Neoadjuvant chemoimmunotherapy or chemoradiotherapy in stage III non-small cell lung cancer: crossing the Rubicon?

Introduction

Lung cancer is currently the most diagnosed cancer worldwide, with a total of 2.4 million new patients annually (1). It is also the leading cause of cancer-related mortality, with approximately 1.8 million deaths per year due to this disease (2). Non-small cell lung cancer (NSCLC) accounts for 80–85% of lung cancer diagnoses (3). Among these, 20–35% are diagnosed at stage III [tumor-node-metastasis (TNM) 8^th edition] (4). NSCLC stage III is a highly heterogeneous disease that ranges from resectable or potentially resectable stages, which may include stages IIIA and even IIIB, to unresectable stages IIIB or IIIC. The percentage of diagnoses in the different sub-stages depends on the series analyzed (5). For example, in a country like Spain, the percentage of diagnoses is 15.8% in stage IIIA, 11.6% in stage IIIB, and 1% in stage IIIC (6).

The treatment of NSCLC stage III today is controversial due to the introduction of induction therapies with chemoimmunotherapy (CT-IO) (7). Since the publication of the CheckMate-816 clinical trial, which evaluated induction with CT-IO in patients with NSCLC stage IB–III, treatment options for stage III vary (8). Prior to neoadjuvant therapy, the management of unresectable stage IIIA and stages IIIB/C has mainly been based on concurrent chemoradiotherapy (CT/RT) followed by maintenance immunotherapy for 1 year, as demonstrated in the PACIFIC trial (9). In 2022, data from the CheckMate-816 trial were published (8), which randomized patients with NSCLC stage IB–IIIA to receive three cycles of platinum doublet chemotherapy (CT) plus nivolumab vs. CT alone. This study showed significantly superior results compared to induction chemotherapy alone, especially notable in the pathological complete response (pCR) rate, which was 24.0% vs. 2.2%.

However, the main issue with clinical trials involving neoadjuvant and/or perioperative CT-IO is the lack of direct comparison with the current standard treatment, which is CT/RT followed by immunotherapy (Figure 1). The main clinical trials conducted so far have used induction CT as the standard arm, despite some allowing inclusion of stage IIIB patients. Therefore, it is difficult to assess the true role of induction CT-IO in stage III disease. Nonetheless, given current data on induction therapy, it would be feasible and tempting in clinical practice to start treatment with induction CT-IO in initially resectable stage III and subsequently evaluate tumour response as a surrogate biomarker (10). This review aims to assess the role of the two current standard treatments for NSCLC stage III: neoadjuvant CT-IO and CT/RT followed by consolidation immunotherapy. We present this article in accordance with the Narrative Review reporting checklist (available at https://cco.amegroups.com/article/view/10.21037/cco-25-50/rc).

Figure 1 Representation of the two main options for stage III NSCLC. CI, confidence interval; CT, chemotherapy; CT/RT, chemoradiotherapy; NSCLC, non-small cell lung cancer; ORR, overall response rate; pCR, pathologic complete response; PD, progressive disease; PD-1, programmed cell death 1; PD-L1, programmed death-ligand 1.

Methods

The reviews, clinical trials and studies included in this narrative review were found through searching several databases published between 2005 and 2025: PubMed, Cochrane, Science Direct, EMBASE, and the clinical trial registry (www.clinicaltrials.gov). The systematic reviews and meta-analysis included reviewed the main clinical trials with CT and or immunotherapy. Subsequently, existing literature reviews were selected, as well as studies that involved data analysis from different hospitals. Search terms and the rest of strategy summary is detailed in Table S1. It was conducted and carried out using the quality standards of narrative or literature review and current guidelines.

Neoadjuvant CT in NSCLC stage III (prior to immunotherapy)

The role of neoadjuvant CT before surgery in stage III has always been controversial, mainly reserved for stage IIIA. Several clinical trials have evaluated these therapies, demonstrating benefits of induction (11). A meta-analysis by the NSCLC Meta-analysis Collaborative Group in 2014, including 15 clinical trials (at least in stage IIIA-N2), showed a 5% improvement in overall survival (OS), from 40% to 45% (12). These studies observed modest pCR rates with CT (5–11%). While pCR rates were low in the trials included, a critical finding was the profound prognostic value of downstaging in general. Specifically in the sub-group of patients with clinical N2 disease who achieved pCR in nodal disease or downstaging after CT, 5-year OS rates were reported to be in the range of 35–45%.

Despite favourable data from some clinical trials, these studies were highly criticised for multiple factors, the main ones being the high rate of pneumonectomies (high postoperative morbidity and mortality rate) and the poor results in the control arms, which were largely surgery only (13). This led to this therapy being chosen only for very selected stage IIIA patients with single-season N2 involvement, where pneumonectomy was preferably not required. Therefore, for most stage III patients, CT/RT was the therapy of choice.

CT/RT in NSCLC stage III

Treatment of part of stage IIIA and stage IIIB/C has been based on concomitant CT/RT until the initiation of neoadjuvant therapy (14). The initiation of concomitant vs. sequential treatment was made in the 2000s where a series of clinical trials demonstrated that concomitant treatment was superior to sequential CT/RT. The meta-analysis by Aupérin et al. found an improvement in OS rates of 5.7% at 3 years and 4.5% at 3 years for concurrent vs. sequential CT/RT (15). A more recent 2021 meta-analysis published by Wang et al. confirmed these results in terms of both survival and objective response rates (16).

In addition to concomitant CT/RT, two other forms of CT/RT have also been studied, like induction with CT prior to CT/RT and consolidation with CT after CT/RT. The phase 3 clinical trial CALGB 39081 evaluated the addiction of two cycles of CT with carboplatin-paclitaxel prior to CT/RT vs. concomitant CT/RT (17). This failed study had overall OS data of 13 vs. 11 months (not statistically significant difference). CT/RT followed by consolidation CT was studied in the Hoosier Oncology Group phase 3 clinical trial LUN01-24 in patients with NSCLC stage III performing consolidation with docetaxel, randomised to receive concurrent CT/RT with docetaxel or placebo (18). In this study, respectively, OS was 21.5 vs. 24.1 months (P=0.94) with a progression-free survival (PFS) of 12.3 vs. 12.9 months (P=0.93). In addition, increased toxicity was observed in the docetaxel arm mainly based on increased radicular pneumonitis. Based on these studies, concurrent CT/RT without induction or consolidation has been the standard of care since the 2000s for most NSCLC stage III.

Subsequently, in 2017, the results of the PACIFIC clinical trial assessing consolidation after concurrent CT/RT with durvalumab [anti-programmed death-ligand 1 (PD-L1)] for 12 months were published (9). This trial showed a PFS of 16.8 months for the durvalumab arm vs. 5.6 months for the placebo arm [hazard ratio (HR) 0.52, P<0.001]. The grade 3–4 adverse event rate was 29.9% vs. 26.1% respectively. At the 5-year data update the OS was 47.5 vs. 29.1 months [HR 0.72; 95% confidence interval (CI): 0.59–0.89] (19). In this clinical trial 97.6% of the included patients were stage III (stage IIIA 52.9% and IIIB 44.7%, stage IIIC was not included because the 7^th TNM edition did not have this category). Following these data, the standard treatment at that time for unresectable stage IIIA patients and almost all stage IIIB and IIIC patients became concurrent CT/RT followed by immunotherapy for 1 year. The PACIFIC trial also presented certain points of debate, mainly because the reasons for non-resectability were not clearly specified.

Finally, the PACIFIC-6 clinical trial evaluated durvalumab after sequential rather than concomitant CT/RT (20). The study involving 117 patients had as its primary endpoint the safety of durvalumab as a 24-month consolidation therapy after sequential CT/RT. The study was positive in its primary endpoint with efficacy data that make it a potential alternative after sequential CT/RT but without current approval by the Food and Drug Administration (FDA) or European Medicines Agency (EMA).

Neoadjuvant with CT-IO in NSCLC stage III

The initiation of neoadjuvant as a standard treatment option for NSCLC stage III began with the publication of data from the CheckMate-816 clinical trial (8) (Table 1). A total of 358 patients were randomised 1:1 to receive three cycles of CT-nivolumab vs. neoadjuvant CT. Within stage III, only stage IIIA patients were allowed to be included, which accounted for 63.7% (228/358). Overall, event-free survival (EFS) was 31.6 vs. 20.8 months for the CT-nivolumab vs. placebo arm (HR 0.63; P=0.005). In subgroup analysis by stage, in IIIA the EFS was 31.6 vs. 15.7 months (HR 0.54; 95% CI: 0.37–0.80). The pCR was 24.0% vs. 2.2% (odds ratio 13.9; 99% CI: 3.5–55.8), being for stage IIIA 23.0% vs. 0.9% (odds ratio 22.1; 99% CI: 14.3–30.7). The rate of patients alive at 24 months of the study was 82.7% vs. 70.6%. Subsequently, the 3-year data update showed that the pCR in PD-L1-positive tumours was 32.6% vs. 2.2%. In PD-L1 negative tumours it was 16.7% vs. 2.6%. Finally, 5-year OS analysis significantly favored neoadjuvant nivolumab plus CT vs. CT (HR 0.72; 95% CI: 0.52–0.99) with consistency across most subgroups (21).

Two other clinically relevant clinical trials have been published with nivolumab in neoadjuvant and perioperative treatment (NADIM II and CheckMate 77T) (22,23). Both studies had similar characteristics allowing for the inclusion of stage IIIA and IIIB. Both trials were positive for their primary endpoints, pCR in NADIM II and EFS in CheckMate 77T. The main difference between the two trials, apart from the number of patients, was the adjuvant treatment time, which was 6 months for NADIM II and 12 months for CheckMate 77T. In addition, neoadjuvant was with three cycles in NADIM II and four cycles in CheckMate 77T, with a design very similar to the KEYNOTE-671.

Pembrolizumab was evaluated in the KEYNOTE-671 trial as perioperative therapy which included 4 cycles of neoadjuvant and 13 cycles of adjuvant therapy (24). An important feature of the trial was its dual primary endpoint of EFS and OS. The percentage of patients with stage IIIA was 55.5% (442/797) and IIIB 14.6% (116/797). Median EFS was not achieved in the Pembrolizumab arm vs. 17 months in the placebo arm (HR 0.57, P<0.001). Median OS was not achieved in the Pembrolizumab arm vs. 45.5 months (P=0.02). At EFS the benefit was greater in stage III than in stage II (HR 0.54 vs. 0.65).

Other immunotherapy drugs have been evaluated in neoadjuvant such as durvalumab (AEGEAN) (25), toripalimab (Neotorch) (26), tislelizumab (RATIONALE 315) (27) or camrelizumab (TD-FOREKNOW) (28). The first three studies assessed perioperative neoadjuvant, and the last one was a randomised phase 2 trial with similar characteristics to CheckMate 816. All studies were positive for their primary endpoints and demonstrated the efficacy of induction with CT-IO in NSCLC stage III. The main differences between the clinical trials were the inclusion criteria for staging. The RATIONALE 315 study was the only one of the four that did not allow inclusion of stage IIIB patients, with the percentage of stage IIIA patients being 58.5% (265/453). The AEGEAN study had a similar protocol to KEYNOTE-671 in both treatment and patient profile, although with a higher percentage of stage IIIB patients (25.1%). Finally, the Neotorch and TD-FOREKNOW studies only studied neoadjuvant stage III, with a percentage of stage IIIB of 31.9% (129/404) and 25% (22/88) respectively.

Neoadjuvant CT-IO or CT/RT?

Several factors should be considered when assessing neoadjuvant in a patient with NSCLC stage III. The first factor to consider is that clinical trials in neoadjuvant have been conducted with different TNM. For example, the CheckMate 816 clinical trial was conducted with the 7^th edition and KEYNOTE-671 with the 8^th edition (29,30). Another factor is that the clinical trials mainly included stage IIIA, with much lower percentages for IIIB. Finally, the designs evaluated neoadjuvant therapy with very different post-surgery adjuvant therapies, and it is unknown whether this is necessary after surgery, especially in cases with pCR.

One of the above issues is addressed in the TNM 9^th edition (31). The new lung cancer staging differentiates between different N2 lymph node involvement, with N2a or N2b depending on single or multiple mediastinal or subcarinal positivity. Thus, in patients with N2a involvement, except in the case of T4, the staging is IIB or IIIA. Conversely, N2b involvement makes the tumour IIIB except in T1, which is IIIA.

Is not possible in all perspectives of a clinical trial (patient profile, efficacy or safety) to compare between CT/RT studies, like PACIFIC, and neoadjuvant studies. However, from an overall perspective in clinical practice, neoadjuvant has several advantages over CT/RT that make this treatment more attractive. The most important is the prospect of dual local treatment, with the possibility of treatment with radiotherapy (RT) or CT/RT after induction if there is no surgical option after induction or if pneumonectomy is required. The second advantage is that the pathological response can be obtained, which allows the patient’s prognosis to be clearly marked, and the question of what to do with patients with pCR (no adjuvant, whether for 6 or 12 months) will probably be resolved in the future. Furthermore, neoadjuvant is carried out with well-known and well-tolerated treatment regimens and increasingly less invasive surgery, making it a treatment with a very favourable safety profile (32,33).

Possibly the main clinical disadvantage is that in the absence of response to neoadjuvant treatment or in case of toxicity limiting surgery such as pneumonitis, subsequent treatment would be suboptimal RT or CT/RT. Based on the data from the different clinical trials and the expert consensus and clinical guidelines, it seems clear that the treatment of stage IIIA can be based on neoadjuvant, with the exception of T4 in which, with few exceptions, CT/RT seems a more feasible option due to the difficulties of surgery in T4. More doubtful could be T1–2N2b (IIIA) in which the option of neoadjuvant seems a more attractive option due to the local treatment options that could be provided later with RT, where the treatment fields may not be very high given the T1–2 (34).

In the case of stage IIIB there are also established data on the efficacy of neoadjuvant treatment in these tumours and given the advantages it is likely that treatment of stage IIIB (T1–3N2b) in most cases will be with induction. N2b nodal involvement should not be an impediment to considering the most radical options possible given the change in the natural history of NSCLC stage III that is occurring (35). Moreover, this is probably more important in those PD-L1 negative cases where the different neoadjuvant clinical trials have demonstrated efficacy regardless of this biomarker, whereas with the 5-year OS in the PACIFIC study being negative for PD-L1 negative (HR 1.15; 95% CI: 0.75–1.75) (19). For this reason, EMA gave positive approval for durvalumab only in PD-L1 ≥1% in tumour cells (36).

Neoadjuvant CT-IO in stage IIIC

The standard treatment in this clinical scenario is CT/RT followed by durvalumab. However, despite the lack of data and evidence both in clinical trials and in the literature on the possibilities of induction, the possibility of patient selection for neoadjuvant treatment in stage IIIC is tempting. A recent study that could play an interesting role in the future and is the phase 2 trial KEYNOTE-799 (37). In this study, which included patients with stage IIIA–C, it evaluated induction CT-IO with one cycle followed by CT-IO plus concurrent RT and subsequent consolidation with immunotherapy for up to 17 cycles. The OS of the non-squamous cohort was 56.7 months with a PFS of 45.3 months. The percentage of patients alive at 4 years was 54.7%. Therefore, these data highlight among other factors that future treatment options for NSCLC stage III, especially in T4 or stage IIIC tumours.

Conclusions

The treatment of NSCLC stage III has changed dramatically since the introduction of neoadjuvant CT-IO. Treatment options are now open and there are multiple options that allow individualisation and personalisation of patient treatment. Neoadjuvant CT-IO is a therapy with proven efficacy and safety in multiple studies and should be considered a therapeutic option in resectable NSCLC stage IIIA and IIIB.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://cco.amegroups.com/article/view/10.21037/cco-25-50/rc

Peer Review File: Available at https://cco.amegroups.com/article/view/10.21037/cco-25-50/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://cco.amegroups.com/article/view/10.21037/cco-25-50/coif). The authors have no conflicts of interest to declare.

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