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Comparison of efficacy and safety of neoadjuvant immunochemotherapy in young and elderly patients with IIA–IIIB non-small-cell lung cancer in real-world practice

BMC Pulmonary Medicine volume 24, Article number: 592 (2024) Cite this article

Abstract

Objective

There is currently no consensus over whether neoadjuvant immunochemotherapy is more effective in young patients than in elderly patients with IIA–IIIB non-small-cell lung cancer (NSCLC). In this study, we compare the efficacy and safety of neoadjuvant immunochemotherapy in young and elderly patients with IIA–IIIB NSCLC.

Methods

This retrospective study consecutively included IIA–IIIB NSCLC patients who received 2–4 cycles preoperative immunochemotherapy at the Department of Thoracic Surgery, the First Affiliated Hospital, Zhejiang University School of Medicine from 2019 to 2022. The 1:1 propensity score match analysis was conducted to balance the confounding factors between the young patient group (< 65 years old) and elderly patient group (≥ 65 years old). The follow-up period would not end until at least 1 year after surgery or patient’s decision to abandon treatment. The primary endpoint was pathological response, while the secondary endpoints were objective response rate (ORR), adverse events (AEs), disease-free survival (DFS) and overall survival (OS).

Results

A total of 179 patients were included in our study: <65 years group (71 patients) and ≥ 65 years group (108 patients). After a 1:1 propensity score matching,132 patients (66 pairs) were analyzed to compare the efficacy and safety between the two groups. The ORR in the young patient group and elderly patient group was 72.7% and 71.2% (P = 1.000), respectively. The incidence of grade 3–4 AEs in the elderly patient group was similar to the young patient group (13.6% vs. 16.7%, P = 0.627). About 62.1% (41/66) in the young patient group and 54.5% (36/66) in the elderly patient group eventually underwent surgery. The rate of major pathological response (MPR) in the young patient group and elderly patient group was 68.3% and 55.6% (P = 0.903), respectively. The rate of pathological complete response (pCR) in the young patient group was significantly higher than that in the elderly patient group (46.3% vs. 22.2%, P = 0.027). The median DFS in the young patient group was not reached and 32.2 months in the elderly patient group (P = 0.071). The 1-year DFS rate, 2-year DFS rate and 3-year DFS rate in the young patient group were 90.2%, 85.4% and 80.5%, with that in the elderly patient group 86.1%, 69.4% and 66.7%. The median OS in the young patient group was 42.4 months and not reached in the elderly patient group (P = 0.067). The 1-year OS rate, 2-year OS rate and 3-year OS rate in the young patient group were 97.6%, 90.2% and 90.2%, with that in the elderly patient group 88.9%, 80.6% and 72.2%.

Conclusions

For IIA–IIIB NSCLC, neoadjuvant immunochemotherapy in young patients can produce a higher percentage of patients with a pCR than in elderly patients. However, the survival benefits and incidence of AEs are similar in young and elderly patients.

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Introduction

Non-small cell lung cancer (NSCLC) is the primary pathological type of lung cancer, accounting for approximately 80-85% [1]. The standard treatment regimen for NSCLC without driver gene mutations is immunotherapy based on programmed cell death ligand 1 (PD-L1)/programmed cell death protein 1 (PD-1) immune checkpoint inhibitors (ICIs) plus chemotherapy. Studies have demonstrated that immunochemotherapy could result in more survival benefits than chemotherapy in patients with stage IIA-IIIB NSCLC. Checkmate-816 and NADIM II studies showed that immunochemotherapy as first-line treatment for patients with IIA-IIIB NSCLC could result in better survival than chemotherapy [2, 3].

In our clinical practice, we have found that the majority of cancer patients are elderly people. The immune system of elderly people is characterized by a decrease in immune surveillance and antigen presentation abilities, an increase in memory lymphocytes and immunosuppressive regulatory T cells, a decrease in the number of lymphocytes capable of exerting anti-tumor effects and a higher risk of developing tumors [4,5,6,7]. Therefore, the response of elderly patient to ICIs may differ from that of young patient, and the clinical benefits and risks of using ICIs in the elderly patient deserve special attention from clinical practitioners. However, there is currently no consensus over whether immunochemotherapy is more effective in young patients than in elderly patients with NSCLC. In addition, although there are many comorbidities and immune system remodeling in elderly patients, there is no clear consensus on whether the elderly population has a higher risk of immunotherapy related adverse events (irAEs).

Until now, there are limited data about the response and toxicity of ICIs in elderly population. Elderly people are commonly thought to be 65 years or older, and many randomized controlled trials have used 65 years as the grouping age. Therefore, we launched this study to compare the efficacy and safety of neoadjuvant immunochemotherapy in young (< 65 years old) and elderly patients (≥ 65 years old) with IIA–IIIB NSCLC.

Methods

Study design and patients

This retrospective real-world study was conducted at the Department of Thoracic Surgery, the First Affiliated Hospital, Zhejiang University School of Medicine. Inclusion criteria of this study were as follows: (I) histopathologically diagnosed IIA-IIIB NSCLC (according to the eighth edition of the AJCC TNM staging [8]); (II) receipt of 2–4 cycles of neoadjuvant immunochemotherapy; (III) Eastern Cooperative Oncology Group (ECOG) performance status of 0 or 1; (IV) complete information at our hospital; (V) no previous anticancer treatment; (VI) no other malignant tumors and (VII) no distant metastases. Included patients were divided into two groups according to age: the young patient group (< 65 years old) and elderly patient group (≥ 65 years old). The 1:1 propensity score match (PSM) was performed using baseline characteristics with significant statistical differences (ECOG performance status and pathology).

This study (Clinical trial number: not applicable) had been approved by the Clinical Research Ethics Committee of the First Affiliated Hospital of Zhejiang University School of Medicine (2021 IIT No. 844) and complied with the Helsinki Declaration (revised in 2013) and Good Clinical Practice Guidelines. We had obtained written informed consent from included patients.

Procedures

The immunotherapy regimen included camrelizumab 200 mg, nivolumab 200 mg, sintilimab 200 mg, tislelizumab 200 mg or pembrolizumab 200 mg. The chemotherapy regimen was comprised of cisplatin (75 mg/m2) or carboplatin (area under the curve [AUC] of the plasma concentration-time curve after a single dose = 5) and albumin-bound paclitaxel (260 mg/m2). Surgical approaches were composed of open radical surgery, video-assisted thoracoscopic surgery (VATS), and robot-assisted thoracoscopic surgery (RATS). And routine lymph node dissection was performed.

Before neoadjuvant therapy and surgery, all patients had undergone systematic examinations (chest computed tomography [CT], endoscopic ultrasound, positron emission tomography [PET]–CT, brain magnetic resonance imaging [MRI] and abdominal ultrasound). During neoadjuvant therapy, chest CT was conducted every 2 cycles. After surgery, imaging evaluations were performed every 1–3 months. The follow-up period would not end until at least 1 year after surgery or patient’s decision to abandon treatment.

Assessments

The primary endpoint was pathological response (pathological complete remission [pCR] and major pathological response [MPR]). We defined MPR as ≤ 10% remaining active cancer cells in the original tumor area, and pCR as no remaining active cancer cells in the original tumor area.

The secondary endpoints were objective response rate (ORR), adverse events (AEs), disease-free survival (DFS) and overall survival (OS). ORR was defined as ≥ 30% reduction in the total diameter of target lesions according to the response evaluation criteria in solid tumor version 1.1 (RECIST 1.1) [9]. The evaluation of AEs was performed on the basis of the Common Terminology Criteria for Adverse Events (CTCAE) version 5.0 [10]. We defined DFS as the time from surgery to disease progression or death, and OS as the time from surgery until death from any cause.

Statistical analysis

We used frequencies(percentages) to express categorical variables, and the chi-square test or Fisher’s exact test was used to compare differences. We adopted median and interquartile range (IQR) to show continuous variables, and the t-test or Wilcoxon test was adopted to compare differences. Kaplan-Meier method was applied to evaluate DFS and OS, and the stratified log-rank test were applied to compare differences. Statistical analyses were performed by R software (version 4.1.2) and GraphPad Prism version 9.0 (GraphPad Software, San Diego, CA, USA) was used to plot. A two-sided P < 0.05 was considered to be significant.

Results

Baseline characteristics

Baseline characteristics were shown in Table 1. A total of 179 patients were included in our study from 2019 to 2022: < 65 years group (n = 71) and ≥ 65 years group (n = 108). There were significant differences among the two groups in ECOG performance status and pathology. After a 1:1 propensity score matching, 132 patients (66 pairs) were analyzed and there were no significant differences among the two groups in sex, ECOG performance status, smoking status, drinking status, diabetes mellitus, hypertension, tumor location, T stage, N stage, clinical stage, pathology, treatment cycle, and immunotherapy regimes.

Table 1 Characteristics at baseline
Full size table

Response to neoadjuvant therapy

As we could see from Fig. 1, whether before or after matching, the maximum diameter of the target lesion was decreased in most patients in the two groups compared to the baseline tumor size, and there was no significant difference in the change of the maximum diameter of target lesion between two groups (P > 0.05). There were no cases of PD in both groups (Fig. 2A and D). Before matching, the ORR in the young patient group and elderly patient group was 71.8% and 71.3% (P = 1.000), respectively. After matching, the ORR in the young patient group was 72.7% and the ORR in the elderly patient group was 71.2% (P = 1.000).

Fig. 1
figure 1

Before matching (n = 179): (A) The percentage change in the maximum diameter of target lesion compared with the baseline tumor size. (B) The change of in the maximum diameter of target lesion before and after neoadjuvant immunochemotherapy in young patients. (C) The change of in the maximum diameter of target lesion before and after neoadjuvant immunochemotherapy in elderly patients. (D) The change of the maximum diameter of target lesion between young patient group and elderly patient group. After matching (n = 132): (E) The percentage change in the maximum diameter of target lesion compared with the baseline tumor size. (F) The change of in the maximum diameter of target lesion before and after neoadjuvant immunochemotherapy in young patients. (G) The change of in the maximum diameter of target lesion before and after neoadjuvant immunochemotherapy in elderly patients. (H) The change of the maximum diameter of target lesion between young patient group and elderly patient group. ns Represents P value > 0.05

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Fig. 2
figure 2

Before matching: The distribution condition of clinical and pathological response: (A) CR/PR/SD, (B) MPR, (C) pCR. After matching: The distribution condition of clinical and pathological response: (D) CR/PR/SD, (E) MPR, (F) pCR. Clinical response included complete response (CR), partial remission (PR), and stable disease (SD). Pathological response included major pathological response (MPR) and pathological complete remission (pCR)

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Adverse events

There were no previously unrecorded AEs in our study. Grade 3–4 AEs of neoadjuvant therapy were summarized in Table 2. Before matching, the incidence of grade 3–4 AEs in the young patient group was 15.5% and 21.3% in the elderly patient group (P = 0.333). After matching, the incidence of grade 3–4 AEs in the young patient group and elderly patient group was 16.7% and 13.6% (P = 0.627), respectively. Whether before or after matching, there were no significant differences in the occurrence of grade 3–4 AEs between the two groups. These AEs were quickly resolved after symptomatic treatment.

Table 2 Grade 3–4 AEs of neoadjuvant therapy
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Surgical outcomes and pathological response

The outcomes of surgery and postoperative complications were summarized in Table 3. Whether before or after matching, no significant differences were observed in the time from first treatment to surgery, surgical approach, surgical method, operation time, blood loss, resection margin, number of lymph node dissections during surgery, pathological grade and ypTNM stage between the two groups. We could see a significant difference in the length of hospital stay (P < 0.05) and elderly patients had a longer hospital stay after surgery compared with young patients. Before matching, the rate of MPR in the young patient group was 71.1% and 56.3% in the elderly patient group (P = 0.115, Fig. 2B). The rate of pCR in the young patient group was 44.4% and 26.6% in the elderly patient group (P = 0.052, Fig. 2C). After matching, the rate of MPR in the young patient group was 69.7% and 68.2% in the elderly patient group (P = 0.250, Fig. 2E). The rate of pCR in the young patient group was significantly higher than in the elderly patient group (46.3% vs. 22.2%, P = 0.027, Fig. 2F). Overall, there were no significant differences in detailed postoperative complications and no perioperative deaths occurred. Before matching, the incidence of postoperative complications in the young patient group was significantly higher than that in the elderly patient group (31.1% vs. 50.0%, P = 0.049). After matching, the incidence of postoperative complications in the young patient group was 34.1% and 50.0% in the elderly patient group (P = 0.159).

Table 3 Surgical outcomes
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Survival

Before matching, the median DFS (Fig. 3A) in the young patient group and elderly patient group was both not reached (hazard ratio [HR], 1.635; 95% confidence interval [CI], 0.705 to 3.792; P = 0.250). The 1-year DFS rate, 2-year DFS rate and 3-year DFS rate in the young patient group were 91.1%, 86.7% and 82.2%, with that in the elderly patient group 84.4%, 75.0% and 73.4%. The median OS (Fig. 3B) in the young patient group was 42.4 months (95% CI, 13.5 to 71.3) and not reached in the elderly patient group (HR, 2.043; 95% CI, 0.734 to 5.687; P = 0.160). The 1-year OS rate, 2-year OS rate and 3-year OS rate in the young patient group were 95.6%, 91.1% and 91.1%, with that in the elderly patient group 92.2%, 82.8% and 78.1%.

Fig. 3
figure 3

Before matching (n = 109): Kaplan Meier curves of DFS (A) and OS (B) between the young patient group and the elderly patient group. After matching (n = 79): Kaplan Meier curves of DFS (C) and OS (D) between the young patient group and the elderly patient group. DFS, disease-free survival; OS, overall survival

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After matching, the median DFS (Fig. 3C) in the young patient group was not reached and 32.2 months (95% CI, NA to NA) in the elderly patient group (HR, 2.254; 95% CI, 0.911 to 5.576; P = 0.071). The 1-year DFS rate, 2-year DFS rate and 3-year DFS rate in the young patient group were 90.2%, 85.4% and 80.5%, with that in the elderly patient group 86.1%, 69.4% and 66.7%. The median OS (Fig. 3D) in the young patient group was 42.4 months (95% CI, 14.8 to 71.4) and not reached in the elderly patient group (HR 2.650; 95% CI, 0.899 to 7.814; P = 0.067). The 1-year OS rate, 2-year OS rate and 3-year OS rate in the young patient group were 97.6%, 90.2% and 90.2%, with that in the elderly patient group 88.9%, 80.6% and 72.2%.

Discussion

Although immunochemotherapy has been shown to be effective and safe for the treatment of NSCLC, the safety and effectiveness of immunochemotherapy in elderly patients have not been clarified. Results of KEYNOTE-407 and KEYNOTE-189 revealed that elderly patients benefited less from immunochemotherapy than young patients after immunochemotherapy [11, 12]. The IMPOWER-150 study found that the benefits of elderly patients were similar to those of young patients after immunochemotherapy [13]. These studies didn’t focus on immunochemotherapy only in elderly patients with NSCLC and just conducted age subgroup analysis. And these studies were generally small sample, and further evidence from real-world studies and clinical studies targeting elderly populations is still needed to support them. Therefore, in our opinion, timely reviewing the effectiveness and safety of immunochemotherapy for elderly NSCLC in the real world is of great significance. And we compared the safety and effectiveness of neoadjuvant immunochemotherapy in young (< 65 years old) and elderly patients (≥ 65 years old) with IIA–IIIB NSCLC in this real-world study.

In our study, we could see a significant difference in the length of hospital stay (P < 0.05) and elderly patients had a longer hospital stay after surgery compared with young patients. This is because elderly people recover slower. And we found that the rate of pCR in the young patient group was significantly higher than in the elderly patient group (46.3% vs. 22.2%, P = 0.027). It could be seen that immunochemotherapy in young patients could produce a higher percentage of patients with a pCR than in elderly patients. The efficacy of immunochemotherapy on tumor regression in young patients is better than that in elderly patients.

In this study, the median DFS in the young patient group was not reached and 32.2 months in the elderly patient group (P = 0.071). The 1-year DFS rate, 2-year DFS rate and 3-year DFS rate in the young patient group were 90.2%, 85.4% and 80.5%, with that in the elderly patient group 86.1%, 69.4% and 66.7%. The median OS in the young patient group was 42.4 months and not reached in the elderly patient group (P = 0.067). The 1-year OS rate, 2-year OS rate and 3-year OS rate in the young patient group were 97.6%, 90.2% and 90.2%, with that in the elderly patient group 88.9%, 80.6% and 72.2%. We could see that the survival benefits were similar in both two groups. This was better than other studies. The CameL study showed that the median DFS of the immunochemotherapy group was 11.3 months among patients aged 65 and above [14]. The CameL-sq study showed that the median DFS of the immunochemotherapy group was 8.5 months among patients aged 65 and above [15]. The NEJ057 study showed that the median OS of the immunochemotherapy group was 20.0 months among patients aged 75 and above [16]. The KEYNOTE-407 study showed found that the median OS of the immunochemotherapy group was 17.1 months among patients aged 65 and above [11]. The KEYNOTE-189 study showed that the median OS of the immunochemotherapy group was 22.0 months among patients aged 65 and above [12].

In this study, all treatment-related AEs were controllable and tolerable. No unexpected or new AEs were found. The incidence of grade 3–4 AEs in the young patient group and elderly patient group was 16.7% and 13.6% (P = 0.627). We could see that the incidence of AEs was also similar in both two groups. This was similar to other studies. The Checkmate-816 study found that the incidence of grade3 and 4 AEs was 40.9% in the immunochemotherapy [2]. The NADIM II study revealed that the incidence of grade 3 and 4 AEs was 19% in the immunochemotherapy [3]. The NEJ057 study showed that the incidence of grade 3 and 4 AEs of immunochemotherapy was 24.3% among patients aged 75 and above [16]. The CheckMate-153 study showed that the incidence of grade 3–4 AEs of immunochemotherapy was 6.0% aged 70 and above [17].

This study has some limitations. Firstly, our study is a retrospective study with a small sample size. Secondly, there is heterogeneity in the selected patients and treatment plans in this study. Therefore, larger scale randomized controlled trials and prospective trials are needed to further validate our results.

In conclusion, neoadjuvant immunochemotherapy for IIA–IIIB elderly NSCLC is effective and safe. Neoadjuvant immunochemotherapy in young patients can produce a higher percentage of patients with a pCR than in elderly patients. However, the survival benefits and incidence of AEs are similar in young and elderly patients.

Data availability

The data of the current study are available from the corresponding author on reasonable request.

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Funding

This research was supported by the National Key Research and Development Program of China (2022YFC2407303); Research Center for Lung Tumor Diagnosis and Treatment of Zhejiang Province (JBZX-202007).

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Author notes

  1. Jiacong Liu, Xuhua Huang and Yuhong Yang contributed equally to this work.

Authors and Affiliations

  1. Department of Thoracic Surgery, the First Affiliated Hospital, Zhejiang University School of Medicine, No. 79 Qingchun Road, Hangzhou, 310003, China

    Jiacong Liu, Xuhua Huang, Yuhong Yang, Wang Lv, Yiqing Wang, Pinghui Xia & Jian Hu

  2. Key Laboratory of Clinical Evaluation Technology for Medical Device of Zhejiang Province, Hangzhou, 310003, China

    Jian Hu

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Contributions

Jiacong Liu (Conceptualization, Data curation, Formal Analysis, Investigation, Visualization, Methodology, Writing - original draft). Xuhua Huang (Conceptualization, Data curation, Investigation, Visualization, Methodology, Writing- review & editing). Yuhong Yang (Conceptualization, Data curation, Formal Analysis, Investigation, Visualization, Methodology, Writing- review & editing). Wang Lv (Conceptualization, Investigation, Visualization, Methodology). Yiqing Wang (Conceptualization, Investigation, Visualization, Methodology). Pinghui Xia (Conceptualization, Investigation, Visualization, Methodology). Jian Hu (Conceptualization, Funding acquisition, Investigation, Resources, Supervision, Validation). All authors contributed to the article and approved the submitted version.

Corresponding authors

Correspondence to Jiacong Liu or Jian Hu.

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Ethical approval

This trial was approved by the Clinical Research Ethics Committee of the First Affiliated Hospital, Zhejiang University School of Medicine (2021 IIT No. 844), and done in accordance with the Declaration of Helsinki (as revised in 2013) and Good Clinical Practice Guidelines. Written informed consent was obtained from patients so that we could acquire and use required information from their medical record in our hospital.

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Liu, J., Huang, X., Yang, Y. et al. Comparison of efficacy and safety of neoadjuvant immunochemotherapy in young and elderly patients with IIA–IIIB non-small-cell lung cancer in real-world practice. BMC Pulm Med 24, 592 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12890-024-03417-8

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BMC Pulmonary Medicine

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