Abstract
Background:
The advent of immunotherapy has significantly revolutionized therapies for advanced esophageal cancer (EC). However, clinical data on combining immune checkpoint inhibitors (ICIs) and radiotherapy (RT) in advanced EC remain insufficient.
Objectives:
This study aimed to evaluate the effectiveness and safety of combining immunotherapy and radiation as a second or subsequent line of treatment for advanced EC.
Design and methods:
We retrospectively analyzed patients with advanced EC who received late-line ICIs and categorized them into two subgroups based on whether they received RT. The differences in survival and adverse events (AEs) were evaluated. Inverse probability of treatment weighting (IPTW) and 1:1 propensity-score matching (PSM) analysis were used to minimize confounding.
Results:
The analysis included data from 131 patients. The median progression-free survival (mPFS) was 9.1 months in the RT group, compared to 4.3 months in the non-radiotherapy (NRT) group (p = 0.0087). The median overall survival (mOS) was 13.5 months in the RT group, which is longer than the 7.3 months in the NRT group (p = 0.014). IPTW and 1:1 PSM analysis also showed that the RT group has longer mOS and mPFS. Among them, a higher biologically effective dose (BED) was associated with better survival than the lower dose group (16.1 months vs 10.2 months, p = 0.048). RT was an independent factor of better overall survival and progression-free survival in multivariable analysis, regardless of whether IPTW was used. For any grade of AE, any grade neutropenia (60.7% vs 41.4%, p = 0.028) and esophagitis (21.3% vs 1.4%, p < 0.001) were more common in the RT group. However, the incidence of grade 3–4 AEs did not differ significantly.
Conclusion:
Adding RT to second-line or later immunotherapy regimens for EC correlates with enhanced survival outcomes and manageable toxicity.
Plain language summary
Radiation therapy is an effective therapy for esophageal cancer that can alleviate patients’ dysphagia symptoms. Our study assessed the efficacy and safety of combination therapy and found that combining radiotherapy and immunotherapy improved progression-free survival and overall survival in advanced EC patients. Toxicity was manageable. Further study needs to explore the best time, appropriate dosage, fraction regimen, and target sites of radiation. In clinical practice, we should select the best course of treatment for each patient while ensuring security, limiting damage to normal tissue, closely monitoring side effects from radiation therapy, and giving patients nutritional support.
Keywords
Introduction
According to GLOBOCAN 2022, esophageal cancer (EC) has emerged as the seventh deadliest tumor globally. 1 For most patients, diagnosis of EC typically occurs in advanced stages. Immunotherapy has become one of the standards of therapy for advanced EC following standard front-line therapy, but its effectiveness remains suboptimal. The median overall survival (mOS) for advanced EC patients is around 6–10 months.2–8 Emerging evidence from clinical trials supports the efficacy of immune checkpoint inhibitors (ICIs) in late-line EC. However, those studies did not include radiotherapy (RT).
RT plays a pivotal role in alleviating dysphagia symptoms and obstructions in EC as a local treatment. Clinical evidence confirms that RT potentiates immunotherapy responses through immune system interactions, generating synergistic anti-tumor activity.9–13 However, the administration of immunotherapy and radiation therapy in thoracic malignancies still poses a considerable risk of toxicity, including pneumonitis, 14 and may produce potential immunosuppressive effects. 11 The use of RT in individuals with advanced EC receiving immunotherapy remains insufficient. We performed a retrospective analysis to assess the efficacy and toxicity of combining immunotherapy and radiation in advanced EC.
Materials and methods
Patient eligibility
Between August 2019 and June 2024, 131 patients who received late-line ICI therapy at West China Hospital were retrospectively analyzed. Clinical information includes patient demographics, tumor features, details of therapy, and treatment history. We identified patients who met the following criteria: (1) histologically or cytologically confirmed EC; (2) received immunotherapy in the second- or later-line therapy; and (3) stage IV. Exclusion criteria were as follows: (1) incomplete clinical records and (2) diagnosis of any other malignancies within the last 5 years. Our retrospective study conforms to the Reporting of Observational Studies in Epidemiology (STROBE) statement 15 (Supplemental Table 1).
Methods and definition
Patients received a median of six cycles of ICIs, with a range of 1–13 cycles. The ICIs used in this study included camrelizumab, nivolumab, pembrolizumab, sintilimab, and tislelizumab. Most ICIs, including camrelizumab, pembrolizumab, sintilimab, and tislelizumab, were administered every 3 weeks at a dose of 200 mg. Nivolumab was administered at a dose of 240 mg every 2 weeks. The RT group included patients who received RT no longer than 6 weeks before or after the first or last immunotherapy treatment, and the non-radiotherapy (NRT) group included those who did not receive RT. Progression-free survival (PFS) was calculated as the period from the start of immunotherapy until progressive disease (PD) or death (whichever occurred first). The period from the beginning of ICIs to the death date was used to calculate the overall survival (OS), and survivors were censored. The response to treatment was assessed using the Response Evaluation Criteria in Solid Tumors (RECIST) version 1.1, and adverse events (AEs) were graded using the NCI Common Terminology Criteria for Adverse Events (CTCAE) version 5.0. All reviews and clinical follow-ups were conducted according to the clinical routine.
Statistical analysis
Categorical variables were compared using chi-squared or Fisher’s exact tests. Ordinal categorical variables were analyzed with Wilcoxon’s rank-sum test. Continuous variables were assessed using Student’s t-test. Survival curves were calculated using the Kaplan–Meier (KM) method, and differences were evaluated with the log-rank test. Follow-up time was calculated using the reverse KM method. Peripheral blood markers included the neutrophil-to-lymphocyte ratio (NLR), lactate dehydrogenase (LDH), and albumin (ALB) prior to first immunotherapy treatment initiation. Patients were stratified into high- and low-NLR groups based on the median NLR value (4.47), while high- and low-LDH groups were determined by the upper limit of normal (ULN) for LDH, and high-ALB and low-ALB groups were defined by the lower limit of normal (LLN) for ALB. Propensity scores were transformed into inverse probability of treatment weighting (IPTW) and propensity-score matching (PSM) for balancing baseline characteristics and weighted survival analysis between the two groups. These variables include age, sex, Eastern Cooperative Oncology Group performance status (ECOG PS), tumor location, lesion length, whether surgery or RT was received as part of front-line treatment, previous lines of therapy, combined therapy, TN stage, metastatic sites, and the number of organs involved. PSM was 1:1 matching without replacement, and the caliper was 0.2 times the standard deviation. Statistical significance was set at p < 0.05. All p values were two-sided. All statistical analyses were done using R version 4.4.2.
Results
Patients’ baseline characteristics
This study included 131 EC patients who met the eligibility criteria (Figure S1). Among the 131 participants, 70 (53.4%) were in the NRT group, while 61 (46.6%) received radiation as part of their treatment (Table 1). After applying IPTW, the baseline characteristics between the two groups became more balanced (Figure S2). Sixty-one patients received radiation at 67 sites, with 6 patients receiving 2 radiation courses. While the majority of radiation sites were metastatic lesions, the most common RT site was metastatic lymph nodes (23, 34.3%), followed by esophagus lesions (15, 22.4%), lung metastases (12, 17.9%), bone metastases (8, 11.9%), liver metastases (5, 7.5%), brain metastases (3, 4.5%), and chest wall metastases (1, 1.5%). The median biologically effective dose10 (BED10) was 59.47 Gy (IQR, 39.00–60.00).
Baseline characteristics of all patients before and after sIPTW analysis.
ECOG PS, Eastern Cooperative Oncology Group performance status; NRT, non-radiotherapy; sIPTW, stable inverse probability of treatment weighting.
Treatment efficacy
Table 2 summarizes the treatment response in each group. The RT group demonstrated significantly superior ORR (29.5% vs 8.6%, p = 0.004) and DCR (82.0% vs 55.7%, p = 0.002) compared to the NRT cohort.
The overall response of all patients before and after sIPTW analysis.
DCR, disease control rate; ORR, objective response rate; PD, progressive disease; PR, partial response; SD, stable disease; sIPTW, stable inverse probability of treatment weighting.
Survival
The overall median follow-up time reached 33.1 months (95% confidence interval (CI), 29.4–45.5) by the data cutoff. Cohort-specific follow-up was 33.1 months for the RT group and 29.4 months for the NRT group. The overall median progression-free survival (mPFS) was 5.4 months (95% CI 4.8–7.4), and the overall mOS was 11.4 months (95% CI 9.3–13.0). By contrast, mPFS was only 4.3 months (95% CI 2.8–5.8) in the NRT group, compared to 9.1 months (95% CI 6.5–10.7) in the RT group (hazard ratio (HR) = 0.61, 95% CI 0.43–0.89, p = 0.009; Figure 1(a)). In addition, the mOS in the RT group was 13.5 months (95% CI 11.5–18.5), longer than the NRT group’s mOS of 7.3 months (95% CI 6.2–11.8), additional RT significantly prolonged the OS (HR = 0.62, 95% CI 0.43–0.91, p = 0.014; Figure 1(c)). The whole 1-year OS rate was 46.5% (95% CI 38.6–56.1), with the RT group having a higher rate of 59% (95% CI 47.9–72.7) compared to the NRT group’s rate of 35.4% (95% CI 25.4–49.3). Sensitivity analyses were conducted using IPTW. Consistent with the primary results, statistically significant differences persisted after IPTW adjustments (Figure 1(b) and (d)). To further validate the robustness of our findings, PSM analysis with a 1:1 ratio was implemented as a sensitivity assessment, yielding 39 matched patient pairs. The results showed that radiation exhibited prolonged median OS and PFS compared to the NRT group, aligning consistently with both the primary analysis and IPTW analysis (Figure S3).
Kaplan–Meier curves for PFS of primary (a) and sIPTW (b) cohort. Kaplan–Meier curves for OS of primary (c) and sIPTW (d) cohort.
The univariable analysis showed that receiving RT, not having received RT in prior line therapy, and N stage were prognostic variables for PFS (Table 3). The multivariate Cox model considered variants from the univariate analysis (p < 0.1). Results showed that for PFS, only whether they received RT (HR = 0.61, 95% CI 0.42–0.90, p = 0.013) was an independent prognostic factor for PFS. Patients who received RT had better PFS. Before IPTW, lesion length was not independently associated with PFS in multivariable analysis; however, after IPTW adjustment, it emerged as a significant prognostic factor (Supplemental Table 2).
Univariate and multivariate analyses of the progression-free survival and overall survival of all patients.
ECOG PS, Eastern Cooperative Oncology Group performance status.
In the univariate analysis, RT, being female, previous lines of therapy, lesion length, not having received RT in prior lines of therapy, and T stage were prognostic factors for OS. Table 3 summarizes the results. Similarly, we also included variants (p < 0.1) into multivariate analysis, and results showed that patients receiving RT (HR = 0.53, 95% CI 0.35–0.80, p = 0.003) or being female (HR = 0.35, 95% CI 0.15–0.82, p = 0.016) were independently associated with an OS benefit, whereas prior treatment ⩾2 lines (HR = 2.00, 95% CI 1.19–3.35, p = 0.009) increased mortality risk. Lesion length also demonstrated a significant OS impact in IPTW-adjusted OS multivariable analysis, contrasting with non-significance in unweighted models (Supplemental Table 2).
Subsequently, we performed subgroup analyses in the RT group, recording the highest radiation BED10 received by each individual. The cutoff BED10 value was calculated to be 59.47 Gray (Gy). Therefore, we divided the RT group into two sub-groups: the high-BED and low-BED groups, according to BED10 received was greater than or equal to 59.47 Gy. Survival analysis for the two sub-groups revealed that the high-BED group had a better mOS of 16.1 months (95% CI 12.6–20.7), while the low-BED group’s mOS was 10.2 months (95% CI 6.0–18.0; p = 0.048; Figure 2(a)). We also explored the effect of RT on prognosis according to the site of radiation, subgroup analysis revealed comparable survival outcomes between patients receiving RT for primary esophageal lesions versus other metastatic sites (p = 0.12; Figure 2(b)). In addition, according to RT-ICI administration timing, patients receiving RT were further stratified by before versus after ICIs, though no statistically significant intergroup difference emerged (Figure 2(c)). When divided based on whether they received stereotactic body radiotherapy (SBRT) or not, we found no difference in OS between the group that received SBRT and the group that had undergone only conventional fractionated radiotherapy (CFRT; 14.1 months vs 13.5 months, p = 0.62; Figure 2(d)). However, these subgroup analyses can only be taken as suggestive due to the small sample size.
Kaplan–Meier curves for OS of patients in the different subgroups who received RT, radiation dose (a), radiation sites (b), radiation timing (c), and radiation course (d).
In addition, we explored associations between laboratory data (including NLR, LDH, and ALB in pretreatment peripheral blood samples) and prognosis. Notably, lower NLR before immunotherapy was significantly correlated with better OS compared to elevated NLR (12.9 months vs 7.8 months, HR = 0.53, 95% CI 0.36–0.78, p = 0.001, Figure 3(a)). Similarly, serum ALB levels above the LLN also correlated with longer OS (13.0 months vs 9.7 months, HR = 0.68, 95% CI 0.47–0.99, p = 0.044, Figure 3(b)). However, OS did not differ significantly between the elevated LDH (>ULN) and normal LDH (⩽ULN) cohorts (Figure 3(c)).
Kaplan–Meier curves for OS of patients in the different subgroups stratified by NLR (a), ALB (b), and LDH (c).
Safety
Anemia, leukopenia, and neutropenia were the most common AEs (Table 4). The rates of neutropenia of any grade were higher in the RT group (p = 0.028). Esophagitis occurred in 13/61 (21.3%) of the RT group (p < 0.001). While all grades 3–4 AEs showed no significant difference. Notably, three patients in each group had experienced esophageal fistulas. In the RT group, two patients received RT to the primary esophageal lesion, while the third underwent RT to mediastinal lymph nodes. In addition, two individuals in the NRT group who developed esophageal fistulas had also received radiation on esophageal lesions in the past. In the RT group, among the two patients who received RT to the esophageal lesion, one was treated with 50.4 Gy in 28 fractions. Another patient, initially scheduled for 50 Gy in 25 fractions, however, developed a perforation after completing only 15 fractions. The third patient in the RT group experienced perforation following RT of the mediastinal lymph node at 50 Gy in 25 fractions. In the NRT group, two of three patients with fistula had a history of prior RT, both staged as T4 and once treated with 50.4 Gy in 28 fractions. It is noteworthy that all other patients who developed esophageal fistula were staged as T4, but the RT group patient who received lymph node RT. Overall, additional RT may have had adverse effects, but the AEs were manageable.
Adverse events of all patients.
ALT, alanine aminotransferase; AST, aspartate aminotransferase.
Discussion
Immunotherapy has recently become a standard therapeutic and promising option for people with advanced EC. In advanced second-line single-agent immunotherapy, the PFS in the subgroup was 1.6–2.2 months, the OS was 7.2–10.9 months.2–6 In high programmed-death ligand 1 (PD-L1) expression group (which means CPS ⩾10), the mOS was 9.3–10.3 months.3,6 In third-line immunotherapy, the mOS ranged from 6.8 to 10.8 months.7,16 The performance of ICI monotherapy in EC was not ideal, with ORR rates ranging from only 12.6% to 20.3%.2–6 When it comes to safety, the rate of grade 3–5 AEs was 18.2%–55.3%, and all grade AEs were 64%–95.7%.2–6 Overall, ICIs prolonged OS for advanced EC, especially in squamous carcinoma and Asian patients. Nevertheless, there was no statistical change in PFS compared to chemotherapy.
A study 17 comparing ICI monotherapy with ICI combination therapy for advanced EC found that combination therapy brings benefits to the endpoints of PFS and OS. Another retrospective study 18 found that mPFS for advanced EC using immunotherapy was only 4.8 months in patients with second- and late-line therapy. Although combination therapy was linked to better survival, it fell short of our expectations.
RT is a powerful treatment for EC, which can palliate patients’ symptoms of dysphagia, while research has demonstrated that additional RT can bring benefits to survival. 19 Several preclinical and clinical studies explore the interactions between the immune drug and radiation, confirming that RT and ICIs have synergistic effects.20–22
A study found that for advanced EC, high-dose radiation (⩾50.4 Gy) brought survival benefits. 23 Another study also found that for oligometastatic EC, the addition of radiation to the primary and metastases to chemotherapy significantly improved symptoms of dysphagia and PFS, with a trend toward improved OS. 24 A study also came to the same conclusion 25 that radiation improves the survival of elderly oligometastatic esophageal squamous cell carcinoma (ESCC) patients. So, RT was found to improve OS and PFS in EC in the chemotherapy era.
Several retrospective studies assessed the effect of RT on ICIs’ effectiveness.26,27 According to the results of one study, 26 radiation was linked to a superior response to ICI treatment and was an independent predictor for PFS and OS. Another study 27 showed RT improved OS and PFS in both groups, but neither was statistically significant. Exploratory subgroup analysis suggests that patients with localized recurrence may benefit from RT. However, those studies did not separate the different clinical stages and treatment lines and did not explore how radiation dose affected the prognosis. This presumption of combining RT and immunotherapy for advanced EC is currently controversial in the context of ICIs.
A retrospective cohort study 28 also evaluated SBRT in patient with oligometastatic recurrent ESCC, the result showed high local control rate (90.7% at 1 year) with limited toxicity, the median OS is 17.3 months, particularly better in de novo cases and locoregional recurrence, the systemic therapies in this study include ICI, chemotherapy, and molecular targeted therapy. In another study, 29 49 patients with oligometastatic ESCC were treated with second-line camrelizumab combined with chemoradiotherapy after prior immunotherapy and chemotherapy, with a DCR of 75.5% and an ORR of 40.8%. Median PFS and OS in this study were 6.9 and 12.8 months, respectively. Lv et al. 30 retrospectively compared RT combined with chemoimmunotherapy versus chemoimmunotherapy alone as first-line treatment for oligometastatic ESCC, finding that RT significantly improved median PFS and OS. Although our patients were not given first-line immunotherapy, we observed similar results in our study.
Our study showed that those who underwent a BED10 dose of at least 59.47 Gy enjoyed better outcomes statistically, while another study showed that patients had a better prognosis when they were given a total physical dose of ⩾50.4 Gy. 23 In another study, a total physical dose of 30–35 Gy found no improvement in symptoms of dysphagia and OS. 31 It seems that the lowest dose of radiation may be necessary, but using a higher dose of radiation does not always provide a survival benefit and may lead to adverse effects such as perforation or other risky complications. 32 However, the BED10 cutoff value was measured based on the median value of 59.47 Gy in our dataset. The value was data-driven, not predefined, and had no clinical significance. A cautious approach is required. While it is a useful tool for analysis in this study, it may not be applicable in other clinical settings or patient populations. High-dose hypofractionated radiation induces immunogenic cell death and produces a durable response in anti-tumor immunity. 33 While the fraction regimen of conventionally fractionated RT may result in an immune suppressive tumor microenvironment, and the target volume of conventionally fractionated RT may also induce immunosuppression, as tumor-associated immune cells and tumor-draining lymph nodes are frequently included. These sites are crucial for initiating anticancer responses.34–36 However, high-dose hypofractionated radiation can also lead to vascular damage and reduced perfusion. 37 Our study found that OS did not differ statistically significantly between patients who received SBRT or not. Therefore, the optimal dose fraction regimen for RT when combined with immunotherapy remains inconclusive. We also explored the impact of the site and timing of RT on immunotherapy, but due to the limitations of the data sample, we are still unable to determine which treatment pattern is more effective.
Lymphocytes as an important role in antitumor-related immunity, and the NLR is a marker that can be detected in peripheral blood. Researchers have found that a high NLR is a negative predictor for immunotherapy.38,39 Our research has similarly found this trend. PD-L1 is more spatiotemporally intratumor heterogeneous and not suitable for dynamic monitoring, whereas NLR, which serves as a convenient and easily accessible metric to predict the response to ICIs, to some extent. Multiple trials are presently being conducted to determine how well RT with immunotherapy works.
Advanced EC patients are often malnourished, and in our study, we found that higher pre-treatment ALB was correlated with longer OS statistically. Consistent with a retrospective study, 40 which shows that nutritional status is correlated with outcomes in EC patients. Therefore, patients should receive appropriate nutritional support tailored to their specific condition.
Immunotherapy may benefit from RT, but side effects must also be considered. Combination therapy may increase RT-related toxicity or immune-related adverse effects.41,42 A meta-analysis 42 included 14 studies with 863 patients, summarizing prospective studies of combining immunotherapy and radiation in EC. 88.97% of patients had at least one grade treatment-related AE, and the rate of high-grade AEs was 18.48%. However, nine of the studies were neoadjuvant and adjuvant. Integrating findings of these trials and our study, patients with EC tolerate immunotherapy and RT may work well together.
This study also has limitations. There was a potential selection bias due to the small sample size. Furthermore, analysis of predictive biomarkers such as PD-L1 expression could not be performed due to incomplete data. In our study, the RT group is defined as receiving RT from 6 weeks before the first ICI dose to 6 weeks after the last ICI administration. This broad range includes where RT is administered before the initiation of ICI therapy, concurrently, or after ICI treatment. Each of these may produce different immunological responses. Although our subgroup analysis stratified by timing (before vs after ICI) showed no statistically significant differences, the small sample size limits the robustness of these findings. This limitation may also hinder the ability to detect other differences between treatment modalities, such as the fractionation regimen of RT. Due to the retrospective design of our study, which involves second-line and beyond treatments, we find it challenging to differentiate the radiation intention between symptom palliation versus local tumor control. Last, some AEs may be underestimated because they were only collected from medical records.
Overall, the findings of our study confirm that combining immunotherapy and RT may bring survival benefits for advanced EC. Treatment variables such as the fractionation regimen of RT, timing, dose, target volume, and adverse effects may differentially impact the immune system and clinical outcomes. Comprehensive studies with a larger sample size are needed to explore the intricate interaction between RT and ICI therapy. Acquiring more detailed data on these variables will be crucial to optimize therapeutic approaches in the treatment of advanced EC. Moreover, in clinical practice, we should choose the optimal treatment choice for each patient while ensuring maximum safety. Future research should evaluate the timing of combining ICIs with RT, optimize the dose and target volume of RT, consider the effect of lymphatic drainage on immunotherapy, and explore whether different types of RT affect the efficacy and safety of treatment while minimizing the damage to normal tissue. Due to incomplete PD-L1 expression data, we were unable to conduct relevant analyses between PD-L1 expression and clinical outcomes in the current study. In the next phase, future research should explore specific biomarkers or omics profiles to gain a better understanding of how they influence treatment response, to identify subgroups most likely to benefit from combined therapeutic approaches. However, it is crucial to highlight that immunotherapy has a late effect, and thus changes in tumor volume during treatment do not entirely represent the response to treatment.
Conclusion
This retrospective study confirms that RT in the context of advanced second-line or late-line immunotherapy for EC is safe, the addition of radiation is an independent factor for OS and PFS, and it is potentially related to better clinical outcomes. More study is required to explore better modalities.
Supplemental Material
sj-docx-4-tag-10.1177_17562848251371785 – Supplemental material for Improving the efficacy of late-line immunotherapy for advanced esophageal cancer: the addition of local radiotherapy
Supplemental material, sj-docx-4-tag-10.1177_17562848251371785 for Improving the efficacy of late-line immunotherapy for advanced esophageal cancer: the addition of local radiotherapy by Yicong Chen, Yalin He, Xiaojuan Zhou, Ruixuan Yu, Yong Xu, Feng Peng, Bingwen Zou, Lin Zhou, Youling Gong, Jin Wang, Yongsheng Wang, Meijuan Huang, You Lu and Yongmei Liu in Therapeutic Advances in Gastroenterology
Supplemental Material
sj-docx-5-tag-10.1177_17562848251371785 – Supplemental material for Improving the efficacy of late-line immunotherapy for advanced esophageal cancer: the addition of local radiotherapy
Supplemental material, sj-docx-5-tag-10.1177_17562848251371785 for Improving the efficacy of late-line immunotherapy for advanced esophageal cancer: the addition of local radiotherapy by Yicong Chen, Yalin He, Xiaojuan Zhou, Ruixuan Yu, Yong Xu, Feng Peng, Bingwen Zou, Lin Zhou, Youling Gong, Jin Wang, Yongsheng Wang, Meijuan Huang, You Lu and Yongmei Liu in Therapeutic Advances in Gastroenterology
Supplemental Material
sj-tif-3-tag-10.1177_17562848251371785 – Supplemental material for Improving the efficacy of late-line immunotherapy for advanced esophageal cancer: the addition of local radiotherapy
Supplemental material, sj-tif-3-tag-10.1177_17562848251371785 for Improving the efficacy of late-line immunotherapy for advanced esophageal cancer: the addition of local radiotherapy by Yicong Chen, Yalin He, Xiaojuan Zhou, Ruixuan Yu, Yong Xu, Feng Peng, Bingwen Zou, Lin Zhou, Youling Gong, Jin Wang, Yongsheng Wang, Meijuan Huang, You Lu and Yongmei Liu in Therapeutic Advances in Gastroenterology
Supplemental Material
sj-tiff-1-tag-10.1177_17562848251371785 – Supplemental material for Improving the efficacy of late-line immunotherapy for advanced esophageal cancer: the addition of local radiotherapy
Supplemental material, sj-tiff-1-tag-10.1177_17562848251371785 for Improving the efficacy of late-line immunotherapy for advanced esophageal cancer: the addition of local radiotherapy by Yicong Chen, Yalin He, Xiaojuan Zhou, Ruixuan Yu, Yong Xu, Feng Peng, Bingwen Zou, Lin Zhou, Youling Gong, Jin Wang, Yongsheng Wang, Meijuan Huang, You Lu and Yongmei Liu in Therapeutic Advances in Gastroenterology
Supplemental Material
sj-tiff-2-tag-10.1177_17562848251371785 – Supplemental material for Improving the efficacy of late-line immunotherapy for advanced esophageal cancer: the addition of local radiotherapy
Supplemental material, sj-tiff-2-tag-10.1177_17562848251371785 for Improving the efficacy of late-line immunotherapy for advanced esophageal cancer: the addition of local radiotherapy by Yicong Chen, Yalin He, Xiaojuan Zhou, Ruixuan Yu, Yong Xu, Feng Peng, Bingwen Zou, Lin Zhou, Youling Gong, Jin Wang, Yongsheng Wang, Meijuan Huang, You Lu and Yongmei Liu in Therapeutic Advances in Gastroenterology
Footnotes
References
Supplementary Material
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