain radiotherapy remains unclear[21].
Management
According to the size and total number of the brain metastases, several types of radiotherapy regimens were utilized, including whole brain radiotherapy (WBRT), stereotactic radiotherapy and stereotactic radiosurgery (SRS). Based on the report of Radiation Therapy Oncology Group 90-05[22], the prescribed dose was determined. The protocol of WBRT were 30 Gy in 10 fractions and 40 Gy in 20 fractions, the scheme of SRS was 15-22 Gy, the protocol of stereotactic radiotherapy was 24-36 Gy.
Treatment response evaluation and follow up
Treatment response was evaluated by the Immunotherapy Response Assessment for Neuro-Oncology criteria[23]. Safety and toxicities were assessed according to the Common Terminology Criteria Adverse Events 5.0[24]. After the completion of anticancer therapy, patient follow up were conducted every 3 months including clinical examination and medical imaging.
Statistical analysis
Statistical analyses were performed using Graphpad Prism 8.1. The difference between clinical variables were compared using the χ2 test or the Fisher exact test. Treatment response, progression free survival (PFS) and overall survival (OS) was the primary endpoints. Concurrent ICI refers to the administration of brain radiation therapy within 30 days prior to ICI initiation. Consolidation ICI was defined as an immunotherapy agent that is administered following initial brain radiation therapy. PFS was defined from the date of brain radiotherapy to the occurrence of disease progression (either intracranial lesions or extracranial lesions), death or the last follow up. OS refers to the time from initiation of brain radiotherapy to date of death, the last follow up. The Kaplan-Meier methodology and log-rank test was applied to evaluate survival. Both univariate and multivariate cox proportional hazard regression models were utilized to identify potential prognostic factors. We refer to statistically significant as P value less than 0.05.
RESULTS
Patient characteristics
In the 116 patients who were eligible for analysis, relevant clinical information was captured, including age, sex, Eastern Cooperative Oncology Group performance score, smoking history, histology, tumor proportion score, total number of brain metastases, tumor diameters, gene mutation status, first line therapy, and extracranial metastases. The ICIs used in the present analysis including nivolumab, pembrolizumab, durvalumab, atezolizumab, and tislelizumab. Median follow up time was 8.9 months (range, 2.5-36.9 months). Median age of the whole patient population was 65 years (range, 43-87 years). There was no difference of the clinical variables between the two group. Most of the patients received programmed death-1 inhibitor, only 7 (6.0%) patients in the concurrent ICI group and 9 (7.8%) patients in the consolidation group were treated by programmed cell death ligand 1 inhibitor. There were 67 (57.8%) males and 49 (42.2%) females. 54 (46.6%) patients were treated with radiotherapy concurrent with ICI, and 62 (53.4%) patients were treated with radiotherapy followed by consolidation ICI. There were 9 patients in the concurrent ICI group that received dexamethasone (3-5 mg, daily during radiotherapy) for the management of increased intracranial pressure, whereas there were 14 patients in the consolidation ICI group that received dexamethasone (3-5 mg, daily during radiotherapy). The most common extracranial metastatic sites were lungs, liver, bone, and mediastinal lymph nodes. There was no difference for extracranial metastatic lesions between concurrent and consolidation ICI groups. The main characteristics of included patients were shown in Table 1.
Table 1 General characteristics of non-small cell lung cancer patients with brain metastases in the concurrent immune checkpoint inhibitor group and consolidation immune checkpoint inhibitor group, n (%).
Characteristic
Concurrent ICI, N = 54
Consolidation ICI, N = 62
P value
Age, years
0.536
≤ 65
17 (31.5)
26 (41.9)
> 65
37 (68.5)
36 (58.1)
Sex
0.492
Male
33 (61.1)
34 (54.8)
Female
21 (38.9)
28 (45.2)
ECOG
0.735
0-1
12 (22.2)
17 (27.4)
2
42 (77.8)
45 (72.6)
Smoking
0.598
Yes
36 (66.7)
27 (43.5)
No
18 (33.3)
35 (56.5)
Histology
0.727
Squamous cell carcinoma
9 (16.7)
14 (22.6)
Adenocarcinoma
40 (74.1)
45 (72.6)
Other types
5 (9.3)
3 (4.8)
Tumor proportion score, %
0.712
≤ 1
19 (35.2)
20 (32.3)
1-49
8 (14.8)
6 (9.7)
≥ 50
15 (27.8)
22 (35.4)
Unknown
12 (22.2)
14 (22.6)
Number of brain metastases
0.421
≤ 3
43 (79.6)
44 (71.0)
> 3
11 (20.4)
18 (29.0)
Tumor diameters, mm
0.335
≤ 20
38 (70.4)
47 (75.8)
> 20
16 (29.6)
15 (24.2)
KRAS mutation
0.256
Positive
5 (9.3)
9 (14.5)
Wild type
49 (90.7)
53 (85.5)
TP53 mutation
0.398
Positive
7 (13.0)
8 (12.9)
Wild type
47 (87.0)
54 (87.1)
First line therapy
0.864
Yes
38 (70.4)
46 (74.2)
No
16 (29.6)
16 (25.8)
Extracranial metastases
0.710
Yes
33 (61.1)
35 (56.5)
No
21 (38.9)
27 (43.5)
Treatment efficacy and survival analysis
Treatment response were shown in Table 2. The objective response rates in the concurrent ICI group and the consolidation ICI group were 66.7% and 59.7%, respectively (P = 0.389). There were 86 death at the end of follow up. The median PFS was 9.56 months [95% confidence interval (CI): 2.6-36.5 months] and 8.15 months (95%CI: 2.5-22.5 months) in the concurrent ICI group and the consolidation ICI group, respectively, [hazard ratio = 0.645 (95%CI: 0.422-0.987), P = 0.038] (Figure 1A). OS analysis also suggests that concurrent radiotherapy and ICI group (median OS: 11.8 months) had an improved outcome compared with radiotherapy followed by ICI cohort (median OS: 22.3 months) [hazard ratio = 0.599 (95%CI: 0.347-1.036), P = 0.009] (Figure 1B).
Treatment-related adverse events (AEs) included skin lesions, pneumonitis, hepatic injury, upper gastrointestinal discomfort, lower gastrointestinal symptoms, renal injury, cardiac impairment, hyperthyroidism, hypothyroidism, and brain necrosis. There was insignificant difference in AEs between concurrent ICI group and consolidation ICI group. ICI was suspended in 5 patients (3.7% in the concurrent ICI group vs 4.8% in the consolidation ICI group), 2 patient displayed severe immune pneumonitis (1.9% in the concurrent ICI group vs 1.6% in the consolidation ICI group), 1 patient in concurrent ICI group exhibited immune hepatitis, 1 patient in consolidation ICI group showed abnormal renal function, 1 patient in concurrent ICI had abnormal thyroid function and 1 patient in concurrent ICI showed exfoliative dermatitis of the whole body. Moreover, a total of 15 (12.9%) patients were associated with treatment related necrosis in the brain after receiving combination therapy, and there was no significant difference between the two group (11.1% in the concurrent ICI group vs 14.5% in the consolidation ICI group).
Multivariate analyses for prognostic factors
The prognostic factors of eligible patients were exhibited in Table 3. The univariate analysis revealed less brain metastases, not receive first line therapy, and no extracranial metastases were associated with better OS. In addition, we performed multivariate analyses to determine the independent prognostic factors of PFS. Our results indicated more brain metastases, receive first line therapy, and extracranial metastases were correlated with poor OS.
Table 3 Cox proportional hazards regression for overall survival.
Variable
Univariate analysis
Multivariate analysis
HR (95%CI)
P value
HR (95%CI)
P value
Age (> 65 vs ≤ 65)
0.871 (0.575-1.325)
0.423
Sex (male vs female)
0.908 (0.599-1.218)
0.278
Smoking (yes vs no)
1.071 (0.764-1.595)
0.649
ECOG (0-1 vs 2)
2.402 (0.752-7.675)
0.139
Number of brain metastases (≤ 3 vs > 3)
0.357 (0.264-0.795)
0.009
0.407 (0.299-0.857)
0.011
Tumor diameters (≤ 20 mm vs > 20 mm)
1.142 (0.752-1.675)
0.339
KRAS mutation (positive vs wild type)
0.432 (0.258-1.113)
0.405
TP53 mutation (positive vs wild type)
1.489 (1.096-2.021)
0.081
First line therapy (yes vs no)
0.612 (0.434-1.019)
0.003
0.658 (0.491-1.134)
0.025
ICI (concurrent vs consolidation)
0.385 (0.347-1.036)
0.009
0.432 (0.386-1.097)
0.007
Extracranial metastases (yes vs no)
1.601 (1.242-1.979)
0.014
1.844 (0.299-2.189)
0.036
DISCUSSION
The present study demonstrated that the sequence of ICI and radiotherapy is essential for prognosis. Our data showed that concurrent radiotherapy and ICI is superior to radiotherapy followed by ICI in NSCLC patients combined with brain metastases. Additionally, objective response rate and treatment related toxicity are similar between the two group. Radiotherapy is a component of the standard of care for metastasis brain tumors; brain radiotherapy is associated with clinical benefits including shrink the cancer and alleviate cancer related symptoms[25]. Moreover, radiotherapy can impair the integrity of the blood brain barrier by inducing damages in the endothelium of intracerebral vessels, changes in morphological structures and surrounding astrocytes[11]. Previous studies reported that radiotherapy was able to stimulate antigen present, cytokine release, and immune cell infiltration, these may involved in modulating treatment response[26-28]. Therefore, the combination of radiotherapy and other anticancer therapy was a promising strategy for metastases brain tumors. In the present analysis, combined treatment was applied and the efficacy of radiotherapy has been improved.
ICI has been recognized as a revolutionary breakthrough in the field of cancer treatment. Immunotherapy was associated with long-term survival benefits and has become the standard of care in advanced NSCLC, benefits for these medications were also observed even in brain metastases tumors[10]. Chajon et al[28] revealed a synergistic effect between radiotherapy and immunotherapy, and a beneficial to patient survival has also been observed. In animal model, radiotherapy is critical to recruiting immune cells to the tumor site and to optimizing the effects of ICI. The combined strategy could bridge the blood brain barrier and reverses immune suppression of both the tumor and surrounding microenvironment[29,30].
The optimal sequence of radiotherapy and immunotherapy was under investigation, the ideal strategy depends on patient-specific factors, tumor biology, and treatment goals. A group from United States studied 17 patients with brain metastases and 49 metastatic lesions who received brain radiotherapy combined with immunotherapy, they found that combined therapy or brain radiotherapy before immunotherapy had better control of local lesions[31]. In the meantime, simultaneous immunotherapy and brain radiotherapy can also reduce the local recurrence of NSCLC brain metastases and the number of new brain metastases[32]. Kiess et al[19] found that patients survival rate of SRS treatment before immunotherapy and simultaneous treatments was significantly higher than patients who received induction immunotherapy first (36%, 31%, 8%). In terms of the survival for intracranial lesions, we found that concurrent ICI group was superior to radiotherapy followed by ICI group for brain metastases. However, while concurrent administration of radiotherapy and ICIs appears to be more effective based on current retrospective studies, the “optimal” sequence is not one-size-fits-all. Ongoing trials (e.g., Atezo-Brain) will refine these strategies, emphasizing personalized approaches based on biomarkers and radiation techniques, further prospective trials are needed to establish the optimal sequence and timing of these treatments in patients with NSCLC and brain metastasis. Furthermore, the specific interval and sequence of combination therapy have not yet been defined, this need to be explored in further analysis.
Researches focused on the treatment-related brain necrosis of ICI and radiotherapy in NSCLC with brain metastases were rare. Shepard reported the incidence of treatment-related brain necrosis in combination with immunotherapy and SRS was similar to SRS alone (5.9% vs 2.9%) in NSCLC cancer patients with brain metastases[33]. Consistently, another study by Hubbeling et al[34] showed there was no difference of radiation necrosis between SRS combined with ICI and SRS only. Interestingly, for patients treated with WBRT, there was no radiation necrosis occurred. In the current study, the total incidence of brain necrosis was 12.9%. Indeed, several retrospective studies of melanoma patients with brain metastases treated by immunotherapy plus SRS also found that the risk of radiation induced brain necrosis could be increased by immunotherapy[35,36]. Considering the intrinsic difference of the sensitivity to ICI and/or radiotherapy between NSCLC and melanoma, the treatment-related brain necrosis after ICI and radiotherapy should be further explored. Overall, careful consideration should be given when treating brain metastases patients with programmed death-1/programmed cell death ligand 1 inhibitors combined with SRS. Likewise, other common AEs, such as immune-related pneumonia, hepatitis, nephritis, myocarditis should be monitored.
Despite our study suggested a favor of concurrent radiotherapy and ICI for NSCLC patients with brain metastases, there were several limitations need to be address. First, this is a single center analysis with a relatively small sample size. Second, the radiation protocols are relatively uniform. Third, detailed grades of AEs were ineligible for the included patients. Besides, potential mechanistic rationale underlying the therapeutic synergy between brain radiotherapy and immunotherapy requires further investigation and refinement. Last, because of the short survival for this malignant disease, long term toxicity was difficult to assess. Therefore, our study is preliminary in nature, its clinical findings should be interpreted with caution. larger groups of patients, alongside a placebo, are needed to confirm the findings.
CONCLUSION
In summary, our results showed the patients with brain metastases showed a favorable survival after concurrent radiotherapy and ICI compared with those treated with radiotherapy followed by consolidation ICI. There was a synergistic effect between radiotherapy and ICI. Future clinical trials based on larger patient cohort are necessary to validate our results.
Footnotes
Provenance and peer review: Invited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Oncology
Country of origin: China
Peer-review report’s classification
Scientific Quality: Grade B, Grade C, Grade D
Novelty: Grade B, Grade C, Grade D
Creativity or Innovation: Grade B, Grade D, Grade D
Scientific Significance: Grade B, Grade B, Grade D
P-Reviewer: Acar C; Pan ZY S-Editor: Wu S L-Editor: A P-Editor: Zhao YQ
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