Interpretation of perioperative immunotherapy for lung cancer in 2024 WCLC/ESMO_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

LI Jiahe ^1,2 , LU Jiayu ³ , ZHANG Chenyuan ³ , FAN Ruitao ³ , ZHANG Xuxu ^1,2 , XU Xinyao ¹ , LI Guizhen ¹ , ZHANG Jipeng ¹ , LI Wei ¹ ,  LU Qiang ¹

1. Department of Thoracic Surgery, Tangdu Hospital, Air Force Medical University, Xi'an, 710038, P. R. China;
2. Shaanxi University of Chinese Medicine, Xianyang, 712046, Shaanxi, P. R. China;
3. Basic Medical College, Air Force Medical University, Xi'an, 710032, P. R. China;

Corresponding author：

LU Qiang, Email: luqiang@fmmu.edu.cn

Keywords：

Lung cancer; World Conference on Lung Cancer; European Society for Medical Oncology; perioperative treatment; immunity

DOI：

10.7507/1007-4848.202412006

Video：

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The 2024 World Conference on Lung Cancer (WCLC) and the European Society for Medical Oncology (ESMO) Annual Meeting, two of the most prestigious events in oncology, have concluded sequentially. As the most authoritative annual gatherings in lung cancer and the entire oncology field, the WCLC and ESMO conferences brought together top oncology experts and scientists from around the world to share, discuss, and publish the latest cutting-edge advancements in oncology. In both conferences, lung cancer immunotherapy remained a hot topic of considerable interest. This article aims to summarize and discuss the important research progress on perioperative immunotherapy for non-small cell lung cancer reported at the two conferences.

1.	Felip E, Altorki N, Zhou C, et al. Adjuvant atezolizumab after adjuvant chemotherapy in resected stageⅠB-ⅢA non-small-cell lung cancer (IMpower010): A randomised, multicentre, open-label, phase 3 trial. Lancet, 2021, 398(10308): 1344-1357.
2.	O'Brien M, Paz-Ares L, Marreaud S, et al. Pembrolizumab versus placebo as adjuvant therapy for completely resected stage ⅠB-ⅢA non-small-cell lung cancer (PEARLS/KEYNOTE-091): An interim analysis of a randomised, triple-blind, phase 3 trial. Lancet Oncol, 2022, 23(10): 1274-1286.
3.	Wakelee HA, Altorki NK, Zhou CC, et al. IMpower010: Final disease-free survival (DFS) and second overall survival (OS) interim results after ≥5 years of follow up of a phase Ⅲstudy of adjuvant atezolizumab vs best supportive care in resected stageⅠB-ⅢA non-small cell lung cancer (NSCLC). J Clin Oncol, 2024, 42(17_suppl): LBA8035.
4.	Felip E, Wakelee HA, Vallieres E, et al. OA01. 04 IMpower010 5-y subgroup analysis and relapse patterns: Phase 3 study of atezolizumab vs BSC in stage Ⅱ-ⅢA NSCLC. J Thorac Oncol, 2024, 19(10): S8-S9.
5.	Goss G, Darling GE, Westeel V, et al. LBA48 CCTG BR.31: A global, double-blind placebo-controlled, randomized phaseⅢstudy of adjuvant durvalumab in completely resected non-small cell lung cancer (NSCLC). Ann Oncol, 2024, 35: S1238.
6.	Chaft JE, Dahlberg SE, Khullar OV, et al. EA5142 Adjuvant nivolumab in resected lung cancers (ANVIL). J Clin Oncol, 2018, 36(15_suppl): TPS8581.
7.	Calvo V, Domine M, Sullivan V, et al. A phaseⅢclinical trial of adjuvant chemotherapy versus chemoimmunotherapy for stage ⅠB-ⅢA completely resected non-small cell lung cancer (NSCLC) patients nadim-adjuvant: New adjuvant trial of chemotherapy versus chemoimmunotherapy. J Clin Oncol, 2021, 39(15_suppl): TPS8581.
8.	Heymach JV, Harpole D, Mitsudomi T, et al. Perioperative durvalumab for resectable non-small-cell lung cancer. N Engl J Med, 2023, 389(18): 1672-1684.
9.	Soh J, Hamada A, Fujino T, et al. Perioperative therapy for non-small cell lung cancer with immune checkpoint inhibitors. Cancers (Basel), 2021, 13(16): 4035.
10.	Versluis JM, Long GV, Blank CU. Learning from clinical trials of neoadjuvant checkpoint blockade. Nat Med, 2020, 26(4): 475-484.
11.	Patel SP, Othus M, Chen Y, et al. Neoadjuvant-adjuvant or adjuvant-only pembrolizumab in advanced melanoma. N Engl J Med, 2023, 388(9): 813-823.
12.	Provencio M, Nadal E, Insa A, et al. Neoadjuvant chemotherapy and nivolumab in resectable non-small-cell lung cancer (NADIM): An open-label, multicentre, single-arm, phase 2 trial. Lancet Oncol, 2020, 21(11): 1413-1422.
13.	Provencio M, Nadal E, Insa A, et al. OA13.05 NADIM study: Updated clinical research and outcomes. J Thorac Oncol, 14(10): S241.
14.	Goldstraw P, Chansky K, Crowley J, et al. The IASLC lung cancer staging project: Proposals for revision of the TNM stage groupings in the forthcoming (eighth) edition of the TNM classification for lung cancer. J Thorac Oncol, 2016, 11(1): 39-51.
15.	Heymach JC, Harpole D, Mitsudomi T, et al. OA13.03 Perioperative durvalumab for resectable NSCLC (R-NSCLC): Updated outcomes from the phase 3 AEGEAN trial. J Thorac Oncol, 19(10): S38-S39.
16.	Spicer J, Girard N, Provencio M, et al. Neoadjuvant nivolumab (NIVO)+chemotherapy (chemo) vs chemo in patients (pts) with resectable NSCLC: 4-year update from CheckMate 816. J Clin Oncol, 42(1717_suppl): LBA8010.
17.	Spicer J, Gao S, Liberman M, et al. LBA56 Overall survival in the KEYNOTE-671 study of perioperative pembrolizumab for early-stage non-small-cell lung cancer (NSCLC). Ann Oncol, 34: S1297-S1298.
18.	Wu YL, Tsuboi M, He J, et al. Osimertinib in resected EGFR-mutated non-small-cell lung cancer. N Engl J Med, 2020, 383(18): 1711-1723.
19.	Provencio Pulla M, wad M, Cascone T, et al. LBA50 Perioperative nivolumab (NIVO) v placebo (PBO) in patients (pts) with resectable NSCLC: Clinical update from the phaseⅢCheckMate 77T study. Ann Oncol, 2024, 35: S1239-S1240.
20.	Food and Drug Administration. FDA approves neoadjuvant/adjuvant nivolumab for resectable non-small cell lung cancer. (2024-10-15) [2024-11-25].
21.	Reck M, Gale D, Zhu Z, et al. LBA49 Associations of ctDNA clearance (CL) during neoadjuvant Tx with pathological response and event-free survival (EFS) in pts with resectable NSCLC (R-NSCLC): Expanded analyses from AEGEAN. Ann Oncol, 2024, 35: S1239.
22.	Owen DH, Chaft JE, Haura EB. et al. MA15.09 LCMC3: Long-term disease-free and overall survival and their association with ctDNA after neoadjuvant atezolizumab for NSCLC. J Thorac Oncol, 2024, 19(10): S119.
23.	Jones DR, Wakelee H, Spicer JD, et al. OA01.03 Association of pathologic regression with EFS in the KEYNOTE-671 study of perioperative pembrolizumab for early-stage NSCLC. J Thorac Oncol, 19(10): S8.
24.	Deutsch JS, Cimino-Mathews A, Thompson E, et al. Association between pathologic response and survival after neoadjuvant therapy in lung cancer. Nat Med, 2024, 30(1): 218-228.
25.	Spicer J, Girard N, Provencio M, et al. Neoadjuvant nivolumab (NIVO)+chemotherapy (chemo) vs chemo in patients (pts) with resectable NSCLC: 4-year update from CheckMate 816. J Clin Oncol, 2024, 42(17_suppl): LBA8010.
26.	Zhou Y, Li A, Yu H, et al. Neoadjuvant-adjuvant vs. neoadjuvant-only PD-1 and PD-L1 inhibitors for patients with resectable NSCLC: An indirect meta-analysis. JAMA Netw Open, 2024, 7(3): e241285.
27.	Forde PM, Peters S, Donington J, et al. PL02.08 Perioperative vs neoadjuvant nivolumab for resectable NSCLC: Patient-level data analysis of CheckMate 77T vs CheckMate 816. J Thorac Oncol, 2024, 19(10): S2.
28.	Jiang J, Zhang Z, Du N, et al. EP.07C.11 Adjuvant immunotherapy for patients with resectable NSCLC after pathologic complete response. J Thorac Oncol, 19(10): S544-S545.
29.	Okami J, Shintani Y, Okumura M, et al. Demographics, safety and quality, and prognostic information in both the seventh and eighth editions of the TNM classification in 18, 973 surgical cases of the Japanese Joint Committee of Lung Cancer Registry Database in 2010. J Thorac Oncol, 2019, 14(2): 212-222.
30.	Tsutani, Y, Sakairi Y, Ikeda N, et al. 1207MO Neoadjuvant nivolumab monotherapy for high-risk clinical stageⅠ non-small cell lung cancer: A phase ⅡPOTENTIAL study. Ann Oncol, 2024, 35: S776.
31.	Lee SH, Ban Y, Park S, et al. 1216P Adjuvant pembrolizumab therapy for completely resected stageⅠNSCLC with micropapillary or solid histological subtype. Ann Oncol, 35: S783.
32.	Schuler M, Cuppens K, Plönes T, et al. Neoadjuvant nivolumab with or without relatlimab in resectable non-small-cell lung cancer: a randomized phase 2 trial. Nat Med, 2024, 30(6): 1602-1611.
33.	Cuppens K, Baas P, Wiesweg M, et al. OA01.05 Neoadjuvant nivolumab with or without relatlimab in resectable NSCLC: Additional analysis and extended follow-up. J Thorac Oncol, 19(10): S9.
34.	Wang C, Zhao X, Zhang L, et al. OA01.06 A phase Ⅱstudy of perioperative alone or combined with chemotherapy in resectable non-small cell lung cancer. J Thorac Oncol, 2024, 19(10): S10.
35.	Cascone T, Kar G, Spicer JD, et al. Neoadjuvant durvalumab alone or combined with novel immuno-oncology agents in resectable lung cancer: The phaseⅡNeoCOAST platform trial. Cancer Discov, 2023, 13(11): 2394-2411.
36.	Garassino MC, Sands J, Paz-Ares L, et al. PL02.11 Normalized membrane ratio of TROP2 by quantitative continuous scoring is predictive of clinical outcomes in TROPION-Lung 01. J Thorac Oncol, 2024, 19(10): S2-S3.
37.	Cascone T, Florian G, Bonanno L, et al. PL02.07 NeoCOAST-2: Efficacy and safety of neoadjuvant durvalumab (D)+novel anticancer agents+CT and adjuvant D±novel agents in resectable NSCLC. J Thorac Oncol, 19(10): S1-S2.
38.	LEE JM, Liao BC, Spicer J, et al. P4.07D.04 TroFuse-019: A phase 3 study of adjuvant pembrolizumab with or without sac-TMT for resectable stage Ⅱ-ⅢB (N2) NSCLC. J Thorac Oncol, 2024, 19(10): S378.

1. Felip E, Altorki N, Zhou C, et al. Adjuvant atezolizumab after adjuvant chemotherapy in resected stageⅠB-ⅢA non-small-cell lung cancer (IMpower010): A randomised, multicentre, open-label, phase 3 trial. Lancet, 2021, 398(10308): 1344-1357.
2. O'Brien M, Paz-Ares L, Marreaud S, et al. Pembrolizumab versus placebo as adjuvant therapy for completely resected stage ⅠB-ⅢA non-small-cell lung cancer (PEARLS/KEYNOTE-091): An interim analysis of a randomised, triple-blind, phase 3 trial. Lancet Oncol, 2022, 23(10): 1274-1286.
3. Wakelee HA, Altorki NK, Zhou CC, et al. IMpower010: Final disease-free survival (DFS) and second overall survival (OS) interim results after ≥5 years of follow up of a phase Ⅲstudy of adjuvant atezolizumab vs best supportive care in resected stageⅠB-ⅢA non-small cell lung cancer (NSCLC). J Clin Oncol, 2024, 42(17_suppl): LBA8035.
4. Felip E, Wakelee HA, Vallieres E, et al. OA01. 04 IMpower010 5-y subgroup analysis and relapse patterns: Phase 3 study of atezolizumab vs BSC in stage Ⅱ-ⅢA NSCLC. J Thorac Oncol, 2024, 19(10): S8-S9.
5. Goss G, Darling GE, Westeel V, et al. LBA48 CCTG BR.31: A global, double-blind placebo-controlled, randomized phaseⅢstudy of adjuvant durvalumab in completely resected non-small cell lung cancer (NSCLC). Ann Oncol, 2024, 35: S1238.
6. Chaft JE, Dahlberg SE, Khullar OV, et al. EA5142 Adjuvant nivolumab in resected lung cancers (ANVIL). J Clin Oncol, 2018, 36(15_suppl): TPS8581.
7. Calvo V, Domine M, Sullivan V, et al. A phaseⅢclinical trial of adjuvant chemotherapy versus chemoimmunotherapy for stage ⅠB-ⅢA completely resected non-small cell lung cancer (NSCLC) patients nadim-adjuvant: New adjuvant trial of chemotherapy versus chemoimmunotherapy. J Clin Oncol, 2021, 39(15_suppl): TPS8581.
8. Heymach JV, Harpole D, Mitsudomi T, et al. Perioperative durvalumab for resectable non-small-cell lung cancer. N Engl J Med, 2023, 389(18): 1672-1684.
9. Soh J, Hamada A, Fujino T, et al. Perioperative therapy for non-small cell lung cancer with immune checkpoint inhibitors. Cancers (Basel), 2021, 13(16): 4035.
10. Versluis JM, Long GV, Blank CU. Learning from clinical trials of neoadjuvant checkpoint blockade. Nat Med, 2020, 26(4): 475-484.
11. Patel SP, Othus M, Chen Y, et al. Neoadjuvant-adjuvant or adjuvant-only pembrolizumab in advanced melanoma. N Engl J Med, 2023, 388(9): 813-823.
12. Provencio M, Nadal E, Insa A, et al. Neoadjuvant chemotherapy and nivolumab in resectable non-small-cell lung cancer (NADIM): An open-label, multicentre, single-arm, phase 2 trial. Lancet Oncol, 2020, 21(11): 1413-1422.
13. Provencio M, Nadal E, Insa A, et al. OA13.05 NADIM study: Updated clinical research and outcomes. J Thorac Oncol, 14(10): S241.
14. Goldstraw P, Chansky K, Crowley J, et al. The IASLC lung cancer staging project: Proposals for revision of the TNM stage groupings in the forthcoming (eighth) edition of the TNM classification for lung cancer. J Thorac Oncol, 2016, 11(1): 39-51.
15. Heymach JC, Harpole D, Mitsudomi T, et al. OA13.03 Perioperative durvalumab for resectable NSCLC (R-NSCLC): Updated outcomes from the phase 3 AEGEAN trial. J Thorac Oncol, 19(10): S38-S39.
16. Spicer J, Girard N, Provencio M, et al. Neoadjuvant nivolumab (NIVO)+chemotherapy (chemo) vs chemo in patients (pts) with resectable NSCLC: 4-year update from CheckMate 816. J Clin Oncol, 42(1717_suppl): LBA8010.
17. Spicer J, Gao S, Liberman M, et al. LBA56 Overall survival in the KEYNOTE-671 study of perioperative pembrolizumab for early-stage non-small-cell lung cancer (NSCLC). Ann Oncol, 34: S1297-S1298.
18. Wu YL, Tsuboi M, He J, et al. Osimertinib in resected EGFR-mutated non-small-cell lung cancer. N Engl J Med, 2020, 383(18): 1711-1723.
19. Provencio Pulla M, wad M, Cascone T, et al. LBA50 Perioperative nivolumab (NIVO) v placebo (PBO) in patients (pts) with resectable NSCLC: Clinical update from the phaseⅢCheckMate 77T study. Ann Oncol, 2024, 35: S1239-S1240.
20. Food and Drug Administration. FDA approves neoadjuvant/adjuvant nivolumab for resectable non-small cell lung cancer. (2024-10-15) [2024-11-25].
21. Reck M, Gale D, Zhu Z, et al. LBA49 Associations of ctDNA clearance (CL) during neoadjuvant Tx with pathological response and event-free survival (EFS) in pts with resectable NSCLC (R-NSCLC): Expanded analyses from AEGEAN. Ann Oncol, 2024, 35: S1239.
22. Owen DH, Chaft JE, Haura EB. et al. MA15.09 LCMC3: Long-term disease-free and overall survival and their association with ctDNA after neoadjuvant atezolizumab for NSCLC. J Thorac Oncol, 2024, 19(10): S119.
23. Jones DR, Wakelee H, Spicer JD, et al. OA01.03 Association of pathologic regression with EFS in the KEYNOTE-671 study of perioperative pembrolizumab for early-stage NSCLC. J Thorac Oncol, 19(10): S8.
24. Deutsch JS, Cimino-Mathews A, Thompson E, et al. Association between pathologic response and survival after neoadjuvant therapy in lung cancer. Nat Med, 2024, 30(1): 218-228.
25. Spicer J, Girard N, Provencio M, et al. Neoadjuvant nivolumab (NIVO)+chemotherapy (chemo) vs chemo in patients (pts) with resectable NSCLC: 4-year update from CheckMate 816. J Clin Oncol, 2024, 42(17_suppl): LBA8010.
26. Zhou Y, Li A, Yu H, et al. Neoadjuvant-adjuvant vs. neoadjuvant-only PD-1 and PD-L1 inhibitors for patients with resectable NSCLC: An indirect meta-analysis. JAMA Netw Open, 2024, 7(3): e241285.
27. Forde PM, Peters S, Donington J, et al. PL02.08 Perioperative vs neoadjuvant nivolumab for resectable NSCLC: Patient-level data analysis of CheckMate 77T vs CheckMate 816. J Thorac Oncol, 2024, 19(10): S2.
28. Jiang J, Zhang Z, Du N, et al. EP.07C.11 Adjuvant immunotherapy for patients with resectable NSCLC after pathologic complete response. J Thorac Oncol, 19(10): S544-S545.
29. Okami J, Shintani Y, Okumura M, et al. Demographics, safety and quality, and prognostic information in both the seventh and eighth editions of the TNM classification in 18, 973 surgical cases of the Japanese Joint Committee of Lung Cancer Registry Database in 2010. J Thorac Oncol, 2019, 14(2): 212-222.
30. Tsutani, Y, Sakairi Y, Ikeda N, et al. 1207MO Neoadjuvant nivolumab monotherapy for high-risk clinical stageⅠ non-small cell lung cancer: A phase ⅡPOTENTIAL study. Ann Oncol, 2024, 35: S776.
31. Lee SH, Ban Y, Park S, et al. 1216P Adjuvant pembrolizumab therapy for completely resected stageⅠNSCLC with micropapillary or solid histological subtype. Ann Oncol, 35: S783.
32. Schuler M, Cuppens K, Plönes T, et al. Neoadjuvant nivolumab with or without relatlimab in resectable non-small-cell lung cancer: a randomized phase 2 trial. Nat Med, 2024, 30(6): 1602-1611.
33. Cuppens K, Baas P, Wiesweg M, et al. OA01.05 Neoadjuvant nivolumab with or without relatlimab in resectable NSCLC: Additional analysis and extended follow-up. J Thorac Oncol, 19(10): S9.
34. Wang C, Zhao X, Zhang L, et al. OA01.06 A phase Ⅱstudy of perioperative alone or combined with chemotherapy in resectable non-small cell lung cancer. J Thorac Oncol, 2024, 19(10): S10.
35. Cascone T, Kar G, Spicer JD, et al. Neoadjuvant durvalumab alone or combined with novel immuno-oncology agents in resectable lung cancer: The phaseⅡNeoCOAST platform trial. Cancer Discov, 2023, 13(11): 2394-2411.
36. Garassino MC, Sands J, Paz-Ares L, et al. PL02.11 Normalized membrane ratio of TROP2 by quantitative continuous scoring is predictive of clinical outcomes in TROPION-Lung 01. J Thorac Oncol, 2024, 19(10): S2-S3.
37. Cascone T, Florian G, Bonanno L, et al. PL02.07 NeoCOAST-2: Efficacy and safety of neoadjuvant durvalumab (D)+novel anticancer agents+CT and adjuvant D±novel agents in resectable NSCLC. J Thorac Oncol, 19(10): S1-S2.
38. LEE JM, Liao BC, Spicer J, et al. P4.07D.04 TroFuse-019: A phase 3 study of adjuvant pembrolizumab with or without sac-TMT for resectable stage Ⅱ-ⅢB (N2) NSCLC. J Thorac Oncol, 2024, 19(10): S378.

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